ForShira,Eytan,Noam,andShani

TableofContentsTitlePagePrologue

ONE-WhataPlantSeesDarwintheBotanistMarylandMammoth:TheTobaccoThatJustKeptGrowingWhataDifferencea(Short)DayMakesBlindPlantsintheAgeofGeneticsWhatPlantsandHumansSee

TWO-WhataPlantSmellsUnexplainedPhenomenaFindingFood(L)eavesdroppingDoPlantsSmell?

THREE-WhataPlantFeelsVenus’sTrapWaterPowerANegativeTouchPlantandHumanFeeling

FOUR-WhataPlantHearsRock-and-RollBotanyDeafGenesTheDeafPlant

FIVE-HowaPlantKnowsWhereItIsKnowingUpfromDownTheMovementHormoneDancingPlantsTheBalancedPlant

SIX-WhataPlantRemembersTheShort-TermMemoryoftheVenusFlytrapLong-TermMemoryofTrauma

TheBigChillInEveryGeneration…IntelligentMemory?

Epilogue:TheAwarePlant

NotesAcknowledgmentsIndexILLUSTRATIONCREDITSANOTEABOUTTHEAUTHORNotesCopyrightPage

PrologueMyinterestintheparallelsbetweenplantandhumansensesgotitsstartwhenIwasayoungpostdoctoralfellowatYaleUniversityinthe1990s.Iwasinterestedinstudyingabiologicalprocessspecifictoplantsandnotconnected to human biology (probably as a response to the six otherdoctorsinmyfamily,allofwhomarephysicians).HenceIwasdrawntothequestionofhowplantsuselighttoregulatetheirdevelopment.Inmyresearch I discovered a unique group of genes necessary for a plant todetermine if it’s in the light or in the dark.Much to my surprise andagainstallofmyplans,IlaterdiscoveredthatthissamegroupofgenesisalsopartofthehumanDNA.Thisledtotheobviousquestionastowhatthese seemingly “plant-specific” genes do in people. Many years laterand after much research we now know that these genes not only areconserved between plants and animals but also regulate (among otherdevelopmentalprocesses)responsestolightinboth!This ledme to realize that thegenetic differencebetweenplants and

animals isnotassignificantasIhadoncebelieved.Ibegantoquestiontheparallelsbetweenplantandhumanbiologyevenasmyownresearchevolvedfromstudyingplantresponsestolighttoleukemiainfruitflies.WhatIdiscoveredwasthatwhilethere’snoplantthatknowshowtosay“Feedme,Seymour!”therearemanyplantsthat“know”quiteabit.Indeed, we tend not to pay much attention to the immensely

sophisticated sensory machinery in the flowers and trees that can befoundright inourownbackyards.Whilemostanimalscanchoose theirenvironments, seek shelter in a storm, search for food and a mate, ormigratewiththechangingseasons,plantsmustbeabletowithstandandadapt to constantly changing weather, encroaching neighbors, andinvading pests, without being able to move to a better environment.Because of this, plants have evolved complex sensory and regulatorysystems that allow them tomodulate their growth in response to ever-changingconditions.Anelmtreehastoknowifitsneighborisshadingitfrom the sun so that it can find its ownway to grow toward the light

that’s available. A head of lettuce has to know if there are ravenousaphidsabouttoeatitupsothatitcanprotectitselfbymakingpoisonouschemicals tokill thepests.ADouglas fir treehas toknow ifwhippingwinds are shaking its branches so that it can grow a stronger trunk.Cherrytreeshavetoknowwhentoflower.Onagenetic level, plants aremorecomplex thanmanyanimals, and

some of the most important discoveries in all of biology came fromresearch carried out on plants. Robert Hooke first discovered cells in1665 while studying cork in the early microscope he built. In thenineteenthcenturyGregorMendelworkedout theprinciplesofmoderngenetics using pea plants, and in the mid-twentieth century BarbaraMcClintockusedIndiancorntoshowthatgenescantranspose,orjump.Wenowknowthatthese“jumpinggenes”areacharacteristicofallDNAand are intimately connected to cancer in humans. And while werecognize that Darwin was a founding father of modern evolutionarytheory, some of his most important findings were inplant biologyspecifically,andwe’llseequiteafewoftheseinthepagesofthisbook.Clearly,myuseoftheword“know”isunorthodox.Plantsdon’thavea

central nervous system; a plant doesn’t have a brain that coordinatesinformation for its entire body. Yet different parts of a plant areintimately connected, and information regarding light, chemicals in theair, and temperature is constantly exchanged between roots and leaves,flowersandstems,toyieldaplantthatisoptimizedforitsenvironment.Wecan’tequatehumanbehaviortothewaysinwhichplantsfunctionintheir worlds, but I ask that you humor me while I use terminologythroughoutthebookthatisusuallyreservedforhumanexperience.WhenIexplorewhataplantseesorwhatitsmells,Iamnotclaimingthatplantshaveeyesornoses(orabrainthatcolorsallsensoryinputwithemotion).ButIbelievethisterminologywillhelpchallengeustothinkinnewwaysaboutsight,smell,whataplantis,andultimatelywhatweare.My book is notThe Secret Life of Plants; if you’re looking for an

argument that plants are just like us, you won’t find it here. As therenowned plant physiologist Arthur Galston pointed out back in 1974during theheightof interest in thisextremelypopularbut scientifically

anemic book, we must be wary of “bizarre claims presented withoutadequate supporting evidence.” Worse than leading the unwary readerastray,The Secret Life of Plants led to scientific fallout that stymiedimportant research on plant behavior as scientists becamewary of anystudiesthathintedatparallelsbetweenanimalsensesandplantsenses.InthemorethanthreedecadessinceTheSecretLifeofPlantscauseda

greatmedia stir, the depth atwhich scientists understand plant biologyhasincreasedimmensely.InWhataPlantKnows,Iwillexplorethelatestresearchinplantbiologyandarguethatplantsdoindeedhavesenses.Bynomeansisthisbookanexhaustiveandcompletereviewofwhatmodernsciencehas tosayaboutplant senses; thatwouldnecessitatea textbookinaccessibletoallbutthemostdedicatedreaders.Instead,ineachchapterIhighlightahumansenseandcomparewhatthesenseisforpeopleandwhatitisforplants.Idescribehowthesensoryinformationisperceived,how it is processed, and the ecological implications of the sense for aplant.AndineachchapterI’llpresentbothahistoricalperspectiveandamodern look at the topic. I’ve chosen to cover sight, feeling, hearing,proprioception,andmemory,andwhileI’lldevoteachaptertosmell,I’mnotfocusingontastehere—thetwosensesareintimatelyconnected.We are utterly dependent on plants.Wewake up in housesmade of

woodfromtheforestsofMaine,pouracupofcoffeebrewedfromcoffeebeansgrowninBrazil,throwonaT-shirtmadeofEgyptiancotton,printoutareportonpaper,anddriveourkidstoschoolincarswithtiresmadeofrubber thatwasgrowninAfricaandfueledbygasolinederivedfromcycads thatdiedmillionsofyearsago.Chemicalsextractedfromplantsreduce fever (think of aspirin) and treat cancer (Taxol).Wheat sparkedtheendofoneageandthedawnofanother,andthehumblepotatoledtomassmigrations.Andplantscontinuetoinspireandamazeus:themightysequoiasare the largest singular, independentorganismsonearth,algaearesomeofthesmallest,androsesdefinitelymakeanyonesmile.Knowing what plants do for us, why not take a moment to find out

moreaboutwhatscientistshavefoundoutaboutthem?Let’sembarkonourjourneytoexplorethesciencebehindtheinnerlivesofplants.We’llstart by uncoveringwhat plants really seewhile they’re hanging out in

thebackyard.

ONEWhataPlantSees

Sheturns,always,towardsthesun,thoughherrootsholdherfast,and,altered,lovesunaltered.

—Ovid,MetamorphosesThinkaboutthis:plantsseeyou.Infact,plantsmonitortheirvisibleenvironmentallthetime.Plantssee

ifyoucomenearthem;theyknowwhenyoustandoverthem.Theyevenknowifyou’rewearingablueoraredshirt.Theyknowifyou’vepaintedyourhouseorifyou’vemovedtheirpotsfromonesideofthelivingroomtotheother.Of course plants don’t “see” in pictures as you or I do. Plants can’t

discernbetween a slightly baldingmiddle-agedmanwithglasses and asmiling littlegirlwithbrowncurls.But theydosee light inmanywaysandcolorsthatwecanonlyimagine.Plantsseethesameultravioletlightthatgivesussunburnsandinfraredlightthatheatsusup.Plantscantellwhenthere’sverylittlelight,likefromacandle,orwhenit’sthemiddleoftheday,orwhenthesunisabouttosetintothehorizon.Plantsknowifthelightiscomingfromtheleft,theright,orfromabove.Theyknowifanotherplanthasgrownover them,blockingtheir light.Andtheyknowhowlongthelightshavebeenon.So, can this be considered “plant vision”? Let’s first examine what

vision is for us. Imagine a person born blind, living in total darkness.Nowimaginethispersonbeinggiventheabilitytodiscriminatebetweenlightandshadow.Thispersoncoulddifferentiatebetweennightandday,inside and outside. These new senses would definitely be consideredrudimentarysightandwouldenablenewlevelsoffunction.Nowimagine

thispersonbeingabletodiscerncolor.Shecanseeblueaboveandgreenbelow.Ofcoursethiswouldbeawelcomeimprovementoverdarknessorbeingabletodiscernonlywhiteorgray.Ithinkwecanallagreethatthisfundamentalchange—fromtotalblindnesstoseeingcolor—isdefinitely“vision”forthisperson.Merriam-Webster’s defines “sight” as “the physical sense by which

light stimuli received by the eye are interpreted by the brain andconstructed into a representation of the position, shape, brightness, andusuallycolorofobjectsinspace.”Weseelightinwhatwedefineasthe“visual spectra.” Light is a common, understandable synonym for theelectromagneticwavesinthevisiblespectrum.Thismeansthatlighthaspropertiessharedwithallothertypesofelectricalsignals,suchasmicro-andradiowaves.RadiowavesforAMradioareverylong,almosthalfamile in length. That’s why radio antennas are many stories tall. Incontrast,X-raywavesarevery,veryshort,onetrilliontimesshorterthanradiowaves,whichiswhytheypasssoeasilythroughourbodies.Light waves are somewhere in the middle, between 0.0000004 and

0.0000007meter long. Blue light is the shortest, while red light is thelongest,with green, yellow, and orange in themiddle. (That’swhy thecolorpatternofrainbowsisalwaysorientedinthesamedirection—fromthecolorswithshortwaves,likeblue,tothecolorswithlongwaves,likered.) These are the electromagnetic waves we “see” because our eyeshavespecialproteinscalledphotoreceptorsthatknowhowtoreceivethisenergy,toabsorbit,thesamewaythatanantennaabsorbsradiowaves.Theretina,thelayeratthebackofoureyeballs,iscoveredwithrows

and rowsof these receptors, sort of like the rows and rowsofLEDs inflat-screen televisions or sensors in digital cameras. Each point on theretinahasphotoreceptorscalledrods,whicharesensitivetoalllight,andphotoreceptors called cones,which respond to different colors of light.Eachconeor rod responds to the light focusedon it.Thehuman retinacontainsabout125millionrodsand6millioncones,allinanareaaboutthesizeofapassportphoto.That’sequivalenttoadigitalcamerawitharesolution of 130megapixels.This huge number of receptors in such asmall area gives us our high visual resolution. For comparison, the

highest-resolutionoutdoorLEDdisplayscontainonlyabout10,000LEDspersquaremeter,andcommondigitalcamerashavearesolutionofonlyabout8megapixels.Rodsaremoresensitivetolightandenableustoseeatnightandunder

low-light conditions but not in color. Cones allow us to see differentcolorsinbrightlightsinceconescomeinthreeflavors—red,green,andblue.Themajordifferencebetweenthesedifferentphotoreceptorsisthespecificchemicaltheycontain.Thesechemicals,calledrhodopsininrodsand photopsins in cones, have a specific structure that enables them toabsorblightofdifferentwavelengths.Bluelightisabsorbedbyrhodopsinand the blue photopsin; red light by rhodopsin and the red photopsin.Purplelightisabsorbedbyrhodopsin,bluephotopsin,andredphotopsin,butnot green photopsin, and so on. Once the rod or cone absorbs thelight, itsendsasignaltothebrainthatprocessesallofthesignalsfromthemillionsofphotoreceptorsintoasinglecoherentpicture.Blindnessresultsfromdefectsatmanystages:fromlightperceptionby

theretinaduetoaphysicalprobleminitsstructure;fromtheinabilitytosensethelight(becauseofproblemsintherhodopsinandphotopsins,forexample);orintheabilitytotransfertheinformationtothebrain.Peoplewhoarecolor-blindforred,forexample,don’thaveanyredcones.Thustheredsignalsarenotabsorbedandpassedontothebrain.Humansightinvolves cells that absorb the light, and the brain then processes thisinformation,whichweinturnrespondto.Sowhathappensinplants?

DarwintheBotanistIt’snotwidelyknownthatforthetwentyyearsfollowinghispublicationof the landmarkOn theOrigin of Species,CharlesDarwin conducted aseriesofexperimentsthatstillinfluenceresearchinplantstothisday.Darwinwasfascinatedbytheeffectsof lightonplantgrowth,aswas

his son Francis. In his final book,The Power of Movement in Plants,Darwinwrote:“Thereareextremelyfew[plants],ofwhichsomepart…

doesnotbend toward lateral light.”Or in lessverbosemodernEnglish:almost all plants bend toward light.We see that happen all the time inhouseplants thatbowandbend toward raysofsunshinecoming in fromthe window. This behavior is called phototropism. In 1864 acontemporaryofDarwin’s,JuliusvonSachs,discoveredthatbluelightisthe primary color that induces phototropism in plants,while plants aregenerally blind to other colors that have little effect on theirbendingtowardlight.Butnooneknewatthattimehoworwhichpartofaplantseesthelightcomingfromaparticulardirection.In a very simple experiment, Darwin and his son showed that this

bendingwasduenot tophotosynthesis, theprocesswherebyplants turnlightintoenergy,butrathertosomeinherentsensitivitytomovetowardlight.Fortheirexperiment,thetwoDarwinsgrewapotofcanarygrassinatotallydarkroomforseveraldays.Thentheylitaverysmallgaslamptwelvefeetfromthepotandkept itsodimthat they“couldnotsee theseedlingsthemselves,norseeapencillineonpaper.”Butafteronlythreehours,theplantshadobviouslycurvedtowardthedimlight.Thecurvingalwaysoccurredatthesamepartoftheyoungplant,aninchorsobelowthetip.

Canarygrass(Phalariscanariensis)

This led them to questionwhich part of the plant saw the light. TheDarwins carried out what has become a classic experimentin botany.Theyhypothesizedthatthe“eyes”oftheplantwerefoundattheseedlingtip andnot at the part of the seedling that bends. They checkedphototropism in five different seedlings, illustrated by the followingdiagram:

SummaryofDarwin’sexperimentsonphototropism

a.Thefirstseedlingwasuntreatedandshowsthattheconditionsoftheexperimentareconducivetophototropism.

b.Thesecondhaditstipprunedoff.c.Thethirdhaditstipcoveredwithalightproofcap.d.Thefourthhaditstipcoveredwithaclearglasscap.e.Thefifthhaditsmiddlesectioncoveredbyalightprooftube.

They carried out the experiment on these seedlings in the sameconditions as their initial experiment, and of course the untreatedseedlingbenttowardthelight.Similarly,theseedlingwiththelightprooftube around its middle (seee above) bent toward the light. If theyremoved thetip of a seedling, however, or covered itwith a lightproofcap,itwentblindandcouldn’tbendtowardthelight.Thentheywitnessedthebehaviorof theplantinscenariofour(d): thisseedlingcontinuedtobendtowardthelighteventhoughithadacaponitstip.Thedifferenceherewasthatthecapwasclear.TheDarwinsrealizedthattheglassstillallowed the light to shine onto the tip of the plant. In one simpleexperiment,publishedin1880,thetwoDarwinsprovedthatphototropismistheresultoflighthittingthetipofaplant’sshoot,whichseesthelightandtransfersthisinformationtotheplant’smidsectiontotellittobendin that direction. The Darwins had successfully demonstratedrudimentarysightinplants.

MarylandMammoth:TheTobaccoThatJustKeptGrowing

Severaldecades later,anewtobaccostraincroppedup in thevalleysofsouthernMarylandandreignited interest in theways thatplantssee theworld. These valleys have been home to some of America’s greatesttobaccofarmssincethefirstsettlersarrivedattheendoftheseventeenthcentury. Tobacco farmers, learning from the Native tribes such as theSusquehannock,whohadgrowntobaccoforcenturies,wouldplant their

crop in the spring and harvest it in late summer. Some of the plantsweren’t harvested for their leaves and made flowers that provided theseed for the next year’s crop. In 1906, farmers began to notice a newstrainoftobaccothatneverseemedtostopgrowing.Itcouldreachfifteenfeet in height, produce almost a hundred leaves, and would only stopgrowing when the frosts set in. On the surface, such a robust, ever-growingplantwouldseemaboontotobaccofarmers.Butasissooftenthecase,thisnewstrain,aptlynamedMarylandMammoth,waslikethetwo-facedRomangodJanus.Ontheonehand,itneverstoppedgrowing;on the other,it rarely flowered,meaning farmers couldn’t harvest seedforthenextyear’scrop.

Tobacco(Nicotianatabacum)

In1918,WightmanW.Garner andHarryA.Allard, two scientists at

theU.S.DepartmentofAgriculture,setout todeterminewhyMarylandMammoth didn’t know when to stop making leaves and start makingflowersandseedsinstead.TheyplantedtheMarylandMammothinpotsand leftonegroupoutside in the fields.Theothergroupwasput in thefield during the day butmoved to a dark shed every afternoon.SimplylimitingtheamountoflighttheplantssawwasenoughtocauseMarylandMammoth to stop growing and start flowering. In other words, ifMarylandMammothwasexposed to the longdaysof summer, itwouldkeepgrowingleaves.Butifitexperiencedartificiallyshorterdays,thenitwouldflower.This phenomenon, called photoperiodism, gave us the first strong

evidence that plants measure how much light they take in. Otherexperimentsover theyearshaverevealedthatmanyplants, just liketheMammoth,floweronlyifthedayisshort;theyarereferredtoas“short-day” plants. Such short-day plants include chrysanthemums andsoybeans. Someplants need a long day to flower; irises and barley areconsidered “long-day” plants. This discoverymeant that farmers couldnowmanipulate flowering to fit their schedulesbycontrolling the lightthataplantsees.It’snotsurprisingthatfarmersinFloridasoonfiguredoutthattheycouldgrowMarylandMammothformanymonths(withoutthe effects of frost encountered inMaryland) and that theplantswouldeventuallyflowerinthefieldsinmidwinterwhenthedayswereshortest.

WhataDifferencea(Short)DayMakesThe concept of photoperiodism sparked a rush of activity amongscientists who were brimming with follow-up questions: Do plantsmeasure the lengthof thedayor thenight?Andwhatcolorof lightareplantsseeing?AroundthetimeofWorldWarII,scientistsdiscoveredthattheycould

manipulatewhenplantsfloweredsimplybyquicklyturningthelightsonandoffinthemiddleofthenight.Theycouldtakeashort-dayplantlike

thesoybeanandkeepitfrommakingflowersinshortdaysiftheyturnedon the lights foronly a fewminutes in themiddleof thenight.On theother hand, the scientists could cause a long-day plant like the iris tomakeflowerseveninthemiddleofthewinter(duringshortdays,whenitshouldn’tnormallyflower), if in themiddleof thenight they turnedonthelightsforjustafewmoments.Theseexperimentsprovedthatwhataplant measures is not the length of theday but the length of thecontinuousperiodofdarkness.Using this technique, flower farmers cankeep chrysanthemums from

flowering until just beforeMother’sDay,which is the optimal time tohave themburst onto the spring flower scene.Chrysanthemum farmershaveaproblemsinceMother’sDaycomesinthespringbuttheflowersnormally blossom in the fall as the days get shorter. Fortunately,chrysanthemums grown in greenhouses can be kept from flowering byturningon the lights for a fewminutes at night throughout the fall andwinter. Then …boom… twoweeks beforeMother’s Day, the farmersstop turning on the lights at night, and all the plants start to flower atonce,readyforharvestandshipping.These scientistswere curious about the color of light that the plants

saw.Whattheydiscoveredwassurprising:theplants,anditdidn’tmatterwhichonesweretested,onlyrespondedtoaflashofredduringthenight.Blueorgreenflashesduringthenightwouldn’tinfluencewhentheplantflowered, but only a few seconds ofred would. Plants weredifferentiatingbetweencolors:theywereusingbluelighttoknowwhichdirectiontobendinandredlighttomeasurethelengthofthenight.Then, in the early 1950s, Harry Borthwick and his colleagues in the

USDA lab where Maryland Mammoth was first studied made theamazingdiscoverythatfar-redlight—lightthathaswavelengthsthatareabitlongerthanbrightredandismostoftenseen,justbarely,atdusk—could cancel the effect of the red light on plants.Letme spell this outmore clearly: if you takeirises, which normally don’t flower in longnights,andgivethemashotofredlightinthemiddleofthenight,they’llmakeflowersasbrightandasbeautifulasanyiris inanaturepreserve.Butifyoushinefar-redlightonthemrightafterthepulseofred,it’sasif

theyneversawtheredlighttobeginwith.Theywon’tflower.Ifyouthenshinered lighton themafter thefar-red, theywill.Hit themagainwithfar-redlight,andtheywon’t.Andsoon.We’realsonottalkingaboutlotsoflight;afewsecondsofeithercolorisenough.It’slikealight-activatedswitch:Theredlightturnsonflowering;thefar-redlightturnsitoff.Ifyou flip the switch back and forth fast enough, nothing happens. On amore philosophical level,we can say that the plant remembers the lastcoloritsaw.BythetimeJohnF.Kennedywaselectedpresident,WarrenL.Butler

andcolleagueshaddemonstratedthatasinglephotoreceptorinplantswasresponsible for both the red and the far-red effects. They called thisreceptor “phytochrome,” meaning “plant color.” In its simplest model,phytochrome is the light-activated switch. Red light activatesphytochrome,turningitintoaformprimedtoreceivefar-redlight.Far-red light inactivates phytochrome, turning it into a form primed toreceive red light.Ecologically, thismakes a lot of sense. Innature, thelastlightanyplantseesattheendofthedayisfar-red,andthissignifiestotheplantthatitshould“turnoff.”Inthemorning,itseesredlightanditwakesup. In thisway aplantmeasureshow long ago it last saw redlightandadjustsitsgrowthaccordingly.Exactlywhichpartoftheplantseestheredandfar-redlighttoregulateflowering?Weknow fromDarwin’s studies of phototropism that the “eye” of a

plantisinitstipwhiletheresponsetothelightoccursinthestem.Sowemightconclude,then,thatthe“eye”forphotoperiodismisalsointhetipoftheplant.Surprisingly,thisisn’tthecase.Ifinthemiddleofthenightyoushineabeamoflightondifferentpartsoftheplant,youdiscoverthatit’ssufficienttoilluminateanysingleleafinordertoregulatefloweringintheentireplant.Ontheotherhand,ifalltheleavesarepruned,leavingonlythestemandtheapex,theplantisblindtoanyflashesoflight,eveniftheentireplantisilluminated.Ifthephytochromeinasingleleafseesred light in the middle of the night, it’s as if the entire plant wereilluminated. Phytochrome in the leaves receives the light cues andinitiatesamobilesignalthatpropagatesthroughouttheplantandinducesflowering.

BlindPlantsintheAgeofGeneticsWehavefourdifferenttypesofphotoreceptorsinoureyes:rhodopsinforlightandshadows,andthreephotopsinsforred,blue,andgreen.Wealsohaveafifthlightreceptorcalledcryptochromethatregulatesourinternalclocks.Sofarwe’veseen thatplantsalsohavemultiplephotoreceptors:they seedirectionalblue light,whichmeans theymusthaveat lastoneblue-lightphotoreceptor,nowknownasphototropin,andtheyseeredandfar-red light for flowering, which points to at least one phytochromephotoreceptor.But in order to determine just howmanyphotoreceptorsplants possess, scientists had towait for the era ofmolecular genetics,whichbeganseveraldecadesafterthediscoveryofphytochrome.Theapproachspearheadedintheearly1980sbyMaartenKoornneefat

WageningenUniversityinHolland,andrepeatedandrefinedinnumerouslabs, used genetics to understand plantsight.Koornneef asked a simplequestion:Whatwoulda“blind”plantlooklike?Plantsgrownindarknessordimlightaretaller thanthosegrowninbright light.Ifyouever tookcare of bean sprouts for a sixth-grade science experiment, you’d knowthattheplantsinthehallclosetgrewuptall,spindly,andyellow,buttheonesoutontheplaygroundwereshort,vigorous,andgreen.Thismakessensebecauseplantsnormallyelongateindarkness,whenthey’retryingtogetoutofthesoilintothelightorwhenthey’reintheshadeandneedtomake theirway to the unobstructed light. IfKoornneef could find ablindmutantplant,perhapsitwouldbetallinbrightlightaswell.Ifhecould identify and grow blind mutant plants, he would be able to usegeneticstofigureoutwhatwaswrongwiththem.He carried out his experiments onArabidopsis thaliana, a small

laboratory plant similar to wild mustard. He treated a batch ofarabidopsis seeds with chemicals known to induce mutations in DNA(and also cause cancer in laboratory rats) and then grew the seedlingsundervariouscolorsof light and looked formutant seedlings thatweretallerthantheothers.Hefoundmanyofthem.Someofthemutantplantsgrewtallerunderbluelight,butwereofnormalheightwhengrownunderredlight.Someweretallerunderredlightbutnormalunderblue.Some

were taller underUV light but normal under all other kinds, and somewere taller under redandblue lights.Afewwere talleronlyunderdimlight,whileothersweretalleronlyunderbright-lightconditions.Manyofthesemutantsthatwereblindtospecificcolorsoflightwere

defective in the particular photoreceptors that absorb the light.A plantthat had no phytochrome grew in red light as if it were in the dark.Surprisingly, a fewof thephotoreceptorscame inpairs,withonebeingspecific for dim light and theotherspecific forbright light.Tomakealongandcomplexstoryshort,wenowknowthatarabidopsishasatleasteleven different photoreceptors: some tell a plant when to germinate,some tell itwhen tobend to the light, some tell itwhen to flower, andsome let it know when it’s nighttime. Some let the plant know thatthere’salotoflighthittingit,someletitknowthatthelightisdim,andsomehelpitkeeptime.1

Arabidopsis(Arabidopsisthaliana)

Soplantvisionismuchmorecomplexthanhumansightatthelevelofperception.Indeed,lightforaplantismuchmorethanasignal; lightisfood.Plantsuselighttoturnwaterandcar-bondioxideintosugarsthatinturn provide food for all animals. But plants are sessile, unmovingorganisms as well. They are literally rooted in one place, unable tomigrateinsearchoffood.Tocompensateforthissessilelife,plantsmusthave the ability to find their food—to seek out and capture light. Thatmeans they need to know where the light is, and rather than movingtowardthefood,asananimalwould,aplantgrowstowarditsfood.Aplantneedstoknowifanotherplanthasgrownaboveit,filteringout

thelightforphotosynthesis.Ifaplantsensesthatitisintheshade,itwillstartgrowingfastertogetout.Andplantsneedtosurvive,whichmeansthey need to know when to “hatch” out of their seeds and when toreproduce.Manytypesofplantsstartgrowinginthespring,justasmanymammals give birth then. How do plants know when the spring hasstarted?Phytochrome tells them that the days are getting progressivelylonger.Plantsalsoflowerandsetseedinthefallbeforethesnowcomes.Howdo theyknowit’sautumn?Phytochrome tells themthat thenightsaregettinglonger.

WhatPlantsandHumansSeePlantsmustbeawareofthedynamicvisualenvironmentaroundtheminordertosurvive.Theyneedtoknowthedirection,amount,duration,andcolorof light todoso.Plantsundoubtedlydetectvisible (and invisible)electromagneticwaves.Whilewecandetectelectromagneticwavesinarelatively tight spectrum, plants detect ones that are both shorter andlonger than those we can detect. Although plants see a much largerspectrum than we do, they don’t see in pictures. Plants don’t have anervous system that translates light signals into pictures. Instead, theytranslatelight signals into different cues for growth. Plants don’t haveeyes,justaswedon’thaveleaves.2

Butwecanbothdetectlight.Sight is the ability not only todetect electromagneticwavesbut also

the ability torespond to thesewaves.Therodsandcones inour retinasdetect thelightsignalandtransfer this informationto thebrain,andwerespond to the information. Plants are also able to translate the visualsignal into a physiologically recognizable instruction. Itwasn’t enoughthatDarwin’s plants saw the light in their tips; they had to absorb thislightandthensomehowtranslateitintoaninstructionthattoldtheplanttobend.Theyneededtorespondtothelight.Thecomplexsignalsarisingfrom multiple photoreceptors allow a plant to optimally modulate itsgrowth inchangingenvironments, just asour fourphotoreceptorsallowourbrainstomakepicturesthatenableustointerpretandrespondtoourchangingenvironments.Toputthingsinabroaderperspective:plantphytochromeandhuman

redphotopsinarenotthesamephotoreceptor;whiletheybothabsorbredlight,theyaredifferentproteinswithdifferentchemistries.Whatweseeismediatedthroughphotoreceptorsfoundonlyinotheranimals.Whatadaffodil sees is mediated through photoreceptors found only in plants.But the plant and human photoreceptors are similar in that they allconsist of aprotein connected to a chemical dye that absorbs the light;thesearethephysicallimitationsrequiredforaphotoreceptortowork.Butthereareexceptionstoeveryrule,anddespitebillionsofyearsof

independent evolution plant and animal visual systems do have somethingsincommon.Bothanimalsandplantscon-tainblue-light receptorscalledcryptochromes.3 Cryptochrome has no effect on phototropism inplants,butitplaysseveralotherrolesinregulatingplantgrowth,oneofwhich is its control over a plant’s internal clock. Plants, like animals,have an internal clock called the “circadian clock” that is in tunewithnormal day-night cycles. In our case, this internal clock regulates allparts of our life, fromwhenwe’re hungry, whenwe have to go to thebathroom, when we’re tired, and when we feel energetic. These dailychanges in our body’s behavior are called circadian rhythms, becausethey continue on a roughly twenty-four-hour cycle even if we keep

ourselves in a closed room that never gets sunlight. Flying halfwayaroundtheworldputsourcircadianclockoutofsyncwiththeday-nightsignals,aphenomenonwecalljetlag.Thecircadianclockcanberesetbylight,butthistakesafewdays.Thisisalsowhyspendingtimeoutsideinthelighthelpsusrecoverfromjetlagfasterthanspendingtimeinadarkhotelroom.Cryptochrome is theblue-light receptor primarily responsible for the

resetting of our circadian clocks by light. Cryptochrome absorbs bluelightandthensignalsthecellthatit’sdaytime.Plantsalsohaveinternalcircadian clocks that regulate many plant processes, including leafmovements and photosyn-thesis.Ifweartificiallychangeaplant’sday-nightcycle,italsogoesthroughjetlag(butdoesn’tgetgrumpy),andittakes a few days for it to readjust. For example, if a plant’s leavesnormallyclose in the lateafternoonandopen in themorning, reversingitslight-darkcyclewillinitiallyleadtoitsleavesopeninginthedark(atthetimethatusedtobeday)andclosinginthelight(atthetimethatusedtobenight).Thisopeningandclosingofleaveswillreadjusttothenewlight-darkpatternswithinafewdays.The plant cryptochrome, just like the cryptochrome in fruit flies and

mice, has a major role in coordinating external light signals with theinternal clock. At this basic level of blue-light control of circadianrhythms,plantsandhumans“see”inessentiallythesameway.Fromanevolutionary perspective, this amazing form of conservation ofcryptochrome function is actually not so surprising. Circadian clocksdeveloped early in evolution in single-celled organisms, before theanimaland theplantkingdomssplitoff.Theseoriginalclocksprobablyfunctioned to protect the cells from damage induced by high UVradiation. In this early clock, an ancestral cryptochromemonitored thelight environment and relegated cell division to the night. Relativelysimple clocks are even found today in most single-celled organisms,includingbacteriaandfungi.Theevolutionoflightperceptioncontinuedfromthisonecommonphotoreceptorinallorganismsanddivergedintothe two distinct visual systems that distinguish plants from animals.Whatmaybemoresurprising,though,isthatplantsalsosmell…

TWOWhataPlantSmells

Stoneshavebeenknowntomoveandtreestospeak.

—Shakespeare,MacbethPlantssmell.Plantsobviouslyemitodorsthatanimalsandhumanbeingsare attracted to, but they also sense theirown odors and those ofneighboring plants. Plants know when their fruit is ripe, when theirneighborhasbeencutbyagardener’sshears,orwhen theirneighbor isbeing eaten by a ravenous bug; they smell it. Some plants can evendifferentiate the smellof a tomato from the smellofwheat.Unlike thelargespectrumofvisualinputthataplantexperiences,aplant’srangeforsmellislimited,butitishighlysensitiveandcommunicatesagreatdealofinformationtothelivingorganism.Ifyoulookuptheword“smell”inastandarddictionarytoday,you’ll

see that it is defined as the ability “to perceive odor or scent throughstimuli affecting the olfactory nerves.” Olfactory nerves can easily beunderstoodas thenerves thatconnect thesmell receptors in thenose tothebrain. Inolfaction, the stimuli are smallmoleculesdissolved in theair.Humanolfactioninvolvesthecellsinournosethatreceiveairbornechemicals,anditinvolvesourbrain,whichprocessesthisinformationsothatwecanrespondtovarioussmells.IfyouopenabottleofChanelN°5on one side of a room, for example, you smell it on the other becausecertain chemicals evaporate from the perfume and disperse across theroom.Themoleculesarepresentinverydilutequantities,butournosesarefilledwiththousandsofreceptorsthatreactspecificallywithdifferentchemicals.Itonlytakesonemoleculetoconnectwithareceptortosense

thenewsmell.Ourbody’smechanism for theperceptionof smells isdifferent from

the mechanism involved in the perception of light. As we saw in theprevious chapter, we only need four classes of photoreceptors thatdifferentiate between red, green, blue, andwhite to see the colors of acompletepalette.Whenitcomestoolfaction,however,wehavehundredsof different receptor types, each specifically designated for a uniquevolatilechemical.Thewaythatasmellreceptorinthenosebindstoachemicalissimilar

to the concept of a lock-and-key system. Each chemical has its ownparticularshapethatfitsintoaspecificproteinreceptor,justaseachkeyhas its own particular structure that fits into a specific lock. Only auniquechemicalcanbindtoauniquereceptor,andoncethishappens,itinitiatesacascadeofsignalsthatendsinanervefiringinthebraintoletus know that the receptor has been stimulated. We interpret this as aparticular smell. Scientists have recordedhundredsof individual aromachemicals such as menthol (the major component of aroma inpeppermint)andputrescine(responsibleforthefoul-smellingaromathatemanatesfromdeadflesh).Butanyparticulararomawesmellisusuallytheresultofamixofseveralchemicals.Forexample,whileabouthalfofthepeppermintodorisduetomenthol,therestisacombinationofmorethanthirtyotherchemicals.That’swhywecandescribethebouquetofanexcellentspaghettisauce,orofadeepredwine,orofanewbornbabyinsomanydifferentways.So what happens in a plant? Our dictionary’s definition of “smell”

excludes plants from the discussion. They are removed from ourtraditional understandings of the olfactory world because they do nothaveanervoussystem,andolfactionforaplantisobviouslyanose-lessprocess.Butlet’ssaywetweakthisdefinitionto“theabilitytoperceiveodor or scent through stimuli.” Plants are indeed more than remedialsmellers.Whatodorsdoesaplantperceive,andhowdosmellsinfluenceaplant’sbehavior?

UnexplainedPhenomenaMy grandmother didn’t study plant biology or agriculture. She didn’tevenfinishhighschool.Butsheknewthatshecouldgetahardavocadoto soften by putting it in a brown paper bag with a ripe banana. Shelearnedthismagicfromhermother,wholearneditfromhermother,andsoon. In fact, this practicegoesback to antiquity, and ancient cultureshad diverse methods for getting fruit to ripen. The ancient Egyptiansslashedopena few figs inorder toget anentirebunch to ripen, and inancientChinapeoplewouldburnritualincenseinastorageroomofpearstogetthefruittoripen.Intheearlytwentiethcentury,farmersinFloridawouldripencitrusin

shedsheatedbykerosene.Thesefarmersweresurethattheheatinducedthe ripening, and of course their conclusion sounds logical. You canimagine their dismay, then,when theyplugged in someelectricheatersnear the citrus and found that the fruit didn’t cooperate at all. So if itwasn’ttheheat,couldtheripeningmagicbecomingfromthekerosene?Itturnedoutthatitwas.In1924,FrankE.Denny,ascientistfromthe

U.S. Department of Agriculture in Los Angeles, demonstrated thatkerosenesmokecontainsminuteamountsofamoleculecalledethyleneand that treating any fruit with pure ethylene gas is enough to induceripening.The lemonshe studiedwere so sensitive to ethylene that theycouldrespondtoatinyamountintheair,ataratioof1to100million.Similarly, it turns out that the smoke from the Chinese incense alsocontainedethylene.Soasimplescientificmodelwouldpositthatthefruit“smells”minusculeamountsofethyleneinthesmokeandtranslatesthissmell into rapid ripening. We smell the smoke from a neighbor’sbarbecue,andwesalivate;aplantdetectssomeethyleneintheair,anditsoftensup.But this explanation doesn’t answer two important questions: First,

why do plants respond to the ethylene in smoke anyway?And second,what about my grandma putting two fruits together in a bag and theEgyptiansslashing their figs?ExperimentscarriedoutbyRichardGaneinCambridgeinthe1930spointtosomeanswers.Ganeanalyzedtheair

immediately surrounding ripening apples and showed that it containedethylene. A year after his pioneering work, a group at the BoyceThompson Institute at Cornell University proposed that ethylene is theuniversalplanthormoneresponsibleforfruitripening.Infact,numeroussubsequentstudieshaverevealedthatallfruits, includingfigs,emitthisorganiccompound.Soit’snotjustsmokethatcontainsethylene;normalfruitemits thisgasaswell.When theEgyptiansslashed their figs, theyallowedtheethylenegastoeasilyescape.Whenweputaripebananainabagwithahardpear,forexample,thebananagivesoffethylene,whichis“smelled” by the pear, and the pear quickly ripens. The two fruits arecommunicatingtheirphysicalstatestoeachother.Ethylene signaling between fruits didn’t evolve so that we can have

perfectly ripe pears whenever we crave them, of course. Instead, thishormone evolved as a regulator of plant responses to environmentalstresses such as drought and wounding and is produced naturallythroughout the life cycle of all plants (including little mosses). Butethylene is particularly important for plant aging as it is the majorregulator of leaf senescence (the aging process that produces autumnfoliage) and is produced incopious amounts in ripening fruit. Theethyleneproducedinripeningapplesensuresnotonlythattheentirefruitripensuniformlybut thatneighboringappleswillalsoripen,whichwillgive off even more ethylene, leading to an ethylene-induced ripeningcascade of McIntoshes. From an ecological perspective, this has anadvantage in ensuring seed dispersal as well.Animals are attracted to“ready-to-eat”fruitslikepeachesandberries.Afulldisplayofsoftfruitsbrought on by the ethylene-induced wave guarantees an easilyidentifiablemarketforanimals,whichthendispersetheseedsastheygoabouttheirdailybusiness.

FindingFoodCuscutapentagona is not your normal plant. It’s a spindly orange vine

thatcangrowup to three feethigh,produces tinywhite flowersof fivepetals,andisfoundalloverNorthAmerica.What’suniqueaboutCuscutaisthatithasnoleavesanditisn’tgreenbecauseitlackschlorophyll,thepigmentthatabsorbssolarenergy,whichallowsplantstoturnlightintosugarsandoxygenthroughphotosynthesis.Cuscutaobviouslycan’tcarryout photosynthesis, asmost plants do, so it doesn’tmake its own foodfromlight.Withallofthisinmind,we’dassumeCuscutawouldstarve,butinsteadit thrives.Cuscutalivesinanotherway:itgetsitsfoodfromits neighbors. It is a parasitic plant. In order to live,Cuscuta attachesitselftoahostplantandsucksoutthenutrientsprovidedbythehostbyburrowing an appendage into the plant’s vascular system. Notsurprisingly,Cuscuta, commonly known as the dodder plant, is anagricultural nuisance and is even classified as a “noxiousweed”by theU.S. Department of Agriculture. But what makesCuscuta trulyfascinatingisthatithasculinarypreferences:itchooseswhichneighborstoattack.BeforewegettothereasonswhyCuscutahasveryspecificandrefined

culinary tastes, let’s see how it starts its parasitical life.Cuscuta seedsgerminatelikeanyotherplantseeds.Placedonsoil,theseedbreaksopen,thenewshootgrowsintotheair,andthenewrootburrowsintothedirt.But ayoungdodder left on its ownwill die if it doesn’t quickly find ahosttoliveoffof.Asadodderseedlinggrows,itmovesitsshoottipinsmall circles, probing the surroundings the way we do with our handswhenwe’reblindfoldedorsearchingforthekitchenlightinthemiddleofthenight.Whilethesemovementsseemrandomatfirst,ifthedodderisnext to another plant (say, a tomato), it’s quickly obvious that theCuscuta is bending and growing and rotating in the direction of thetomatoplantthatwillprovideitwithfood.Thedodderbendsandgrowsandrotatesuntil finally it findsa tomatoleaf.Butrather thantouchtheleaf, thedodder sinksdownandkeepsmovinguntil it finds thestem ofthetomatoplant.Inafinalactofvictory,ittwirlsitselfaroundthestem,sendsmicroprojec-tionsintothetomato’sphloem(thevesselsthatcarrytheplant’ssugarysap),andstartssiphoningoffsugarssothatitcankeepgrowingandeventuallyflower.Oh,andthetomatoplantstartstowiltas

thedodderthrives.

Five-angleddodder(Cuscutapentagona)

Dr.ConsueloDeMoraesevendocumentedthisbehavioronfilm.4Sheis an entomologist at Penn State University whose main interest isunderstandingvolatilechemicalsignalingbetweeninsectsandplants,andbetweenplants themselves.OneofherprojectscenteredonfiguringouthowCuscuta locates its prey. She demonstrated that the dodder vinesnever grow toward empty pots or pots with fake plants in them butfaithfullygrowtoward tomatoplantsnomatterwheresheput them—inthelight,intheshade,wherever.DeMoraeshypothesizedthatthedodderactuallysmelled the tomato. To check her hypothesis, she and herstudentsputthedodderinapotinaclosedboxandputthetomatoinasecondclosedbox.Thetwoboxeswereconnectedbyatubethatenteredthedodder’sboxononeside,whichallowedthefreeflowofairbetweentheboxes.The isolateddodderalwaysgrewtoward the tube,suggesting

thatthetomatoplantwasgivingoffanodorthatwaftedthroughthetubeintothedodder’sboxandthatthedodderlikedit.If theCuscuta was really going after the smell of the tomato, then

perhaps De Moraes could just make a tomato perfume and see if thedodderwouldgoforthat.ShecreatedaneaudetomatostemextractthatsheplacedoncottonswabsandthenputtheswabsonsticksinpotsnexttotheCuscuta.Asacontrol,sheputsomeofthesolventsthatsheusedtomakethetomatoperfumeonotherswabsofcottonandputtheseonsticksnext to theCuscuta as well.As predicted, she tricked the dodder intogrowing toward the cotton giving off the tomato smell, thinking itwasgoingtofindfood,butnottothecottonwiththesolvents.Clearly, thedoddercansmellaplant tofindfood.ButasIexplained

earlier, thisnoxiousweedhasitspreferences.Givenachoicebetweenatomatoandsomewheat,thedodderwillchoosethetomato.Ifyougrowyour dodder in a spot that is equidistant between two pots—onecontainingwheat,theothercontainingtomato—thedodderwillgoforthetomato.Evenat the level of fragrance, andnot thewholeplant, dodderpreferseaudetomatotoeaudewheat.Atthebasicchemicallevel,eaudetomatoandeaudewheatarerather

similar. Both contain beta-myrcene, a volatile compound (one of thehundredsofuniquechemical smellsknown) thaton itsowncan induceCuscutatogrowtowardit.Sowhythepreference?Oneclearhypothesisisthecomplexityofthebouquet.Inadditiontobeta-myrcene,thetomatogives off two other volatile chemicals that the dodder is attracted to,making for an overall irresistible dodder-attracting fragrance. Wheat,however,onlycontainsonedodder-enticingodor, thebeta-myrcene,andnot the other two found in the tomato. What’s more, wheat not onlymakes fewer attractants but also makes (Z)-3-Hexenyl acetate, whichrepels the dodder more than the beta-myrcene attracts it. In fact, theCuscuta growsaway from (Z)-3-Hexenyl acetate, finding the wheatsimplyrepulsive.

(L)eavesdroppingIn1983,twoteamsofscientistspublishedastonishingfindingsrelatedtoplantcommunicationthatrevolutionizedourunderstandingofeverythingfrom thewillow tree to the limabean.The scientists claimed that treeswarneachotherof imminent leaf-eating-insect attack.The resultswererelatively straightforward; the implications astounding. News of theirwork soon spread to popular culture, with the idea of “talking trees”found in the pages not only ofScience but of mainstream newspapersaroundtheworld.DavidRhoadesandGordonOrians,twoscientistsfromtheUniversity

of Washington, noticed that caterpillars were less likely to forage onleavesfromwillowtreesifthesetreesneighboredotherwillowsalreadyinfestedwithtentcaterpillars.Thehealthytreesneighboringtheinfestedtrees were resistant to the caterpillars because, as Rhoades discovered,theleavesoftheresistanttrees,butnotofsusceptibleonesisolatedfromthe infested trees, contained phenolic and tannic chemicals that madethemunpalatabletotheinsects.Asthescientistscoulddetectnophysicalconnections between the damaged trees and their healthy neighbors—they did not share common roots, and their branches did not touch—Rhoades proposed that the attacked trees must be sending an airbornepheromonal message to the healthy trees. In other words, the infestedtrees signaled to the neighboring healthy trees, “Beware! Defendyourselves!”

Whitewillow(Salixalba)

Just three months later, the Dartmouth researchers Ian Baldwin andJack Schultz published a seminal paper that supported the Rhoadesreport. Baldwin and Schultz had been incontact with Rhoades anddesigned their experiment to be carried out under very controlledconditions,ratherthanmonitoringtreesgrownopeninnature,asRhoadesand Orians had done. They studied poplar and sugar maple seedlings(aboutafoottall)growninairtightPlexiglascages.Theyusedtwocagesfortheirexperiment.Thefirstcontainedtwopopulationsoftrees:fifteentrees that had two leaves torn in half, and fifteen trees that were notdamaged.The second cage contained the control trees,whichof coursewerenotdamaged.Twodayslater,theremainingleavesonthedamagedtrees contained increased levels of a number of chemicals, includingtoxicphenolicandtanniccompoundsthatareknowntoinhibitthegrowth

ofcaterpillars.Thetreesinthecontrolcagedidn’tshowincreasesinanyofthesecompounds.Theimportantresultherewasthattheleavesoftheintact trees in the same cage as the damaged ones also showed largeincreases in phenolic and tannic compounds. Baldwin and Schultzproposed that the damaged leaves, whether by tearing as in theirexperiments or by insect feeding as in Rhoades’s observations of thewillowtrees,emittedagaseoussignalthatenabledthedamagedtreestocommunicate with the undamaged ones, which resulted in the latterdefendingthemselvesagainstimminentinsectattack.

Whitepoplar(Populusalba)

These early reports of plant signalingwere often dismissed by otherindividualsinthescientificcommunityaslackingthecorrectcontrolsorashavingcorrectresultsbutexaggeratedimplications.Atthesametime,the popular press embraced the idea of “talking trees” and

anthropomorphizedtheconclusionsoftheresearchers.WhetheritwastheLos Angeles Times orThe Windsor Star in Canada orThe Age inAustralia,newsoutletswentberserkovertheideaandcarriedstorieswithtitles like“ScientistsTurnNewLeaf,FindTreesCanTalk”and“Shhh.LittlePlantsHaveBigEars,”andthefrontpageoftheSarasotaHerald-Tribuneboretheheadline“TreesTalk,RespondtoEachOther,ScientistsBelieve.”TheNewYorkTimes even titled itsmain editorial on June 7,1983,“WhenTreesTalk,”inwhichthewriterspeculatedabout“talkingtrees whose bark is worse than their blight.”All this public attentiondidn’t help convince scientists to adopt the ideas of chemicalcommunication being posited by Baldwin and his colleagues. But overthepastdecade, thephenomenonofplantcommunicationthroughsmellhasbeenshownagainandagainfora largenumberofplants, includingbarley, sagebrush, and alder, and Baldwin, a young chemist justbarelyout of college at the time of the original publication, has gone on to aprominentscientificcareer.5While the phenomenonof plants being influencedby their neighbors

through airborne chemical signals is now an accepted scientificparadigm, the question remains: Are plants truly communicating witheachother(inotherwords,purposelywarningeachotherofapproachingdanger),orarethehealthyonesjusteavesdroppingonasoliloquybytheinfestedplants,whichdonotintendtobeheard?Whenaplantreleasesasmellintheair,isitaformoftalking,orisit,sotosay,justpassinggas?While the ideaofaplantcallingoutforhelpandwarning itsneighborshas allegorical and anthropomorphic beauty, does it really reflect theoriginalintentofthesignal?Martin Heil and his team at the Center for Research andAdvanced

Studies in Irapuato, Mexico, have been studying wild lima beans(Phaseolus lunatus) for the past several years to further explore thisquestion.Heil knew thatwhen a lima bean plant is eaten by beetles, itresponds in two ways. The leaves that are being eaten by the insectsrelease a mixture of volatile chemicals into the air, and the flowers(thoughnotdirectlyattackedbythebeetles)produceanectarthatattracts

beetle-eating arthropods.6 Early in his career at the turn of themillennium,Heil hadworked at theMaxPlanck Institute forChemicalEcologyinGermany,thesameinstitutewhereBaldwinwas(andstillis)a director, and likeBaldwinbefore himHeilwonderedwhy itwas thatlimabeansemittedthesechemicals.Heilandhiscolleaguesplacedlimabeanplantsthathadbeenattacked

by beetles next to plants that had been isolated from the beetles andmonitored the air around different leaves. They chose a total of fourleaves from three different plants: from a single plant that had beenattackedbybeetles they chose two leaves, one leaf that hadbeen eatenand another that was not; a leaf from a neighboring but healthy“uninfested” plant; and a leaf from a plant that had been kept isolatedfrom any contact with beetles or infested plants. They identified thevolatile chemical in the air surrounding each leaf using an advancedtechnique known as gas chromatography–mass spectrometry (oftenfeaturedontheshowCSIandemployedbyperfumecompanieswhentheyaredevelopinganewfragrance).

Wildlimabean(Phaseoluslunatus)

Heilfoundthattheairemittedfromtheforagedandthehealthyleaveson the same plant contained essentially identical volatile chemicals,whiletheairaroundthecontrolleafwasclearofthesegases.Inaddition,the air around the healthy leaves from the lima beans that neighboredbeetle-infestedplantsalsocontainedthesamevolatilesasthosedetectedfrom the foraged plants. The healthy plantswere also less likely to beeatenbybeetles.In this set of experiments, Heil confirmed the earlier studies by

showing that the proximity of the undamaged leaves to the attackedleavesprovidedthemwithadefensiveadvantageagainsttheinsects.ButHeilwasnotconvincedthatdamagedplants“talk”tootherplantstowarnthemagainstimpendingattack.Rather,heproposedthattheneighboringplantmustbepracticingaformofolfactoryeavesdroppingonaninternalsignalactuallyintendedforotherleavesonthesameplant.Heilmodifiedhisexperimentalsetupinasimple,albeitingenious,way

to test his hypothesis. He kept the two plants next to each other butenclosedtheattackedleavesinplasticbagsfortwenty-fourhours.Whenhechecked thesamefour typesof leavesas in thefirstexperiment, theresultsweredifferent.Whiletheattackedleafcontinuedtoemitthesamechemical as it did before, the other leaves on the same vine andneighboring vines now resembled the control plant; the air around theleaveswasclear.Heilandhisteamopenedthebagaroundtheattackedleaf,andwiththe

helpofasmallventilatorthat’susuallyusedontinymicrochipstohelpcoolcomputers,theyblewtheairinoneoftwodirections:eithertowardtheneighboringleavesfartherupthevineorawayfromthevineandintotheopen.Theycheckedthegasescomingoutoftheleaveshigherupthestem andmeasured howmuch nectar they produced. The leaves blownwithair coming from the attacked leaf started to emit the same gasesthemselves,andtheyalsoproducednectar,whiletheleavesthatwerenotexposedtotheairfromtheattackedleafremainedthesame.

AnillustrationofHeil’sexperiments.OnthetoptwopanelsHeilletbeetlesattackthegrayleavesandthencheckedtheairaroundotherleavesonboththesamevineandtheneighboringvine.Onthetopleftweseethattheairaroundalltheleavesofbothvinescontainedthesamechemicals,whileonthetopright,whenHeilisolatedtheattackedleavesinplasticbags,theairaroundthemwasdifferentfromtheairaroundalltheotherleavesonbothvines.Onthebottomweseehissecondexperiment.Heilblewairfromattackedleaveseitherontootherleavesonthesamevine(ontheleft)orawayfromtheotherleaves(thebottomrightpanel).

The results were significant because they revealed that the gasesemittedfromanattackedleafarenecessaryforthesameplanttoprotectits other leaves from future attacks. In other words, when a leaf isattackedbyaninsectorbybacteria,itreleasesodorsthatwarnitsbrotherleaves to protect themselves against imminent attack, similar to guardtowersontheGreatWallofChinalightingfirestowarnofanoncomingassault.Inthisway,theplantensuresitsownsurvivalasleavesthathave“smelled” the gases given off by the attacked leaves will be moreresistanttotheimpendingonslaught.So what about the neighboring plant? If it’s close enough to the

attackedplant, then it benefits from this internal “conversation”amongleaves on the infested plant. The neighboring plant eavesdrops on anearby olfactory conversation, which gives it essential information tohelpprotect itself. Innature, this olfactory signal persists for at least afew feet (different volatile signals, depending on their chemicalproperties, travel forshorterormuch longerdistances).For limabeans,whichnaturallyenjoycrowding,thisismorethanenoughtoensurethatifoneplantisintrouble,itsneighborswillknowaboutit.

Whatexactlyisthelimabeansmellingwhenitsneighboriseaten?Eaudelima,justliketheeaudetomatodescribedinthedodderexperiment,isacomplexmixtureofaromas.In2009,HeilcollaboratedwithcolleaguesfromSouthKoreaandanalyzedthedifferentvolatilecompoundsemittedfrom the leavesof the attackedplants inorder to identify the chemicalmessenger.Butthetrickwasidentifyingtheonechemicalresponsibleforthe evident communication with other leaves. They compared thecompounds emitted by leaves following bacterial infection with thoseemitted following an insect feeding. Both treatments resulted in theexpression of similar volatile gases, except for two gases thatdiscriminated between the two treatments. The leavesunderbacterialattackemittedagascalledmethylsalicylate,andthoseeatenbybugsdidnot;thelatterproducedagascalledmethyljasmonate.Methylsalicylateisverysimilarinstructuretosalicylicacid.Salicylic

acidisfoundincopiousamountsinthebarkofwillowtrees.Infact,theancient Greek physician Hippocrates described a bitter substance, nowknown tobe salicylic acid, fromwillowbark that couldease aches andreducefevers.OtherculturesintheancientMiddleEastalsousedwillowbark as amedicine, as didNativeAmericans.Centuries later,weknowsalicylic acid as the chemical precursor for aspirin (which isacetylsalicylicacid),andsalicylicaciditselfisakeyingredientinmanymodernanti-acnefacewashes.Althoughwillowisawell-knownproducerofsalicylicacid,whichhas

beenextractedfromthistreeforyears,allplantsproducethischemicalinvariousamounts.Theyalsoproducemethylsalicylate(whichbythewayis an important ingredient inBengayointment).Butwhywouldaplantproduceapainrelieverandfeverreducer?Aswithanyphytochemical(orplant-produced chemical), plants don’t make salicylic acid forourbenefit.Forplants,salicylicacidisa“defensehormone”thatpotentiatestheplant’simmunesystem.Plantsproduceitwhenthey’vebeenattackedbybacteriaorviruses.Salicylicacidissolubleandreleasedattheexactspotof infection tosignal throughtheveins to therestof theplant thatbacteria are on the loose. The healthy parts of the plant respond byinitiating a number of steps that either kill the bacteria or, at the very

least,stoptheplague’sspread.Someoftheseincludeputtingupabarrierofdeadcellsaroundthesiteofinfection,whichblocksthemovementofthebacteriatootherpartsoftheplant.Yousometimesseethesebarrierson leaves; they appear aswhite spots.These spots are areas of theleafwherecellshaveliterallykilledthemselvessothatthebacterianearthemcan’tspreadfarther.Atabroadlevel,salicylicacidservessimilarfunctionsinbothplants

andpeople.Plantsusesalicylicacidtohelpwardoff infection(inotherwords,whenthey’resick).We’veusedsalicylicacidsinceancienttimes,and we use the modern derivative of aspirin when we’re sick with aninfectionthatcausesachesandpains.Returning to Heil’s experiments: his lima beans emitted methyl

salicylate,avolatileformofsalicylicacid,aftertheywereattackedwithbacteria.This result supportedworkdone adecade earlier in the labofIlyaRaskinatRutgersUniversity,whohadshownthatmethylsalicylatewas the major volatile compound produced by tobacco following viralinfection. Plants can convert soluble salicylic acid to volatile methylsalicylateandviceversa.Onewaytounderstandthedifferencebetweensalicylicacidandmethylsalicylateisthis:plantstastesalicylicacid,andt h e ysmell methyl salicylate. (As we know, taste and smell areinterrelated senses. The major difference is that wetaste solublemoleculesonthetongue,whilewesmellvolatilemoleculesinthenose.)Byenclosingtheinfectedleavesinplasticbags,Heilhadblockedthe

methylsalicylatefromwaftingfromtheinfectedleaftothenoninfectedone, whether on the same vine or on a neighboring plant. When thenoninfected leaf finally smelled themethyl salicylate byhaving the airfromtheinfectedleafblownontoit,itinhaledthegasesthroughthetinyopeningsontheleafsurface(calledstomata).Oncedeepintheleaf,themethylsalicylatewasconvertedbacktosalicylicacid,which,aswenowknow,plantstakewhenthey’refeelingsick.7

DoPlantsSmell?

Plants give off a literal bouquet of smells. Imagine the smell of roseswhen youwalk on a garden path in the summertime, or of freshly cutgrassinthelatespring,orofjasminebloomingatnight.Howaboutthesweetpungentodorofabrownbanana in-temingledwith themyriadofsmells at a farmers’ market?Without looking, we know when fruit isreadytoeat,andnovisitortoabotanicalgardencanbeoblivioustotheoffensive odor of the world’s largest (and smelliest) flower, theAmorphophallustitanum,betterknownasthecorpseflower.(Luckily, itbloomsonlyonceeveryfewyears.)Many of these aromas are used in complex communication between

plants and animals. The smells induce different pollinators to visitflowers and seed spreaders to visit fruits, and as the author MichaelPollaninfers,thesearomascaneveninducepeopletospreadflowersallovertheworld.Butplantsdon’tjustgiveoffodors;aswe’veseen,theyundoubtedlysmellotherplants.

Corpseflower(Amorphophallustitanum)

Ofcourse, likeplants,wesenseairbornevolatilecompounds.Weuse

ournosestogetawhiffofmanythings,particularlyfood.Butweneedtorememberthat“olfaction”meansmuchmorethan smelling good food. Our language is littered with olfactory-

tainted statements like “the smell of fear” and “I smell trouble,” andsmells are intimately tied with memory and emotion. The olfactoryreceptors in our noses are directly connected to the limbic system (thecontrolcenterforemotion)andevolutionarilytothemostancientpartofourbrains.Likeplants,wecommunicateviapheromones, thoughwe’reoftennotawareofit.Pheromones are given off by one individual and trigger a social

response in another. Pheromones in different animals, from flies tobaboons, communicate various situations: social dominance, sexualreceptiveness,fear,andsoon.Wealsoareinfluencedbyodorsandemitodors that affect those around us. For example, synchronization ofmenstrualcyclesamongwomenlivinginclosequartershasbeenfoundtobedue toodorcues inperspiration.Arecent(andprovocative)studyinScience showed that men who simply sniffed negative-emotion-relatedodorless tears obtained from women showed reduced levels oftestosteroneandreductionsinsexualarousal.Sosubtleolfactorysignalscouldpotentiallyaffectmanyaspectsofourpsyche.Plants and animals sense volatile compounds in the air, but can this

really be considered olfaction by plants? Plants obviously don’t haveolfactorynervesthatconnecttoabrainthatinterpretsthesignals,andasof2011onlyonereceptorforavolatilechemical,theethylenereceptor,hasbeenidentifiedinplants.Butripeningfruits,Cuscuta,Heil’splants,andotherflorathroughoutournaturalworldrespondtopheromones,justaswedo.Plantsdetectavolatilechemicalintheair,andtheyconvertthissignal(albeitnerve-free)intoaphysiologicalresponse.Surelythiscouldbeconsideredolfaction.So if plants can “smell” in their own uniquewayswithout olfactory

nerves,isitpossibletheycan“feel”aswellwithoutsensorynerves?

THREEWhataPlantFeels

IwilltouchahundredflowersAndnotpickone.

—EdnaSt.VincentMillay,“AfternoononaHill”

Mostofusinteractwithplantseveryday.Attimesweexperienceplantsassoftandcomforting, likegrass inaparkduringan indulgentmiddaynap or fresh rose petals spread across silk sheets.Other times they areroughandprickly:wenavigatearoundpeskythornstogettoablackberrybush on ameander through thewoods or trip over a knotted tree trunkthat’s worked its way up through the street. But in most cases, plantsremainpassiveobjects,inertpropsthatweinteractwithbutignorewhilewedoso.Wepluckpetalsfromdaisies.Wesawthelimbsoffunsightlybranches.Whatifplantsknewweweretouchingthem?It’sprobablyabit surprising, andmaybeevenabit disconcerting, to

discoverthatplantsknowwhenthey’rebeingtouched.Notonlydotheyknowwhen they’re being touched, but plants can differentiate betweenhot and cold, and know when theirbranches are swaying in the wind.Plantsfeeldirectcontact:someplants,likevines,immediatelystartrapidgrowthuponcontactwithanobjectlikeafencetheycanwrapthemselvesaround, and the Venus flytrap purposely snaps its jaws shut when aninsectlandsonitsleaves.Andplantsseeminglydon’tliketobetouchedtoomuch,assimplytouchingorshakingaplantcanleadtogrowtharrest.Of course, plants don’t “feel” in the traditional sense of the term.

Plantsdon’tfeelregret;theydon’tgetafeelforanewjob.Theydonothave an intuitive awareness of amental or emotional state. But plantsperceive tactile sensation, and someof themactually “feel” better than

we do. Plants like the burr cucumber (Sicyos angulatus) are up to tentimesmoresensitive thanwearewhen itcomes to touch.Vinesfromaburrcucumbercanfeelastringweighingonly0.009ounce(0.25gram),whichisenoughtoinducethevinetostartwindingitselfaroundanearbyobject.Ontheotherhand,mostofuscanonlyfeelthepresenceofaverylightpieceofstringonourfingersthatisabout0.07ounce(or2grams)inweight.Althoughaplantmaybemoresensitivetotouchthanahumanbeing, plants and animals have some surprising similarities when itcomestofeelingthattouch.Oursenseoftouchtransmitsvastlydifferentsensations,fromapainful

burn to the light traceofabreeze.Whenwecome intocontactwithanobject, nerves are activated, sending a signal to the brain thatcommunicates the type of sensation—pressure, pain, temperature, andmore.Allphysicalsensationsareperceivedthroughournervoussystemby specific sensory neurons in our skin, muscles, bones, joints, andinternalorgans.Throughtheactionofdifferenttypesofsensoryneurons,we experience a vast array of physical sensations: tickling, sharp pain,heat, light touch,ordullache, tonamea few.Justasdifferent typesofpho-toreceptorsarespecificfordifferentcolorsoflight,differentsensoryneuronsarespecificfordifferenttactileexperiences.Differentreceptorsare activated by an ant crawling on your arm and by a deep Swedishmassageatthespa.Ourbodieshavereceptorsforcoldandreceptorsforheat.Buteachofthedifferenttypesofsensoryneuronsactsinessentiallythesameway.Whenyoutouchsomethingwithyourfingers,thesensoryneurons for touch (knownasmechanoreceptors) relay their signal to anintermediaryneuronthatconnectsuptothecentralnervoussysteminthespinal cord. From there, other neurons convey the signal to the brain,whichtellsusthatwe’vefeltsomething.

Burrcucumber(Sicyosangulatus)

The principle involved in neural communication is the same for allnervecells:electricity.Theinitialstimulusstartsarapidelectrochemicalreactionknownasdepolarization,whichispropagatedalongthelengthofthe nerve. This electric wave hits the adjacent neuron, and the wavecontinuesalong thenewneuron,andsoon,until it reaches thebrain.Ablock in the signal at any stage can be catastrophic, as in the case oftraumaticspinedamage,whichcutsthissignal,leadingtolossoffeelinginthelimbsthathavebeenaffected.While the mechanisms involved in electrochemical signaling are

complex, thebasicprinciplesare simple. Justasabatterymaintains itschargebyhousingdifferentelectrolytesindifferentcompartments,acellhas a chargeowing todifferent amountsofvarious salts in andoutsidethecell.Thereismoresodiumontheoutsideofcellsandmorepotassiuminside.(That’swhysaltbalancesaresoimportant inourdiets.)Whenamechanoreceptorisactivated,let’ssaybyyourthumbtouchingthespacebaronakeyboard,specificchannelsopenupnearthepointofcontactin

thecellmembranethatallowsodiumtopassintothecell.Thismovementof sodium changes the electric charge, which leads to the opening ofadditional channels and increased sodium flux. This results in thedepolarizationthatpropagatesalongthelengthoftheneuronlikeawavepropagatingacrosstheocean.Attheendofaneuron,atthejunctionwhereitmeetsanadjacentone,

the action potential leads to a rapid change in the concentration of anadditionalion,calcium.Thiscalciumspikeisnecessaryforthereleaseofneurotransmittersfromtheactiveneuron,whicharereceivedbythenextneuron. Neurotransmitters binding to the second neuron initiate newwavesofactionpotentials.Thesespikes inelectricalactivityexemplifytheways inwhichnerves communicate,whether froma receptor to thebrainorfromthebraintoamuscletocauseamovement.Theubiquitouscardiacmonitors in hospitals depict this kind of electricalactivity as itrelates to heart function—a spike of activity followed by a recovery,whichisrepeatedagainandagain.Mechanosensoryneuronssendsimilarspikes of activity to the brain, and the frequency of the spikescommunicatesthestrengthofthesensation.Buttouchandpainarebiologicallynotthesamephenomena.Paindoes

not simply result froman increase in the signals emanating from touchreceptors.Ourskinfeaturesdistinctreceptorneuronsfordifferent typesof touch, but it also has unique receptor neurons for different types ofpain.Painreceptors(callednociceptors)requireamuchstrongerstimulusbeforetheysendactionpotentialstothebrain.Advil,Tylenol,andotherpain relievers work because they specifically mute the signal comingfromthenociceptorsbutnotthemechanoreceptors.Sohumantouchisacombinationofactionsintwodistinctpartsofthe

body—cells that sense the pressure and turn this pressure into anelectrochemicalsignal,andthebrainthatprocessesthiselectrochemicalsignal into specific types of feelings and initiates a response. So whathappensinplants?Dotheyhavemechanoreceptors?

Venus’sTrapThe Venus flytrap8 (otherwise known asDionaea muscipula) is thequintessentialexampleofaplantthatrespondstotouch.ItgrowsinthebogsoftheCarolinas,wherethesoillacksnitrogenandphosphorous.Tosurvive in such a nutritionally poor environment,Dionaea has evolvedthe amazing ability to garner nutrition not only from light but frominsects—and small animals as well. These plants carry outphotosynthesis, like all green plants, but theymoonlight as carnivores,supplementingtheirdietwithanimalprotein.

Venusflytrap(Dionaeamuscipula)

TheleavesoftheVenusflytrapareunmistakable:theyendintwomainlobesconnectedbyacentralmidrib,and theedgesof the two lobesarebordered by long protrusions, called cilia, that resemble the teeth of acomb.These two lobes,connectedononesidebyahinge,arenormallyspreadatanangle, formingaV-likestructure.The internal sidesof thelobehavepinkandpurplehuesandexcretenectar that is irresistible tomany creatures. When an unassuming fly, a curious beetle, or even asmall,meandering frogcrawls across the surfaceof the leaves, the two

leaves spring together with surprising force, sandwiching theunsuspecting prey and blocking its escape with its jail bars ofinterlocking cilia.9 The trap closes at an astounding speed: unlike ourfutile attempts to swat at apesky fly, theVenus flytrap springs shut inless than one-tenth of a second. Once activated, the trap excretesdigestivejuicesthatdissolveandabsorbthepoorprey.Theamazingcharacteristicsof theVenus flytrap ledCharlesDarwin,

whowas among the first scientists to publish an in-depth study of theplant and other carnivorous flora, to describe it as “one of the mostwonderful[plants]intheworld.”Darwin’sinterestincarnivorousplantsillustrates how naive curiosity can lead a trained scientist togroundbreaking discoveries. Darwin begins his 1875 treatiseInsectivorous Plants in this way: “During the summer of 1860, I wassurprised by finding how large a number of insectswere caught by theleavesofthecommonsun-dew[plant](Droserarotundifolia )onaheathin Sussex. I had heard that insectswere thus caught, but knew nothingfurtheronthesubject.”Fromknowingvirtuallynothingaboutthematter,Darwinbecametheforemostexpertoncarnivorousplants,includingtheVenus flytrap, in the nineteenth century, and indeed his work is stillreferencedtoday.Wenowknow that theVenus flytrap feels its prey and senses if the

organism crawling around inside its trap is the right size to consume.There are several large black hairs on the pink surface of the inside ofeachlobe,andthehairsactastriggersthatspringthetrapclosed.Butonehairbeingtouchedisnotenoughtospringthetrap;studieshaverevealedthatatleasttwohavetobetouchedwithinabouttwentysecondsofeachother. This ensures that the prey is the ideal size andwon’t be able towiggleoutof the traponce it closes.Thehairsareextremely sensitive,but they are also very selective. As Darwin noted in his bookInsectivorousPlants:

Drops of water, or a thin broken stream, falling from a

heightonthefilaments[hairs],didnotcausethebladestoclose…Nodoubt, theplant is indifferent to theheaviestshower of rain … I blew many times through a finepointed tube withmy utmost force against the filamentswithout any effect; such blowing being received with asmuchindifferenceasnodoubtisaheavygaleofwind.Wethus see that the sensitiveness of the filaments is of aspecializednature.

Even though Darwin described in great detail the series of eventsleadingtotrapclosureandthenutritionaladvantageoftheanimalproteintotheplants,hecouldn’tcomeupwiththemechanismofthesignalthatdifferentiatedbetweenrainandflyandenabledtherapidimprisonmentofthelatter.Convincedthattheleafwasabsorbingsomemeatyflavorfromthepreyonthelobes,Darwintestedalltypesofproteinsandsubstancesontheleaf.Butthesestudieswerefornaught,ashecouldnotinducetrapclosurewithanyofhistreatments.HiscontemporaryJohnBurdon-Sandersonmadethecrucialdiscovery

that explained the triggering mechanism once and for all. Burdon-Sanderson, a professor of practical physiology atUniversityCollege inLondonandaphysicianbytraining,studiedtheelectricalimpulsesfoundinallanimals,fromfrogstomammals,butfromhiscorrespondencewithDarwin became particularly fascinated by the Venus flytrap. Burdon-SandersoncarefullyplacedanelectrodeintheVenusflytrapleaf,andhediscovered that pushing on two hairs released an action potential verysimilartothoseheobservedwhenanimalmusclescontract.Hefoundthatit took several seconds for the electrical current to return to its restingstateafter ithadbeen initiated.Herealized thatwhenan insectbrushesup against the hairs inside the trap, it induces a depolarization that isdetectedinbothlobes.Burdon-Sanderson’s discovery that pressure on two hairs leads to an

electricalsignalthatisfollowedbythetrapclosingwasoneofthemost

important of his career and was the first demonstration that electricalactivityregulatesplantdevelopment.Buthecouldonlyhypothesizethatthe electric signal was the direct cause of trap closure.More than onehundred years later,Alexander Volkov and his colleagues at OakwoodUniversity inAlabama proved that the electric stimulation itself is thecausative signal for the trap’s closing. They applied a form of electricshock therapy to the open lobes of the plant, and it caused the trap toclose without any direct touch to the trigger hairs. Volkov’s work andearlierresearchinotherlabsalsomadeitclearthatthetrapremembersifonly a single trigger hair has been touched, and then it waits until asecond hair is triggered before closing. Only very recently did thisresearch shed light on themechanism that allows the Venus flytrap torememberhowmanyofitshairshavebeentriggered,whichI’llexploreinchaptersix.Beforewegettothewaysinwhichplantsremember,weneed to take some timewith the connectionbetween the electric signalandthemovementoftheleaves.

WaterPowerBurdon-Sanderson observed that the electrical pulse he detected in theclosing Venus flytrap was very similar to the action of a nerve and acontractingmuscle.Whiletheactionpotentialsintheabsenceofnerveswerecleartohim,themechanismofmovementintheabsenceofmuscleswasobscure.ToBurdon-Sanderson’sknowledge, the actionpotential inthe plant had no clearmuscle-like target to act on to induce the trap’sclosing.Studies ofMimosapudicaprovidedawonderfulexperimental system

to understand the world of leaf movements, which could then begeneralized to other plants. TheMimosa pudica is native to South andCentralAmericabut isnowgrownworldwideasanornamentalbecauseof its fascinatingmoving leaves. Its leaves are hypersensitive to touch,andifyourunyourfingerdownoneofthem,alltheleafletsrapidlyfold

inward and droop. They reopen several minutes later, only to rapidlycloseoncemore ifyoutouchthemagain.Thenamepudica reflects thisdroopingmovement. It means “shy” in Latin. The plant is also knownthroughoutmanyregionsas“thesensitiveplant.”Itsunusualbehaviorisreferredtoas“falsedeath”intheWestIndies,anditisreferredtoasthe“don’ttouchme”plantinHebrewandthe“shyvirgin”inBengali.Th eMimosa’s characteristic drooping and opening action is very

similartothatoftheVenusflytrapevenatthelevelofelectrophysiology.ThiswasnoticedbySirJagadishChandraBose,anotedphysicistturnedplant physiologist fromCalcutta, India.While carrying out research intheDavyFaradayResearchLaboratoryof theRoyalInstitutionofGreatBritain,BosereportedtotheRoyalSocietyinalecturein1901thattouchinitiatedanelectric actionpotential that radiated the lengthof the leaf,resulting in the rapid closing of theMimosa leaflets. (Unfortunately,Burdon-SandersonwashighlycriticalofBose’sworkandrecommendedthat hisMimosa paper be rejected from theProceedings of the RoyalSociety of London, though subsequent studies in many labs have sinceshownthatBosewasindeedcorrect.)

Mimosapudica

Studiesrevealedthatwhentheelectricsignalactsonagroupofcells

called the pulvinus, which are themotor cells thatmove the leaves, itleads to the drooping behavior of theMimosa’s leaves. To understandhowthepulvinusmovestheleavesintheabsenceofmuscles,wehavetounderstandalittlebitofbasicplantcellbiology.Theplantcellcontainstwomainparts.Theprotoplast, similar tocells inanimals, resemblesawaterballoon:athinmembranesurroundsaliquidinterior.Thisinteriorcontainsseveralmicroscopicparts, includingthenucleus,mitochondria,proteins,andDNA.What’suniqueaboutplantcellsisthattheprotoplastisenclosedwithinthesecondpart,aboxlikestructurecalledthecellwall.The cell wall gives a plant its strength in the absence of a supportingskeleton. Inwood, cotton, and nutshells,forexample, thecellwallsarethickandsturdy,whileinleavesandpetalsthewallsarethinandpliable.(Weare incrediblydependentoncellwalls, in fact, as theyareused tocreatepaper,furniture,clothing,ropes,andevenfuel.)Normally, the protoplast contains so much water that it presses

stronglyonthesurroundingcellwall,whichallowsplantcellstobeverytight and erect and to support weight. But when a plant lacks water,there’slittlepressureonthecellwalls,andtheplantwilts.Bypumpingwater in and out of cells, the plant can control how much pressure isappliedtothecellwall.ThepulvinuscellsarefoundatthebaseofeachMimosa leaflet and act asmini hydraulic pumps thatmove the leaves.Whenthepulvinuscellsarefilledwithwater,theypushtheleafletsopen;when they lose water, the pressure drops, and the leaves fold intothemselves.Wheredo the electric actionpotentials come intoplay?Theyare the

criticalsignal that tells thecellwhethertopumpwaterinorout.Undernormalconditions,whentheMimosa’sleavesareopen,thepulvinuscellsarefullofpotassiumions.Thehighconcentrationofpotassiuminsidethecell relative to the outside causes water to enter the cell in a futileattempttodilutethepotassium,whichresultsingreatpressureonthecellwall—and in erect leaves. Potassium channels are opened when theelectricsignalreachesthepulvinus,andasthepotassiumleavesthecell,so does the water. This causes the cells to become flaccid. Once thesignalhaspassed,thepulvinuspumpspotassiumintothecellsagain,and

theresultinginfluxofwateropensuptheleafagain.Calcium,thesameioncriticalforneuralcommunicationinhumans,regulatestheopeningofthe potassium channels, and as we’ll see, it is essential for a plant’sresponsetotouch.

ANegativeTouchIn the early 1960s, Frank Salisbury was studying the chemicals thatinduce flowering in cocklebur (Xanthium strumarium), a weed foundthroughout North America and most notorious for its little football-shapedburrs,whicharecommonlyfoundclingingtohikers’clothing.Tounderstandhowtheplantgrew,SalisburyandhisteamoftechniciansatColoradoStateUniversitydecided tomeasure thedaily increase in leaflength by going out into the field and physicallymeasuring the leaveswitharuler.Tohisbewilderment,Salisburynoticedthattheleavesbeingmeasured never reached their normal length. Not only that, as theexperiment continued, they eventually turned yellow and died. But theleavesonthesameplantthatwerenothandledandmeasuredthrived.AsSalisburyexplained,“Wewereconfrontedwiththeremarkablediscoverythatonecankillacockleburleafsimplybytouchingitforafewsecondseachday!”

Cocklebur(Xanthiumstrumarium)

As Salisbury’s interests lay elsewhere, a decade passed before hisobservationwasputintobroadercontext.MarkJaffe,aplantphysiologistwhowasbasedatOhioUniversityintheearly1970s,recognizedthatthistouch-induced growth inhibition is a general phenomenon in plantbiology.Hecoined the cumbersome term“thigmomorphogenesis” fromtheGreekrootsthigmo-(touch)andmorphogenesis(creationofshape)todescribethegeneraleffectofmechanicalstimulationonplantgrowth.Ofcourse,plantsareexposedtomultipletactilestressessuchaswind,

rain, and snow, and animals regularly come into contact withmany ofthem.Soinretrospect,itisn’tsosurprisingthataplantwouldretarditsgrowth in response to touch.A plant feelswhat type of environment itlives in. Trees growing high on amountain ridge are often exposed tostrongwinds,andtheyadapttothisenvironmentalstressbylimitingtheirbranchdevelopmentandgrowingshort,thicktrunks.Thesamespeciesoftreegrowninaprotectedvalley,ontheotherhand,willbetall,thin,andfull of branches. Growth retardation in response to touch is anevolutionaryadaptationthatincreasesthechancesthataplantcansurvivemultiple, and often violent, perturbations. Indeed, from an ecologicalpointofview,aplantfacesmanyofthesamechoicesthatwewouldifwe

were building a home. What types of resources should go into thefoundation?Howabout theframe?Ifyou live inanareawith lowwindlevels,or lowriskforearthquakes, thenyour resourcesmaygo into theoutwardappearanceofyourhome.Butinanareaofhighwindlevels,orhigh risk for earthquakes, your resources have to go into a substantialfoundationandframe.What holds true for trees also holds true for our littlemustardplant

Arabidopsis thaliana that we met in the first chapter. An arabidopsisplant that’s touchedafewtimesaday in the labwillbemuchsquatter,and flower much later, than one that’s left to its own accord. Simplystroking its leaves three times a day completely changes its physicaldevelopment.Whilethischangeinoverallgrowthtakesmanydaysforusto witness, the initial cellular response is actually quite rapid. In fact,Janet Braam and her colleagues at Rice University demonstrated thatsimply touching an arabidopsis leaf results in a rapid change in thegeneticmakeupoftheplant.ThatBraamdiscoveredthisphenomenonatallwasquiteserendipitous.

Initially, as a young research fellow at Stanford University, she wasinterested not in the effect of touch on plants but rather in the geneticprograms activated by plant hormones. In one of her experimentsdesigned to elucidate the effect of the hormone gibberellin on plantbiology, she sprayed arabidopsis leaves with this hormone and thenchecked which genes were activated by the treatment. She discoveredseveralgenesthatwererapidlyturnedonfollowingherspraytreatment,and she assumed that they were responding to the gibberellin. But itturnedout that theiractivity increasedafter theyweresprayedwithanynumberofsubstances—evenwater.Not tobedefeated,Braampressedon, trying to figureoutwhy these

genes were activated even by water. She experienced a true eurekamomentwhensherealizedthatthecommonfactorinthetreatmentswast h ephysical sensation of being sprayed with the solutions. Braamhypothesized that the genes she discovered were responding to thephysical treatment of the leaves. To test this, she continued herexperiment, but rather than spraying the plants with water, she simply

touchedthem.Tohersatisfaction,thesamegenesthathadbeeninducedby spraying withthe hormone, or with water, were also activated bytouching the plants. Braam understood that her newfound genes wereclearly activatedby touch, and she aptly named them the “TCH genes”sincetheywereinducedbytouchingtheplants.Furtherunderstanding the importanceof thisdiscoverynecessitatesa

quickexplorationofhowgeneswork ingeneral.TheDNAfound in thenucleus of each cell thatmakes up an arabidopsis plant contains abouttwenty-fivethousandgenes.Atthesimplestlevel,eachgeneencodesoneprotein.While theDNAis thesame ineachcell,differentcellscontaindifferentproteins.Forexample,acellinaleafcontainsproteinsdifferentfromthoseinarootcell.Theleafcellcontainsproteinsthatabsorblightfor photosynthesis, while the root cell contains proteins that help itabsorb minerals from the soil. Various cell types contain differentproteins because different genes are active—ormore exactly, differentgenes are transcribed—in each type of cell. While some genes aretranscribedinallcells(likethegenesneededformakingmembranes,forexample), most genes are transcribed in only specific subsets of celltypes.Sowhileeachcellhas thepotential toturnonanyofthetwenty-fivethousandgenes,inpracticeonlyseveralthousandgenesareactiveinaparticularcelltype.Tofurthercomplicatematters,manygenesarealsocontrolled by the external environment. Some genes are transcribed inleaves only after the leaves see blue light. Some are transcribed in themiddleofthenight,someafteraheatspell,someafterabacterialattack,andsomeaftertouch.What are these touch-activated genes? The first of theTCH genes

Braam identified encode proteins involved in calcium signaling in thecell.Aswe’veseenearlier,calciumisoneoftheimportantsaltionsthatregulates both the cell’s electrical chargeand communication betweencells.Inplantcells,calciumhelpsmaintaincellturgor(asinthepulvinuscells in the case of theMimosa plant) and is also part of the plant cellwall. Calcium is essential for humans and other animals to propagateelectricsignalsfromneurontoneuron,anditisalsonecessaryformusclecontraction. Although we do not yet know all of the ways in which

calciumregulatessuchdiversephenomenaatthesametime,itisafieldofintensestudy.Scientists do know that following a mechanical stimulation like the

shakingofabranchoraroothittingarock,theconcentrationofcalciumions inaplant cellpeaks rapidlyand thendrops.This spikeaffects thecharge across the cell membrane, but it also directly affects multiplecellular functions as a “second messenger,” a mediator molecule thatrelays information fromspecific receptors tospecificoutputs.This freesolublecalciumisnotveryefficientonitsownincausingsomeresponse,becausemostproteinscan’tbindcalciumdirectly;hencecalcium,inbothplantsandanimals,usuallyworksinconjunctionwithasmallnumberofcalcium-bindingproteins.Among these, the most studied is calmodulin (calcium-modul ated

protein).Calmodulinisarelativelysmallbutveryimportantprotein,andwhenitbindswithcalcium,it interactswith,andmodulatestheactivityof,anumberofproteinsinvolvedinprocessesinhumanbeings—suchasmemory,inflammation,musclefunction,andnervegrowth.Gettingbacktoplants,BraamshowedthatthefirstTCHgeneencodedcalmodulin.Inotherwords,whenyoutouchaplant,beitarabidopsisorpapaya,oneofthe first things it does is make more calmodulin. Most likely, a plantmakesmorecalmodulintoworkwiththecalciumthatitreleasesduringtheactionpotentials.ThankstothecontinuingworkofBraamandotherscientists,wenow

knowthatover2percentofarabidopsisgenes(including,butnotlimitedto, genes encoding calmodulin and other calcium-related proteins) areactivatedafteraninsectlandsonitsleaf,ananimalbrushesupagainstit,or thewindmoves its branches. This is a surprisingly large number ofgenes,whichindicatesjusthowfar-reachingaplant’sresponseiswhenitcomestomechanicalstimulationandsurvival.

PlantandHumanFeeling

Wecanfeelavariedandcomplexmixtureofphysicalsensationsduetothepresenceofspecializedmechanosensoryreceptornervesandduetoabrain that translates these signals into sensations with emotionalconnotations. These receptors enable us to respond to a vast array oftactilestimulations.AspecificmechanosensoryreceptorcalledMerkel’sdisks detects sustained touch and pressure on our skin and muscles.Nociceptors in our mouths are activated by capsaicin, the ultrahotchemicalfoundinchilipeppers,andnociceptorssignalthatourappendixisinflamedbeforeanappendectomy.Painreceptorsexisttoenableustowithdraw from a dangerous situation or to let us knowof a potentiallydangerousphysicalprobleminsideourbodies.Whileplantsfeeltouch,theydon’tfeelpain.Theirresponsesarealso

not subjective. Our perception of touch and pain is subjective, varyingfrompersontoperson.Alighttouchcanbepleasurabletoonepersonoranannoyingtickletoanother.Thebasisforthissubjectivityrangesfromgeneticdifferencesaffectingthethresholdpressureneededtoopenanionchannel to psychologicaldifferencesthatconnect tactilesensationswithassociations such as fear, panic, and sadness,which can exacerbate ourphysiologicalreactions.A plant is free from these subjective constraints because it lacks a

brain. But plants feel mechanical stimulation, and they can respond todifferent types of stimulation in unique ways. These responses do nothelp the plant avoid pain but modulate development to best suit theambient environment. An amazing example of this was provided byDiannaBowles and her teamof researchers at theUniversity ofLeeds.Earlier researchhad shown thatwounding a single tomato leaf leads toresponsesintheunwoundedleavesonthesameplant(similartothetypesof research outlined in chapter two). These responses include thetranscriptionofaclassofgenescalledproteinaseinhibitorsintheintactleaves.

Tomato(Solanumlycopersicum)

Bowleswascurioustoknowmoreaboutthenatureofthesignalfromawounded leaf to an unharmed leaf. The accepted paradigm was that asecretedchemicalsignalwastransportedintheveinsofawoundedleafto the rest of the plant. But Bowles hypothesized that the signal waselectric. To test her hypothesis, she burned one tomato leafwith a hotsteelblockandfoundthatanelectricsignalcouldbedetectedinthestemof the sameplant at adistance from thewounded leaf.Theplant couldstill detect the signal even if she iced the stem-like structure thatconnectstheleaftothestem(calledapetiole).Shefoundthat icingthepetiole blocked chemical flow from the leaf to the stem—but notelectrical flow.Moreover,whenshe iced thepetioleof theburned leaf,theuntreated leaves still transcribed theproteinase inhibitorgenes.The

leaf did not feel pain. The tomato responded to the hot metal not bymoving away from it but by warning its other leaves of a potentiallydangerousenvironment.As sessile, rooted organisms, plants may not be able to retreat or

escape, but theycan change their metabolism to adapt to differentenvironments. Despite the differences between the ways plants andanimalsreacttotouchandotherphysicalstimulationsattheorganismallevel, at the cellular level the signals initiated are hauntingly similar.Mechanicalstimulationofaplantcell, likemechanicalstimulationofanerve, initiates a cellular change in ionic conditions that results in anelectric signal.And just like inanimals, this signal canpropagate fromcell to cell,and it involves the coordinated function of ion channelsincludingpotassium,calcium,calmodulin,andotherplantcomponents.Aspecializedformofmechanoreceptorisalsofoundinourears.Soif

plantscansensetouchasaresultofthemechanoreceptorssimilartotheones in our skin, can they also hear by sensing sound throughmechanoreceptorssimilartotheonesinourears?

FOURWhataPlantHears

ThetemplebellstopsbutIstillhearthesoundcomingoutoftheflowers.

—MatsuoBash

Forests reverberatewith sounds.Birds sing, frogs croak, crickets chirp,leaves rustle in the wind. This never-ending orchestra includes soundsthatsignaldanger,soundsrelatedtomatingrituals,soundsthatthreaten,sounds that appease. A squirrel jumps on a tree at the crunch of abreakingbranch;abirdanswers thecallofanother.Animalsconstantlymove in response to sound, and as theymove, they create new sounds,contributingtoacyclicalcacophony.Butevenastheforestchattersandcrackles,plantsremaineverstoic,unresponsive to thedinaroundthem.Areplants deaf to the clamor of a forest?Or arewe just blind to theirresponse?Whilevarious formsof rigorous scientific researchhavehelped shed

lightontheplantsenseswe’vecoveredsofar,littlecredible,conclusiveresearch exists when it comes to a plant’s response to sound. This issurprising,giventheamountofanecdotalinformationwehaveabouttheways inwhichmusicmayinfluence howa plant grows.Whilewemaythink twicewhenwehear thatplantscansmell, the idea thatplantscanhear comes as no surprise at all.Many of us have heard stories aboutplants flourishing in rooms with classical music (though some peopleclaimit’sreallypopmusicthatgetsaplantmoving).Typically,though,much of the research on music and plants has been carried out byelementary school students and amateur investigators who do notnecessarilyadhere to thecontrols found in laboratoriesgrounded in the

scientificmethod.Beforewedelveintowhetherornotplantscanactuallyhear,let’sgeta

better understanding of human hearing. A common definition of“hearing”is“theabilitytoperceivesoundbydetectingvibrationsviaanorgan such as the ear.” Sound is a continuum of pressure waves thatpropagate through the air, throughwater, or even through solid objectssuchasadoorortheearth.Thesepressurewavesareinitiatedbystrikingsomething (such as by beating a drum) or starting a repeated vibration(like plucking a string) that causes the air to compress in a rhythmicfashion.Wesensethesewavesofairpressurethroughaparticularformof mechanoreception by tactile-sensitive hair cells in our inner ears.These hair cells are specialized mechanosensory nerves from whichextendhairlikefilamentscalledstereociliathatbendwhenanair-pressurewave(asound)hitsthem.Thehaircellsinourearsconveytwotypesofinformation:volumeand

pitch.Volume (inotherwords, thestrengthof thesound) isdeterminedbytheheightofthewavereachingtheear,orwhat’sbetterknownastheamplitudeofthewaves.Loudnoiseshavehighamplitude,andsoftnoiseshave lowamplitude.Thehigher the amplitude, themore the stereociliabend. Pitch, on the other hand, is a function of thefrequency of thepressure waves—how many times per second the wave is detectedregardlessof its amplitude. The faster the frequency of the wave, thefasterthestereociliabendbackandforthandthehigherthepitch.10As the stereocilia vibrate in the hair cells, they initiate action

potentials(asdoothertypesofmechanoreceptorsthatweencounteredinthe previous chapter) that are relayed to the auditory nerve, and fromthere they travel to the brain, which translates this information intodifferent sounds. So human hearing is the result of two anatomicaloccurrences: thehaircells inourears receive thesoundwaves,andourbrain processes this information so that we can respond to differentsounds.Now,ifplantsarecapableofdetectinglightwithouthavingeyes,cantheydetectsoundiftheydon’thaveears?

Rock-and-RollBotanyAtonepointoranother,manyofushavebeenintriguedbytheideathatplants respond to music. Even Charles Darwin (who, as we’ve seen,carried out his seminal research into plant vision and feeling over acenturyago)studiedwhetherplantscouldpickuponthetunesheplayedfor them. In one of his more bizarre experiments, Darwin (who, inaddition to his lifetime commit-mentto biology research, was an avidbassoonist) monitored the effects of his own bassoon music on plantgrowth by seeing if his bassoon could induce the leaves of theMimosaplant to close (it couldn’t, and he described his study as a “fool’sexperiment”).Researchdealingwithplantauditoryprowesshasn’texactlyblossomed

sinceDarwin’sfailedattempts.Hundredsofscientificarticleshavebeenpublished in the last year alone that dealwith plant responses to light,smell, and touch, yet only a handful have been published over the lasttwentyyears that havedealt specificallywithplant responses to sound,and even then many of them don’t hold up to my standards for whatwouldbeevidenceofa“hearing”plant.Anexampleofoneofthesepapers(albeitazanyone)waspublishedin

TheJournalofAlternativeandComplementaryMedicine. Itwaswrittenby Gary Schwartz, a professor of psychology and medicine, and hiscolleagueKatherineCreath,aprofessorofopticalsciences,bothbasedatthe University of Arizona, where Schwartz founded the VERITASResearch Program. This program “test[s] the hypothesis that theconsciousness (or personality or identity) of a person survives physicaldeath.” Obviously, studying consciousness after death presents someexperimental difficulties, so Schwartz also studies the existence of“healingenergy.”Becausehumanparticipantsinastudycanbestronglyinfluencedbythepowerofsuggestion,SchwartzandCreathusedplantsinstead, in order to uncover the “biologic effects of music, noise, andhealing energy.”Of course, plants cannot be influenced by the placeboeffector,asfarasweknow,bymusicalpreferences(thoughresearcherscarryingoutandanalyzingexperimentscanbe).

They hypothesized that healing energy and “gentle” music (whichconsistedofNativeAmericanfluteandnaturesounds,which theynotedwere preferred by the experimenter) would be conducive to thegermination of seeds.11 Creath and Schwartz explained that their datarevealed that slightly more zucchini and okra seeds germinated in thepresence of gentle music sounds than seeds that were kept in silence.They also noted that germination rates could increase as a result ofCreath’shealingenergy,whichsheappliedtotheseedswithherhands. 12It goes without saying that these results have not been validated bysubsequent research in other plant laboratories, but one of the sourcesCreath and Schwartz cited in support of their results was DorothyRetallack’sTheSoundofMusicandPlants.Dorothy Retallack was a self-described “doctor’s wife, housekeeper

andgrandmother to fifteen,” and sheenrolledas a freshman in1964 inthenow-defunctTempleBuellCollegeafterherlastchildhadgraduatedfrom college. Retallack, a professional mezzo-soprano who oftenperformedatsynagogues,churches,andfuneralhomes,decidedtomajorinmusicatTempleBuell.ShetookanIntroductiontoBiologycoursetocompletehersciencerequirementsandwasaskedbyherteachertocarryout any experiment that she thought would interest her. Retallack’sjuxtaposingofherbiologyrequirementwithher loveformusicresultedin a book spurned bymainstream science but quickly embraced by thepopularculture.Retallack’sTheSoundofMusicandPlantsprovidesawindowintothe

cultural-political climate of the 1960s, but it alsosheds light on herperspective as well. Retallack comes across as a unique mixture of asocial conservative who believed that loud rock music correlated withantisocial behavior among college students and a New Age religiousspiritualistwhosawasacredharmonybetweenmusicandphysicsandallofnature.

DorothyRetallackinthelabwithheradviserDr.FrancisBroman

Retallackexplainedthatshewasintriguedbyabookpublishedin1959titledThePowerofPrayeronPlants, inwhich the author claimed thatplants that were prayed to thrivedwhile those bombardedwith hatefulthoughts died. Retallack wondered whether similar effects could beinducedbypositiveornegativegenresofmusic(therulingofpositiveornegativewasdictated,ofcourse,byherownmusicaltaste).Thisquestionbecamethebasisofherresearchrequirement.Bymonitoringtheeffectofdifferent music genres on plant growth, she hoped to provide hercontemporarieswithproofthatrockmusicwaspotentiallyharmful—notonlytoplants,buttohumansaswell.Retallack exposed different plants (philodendrons, corn, geraniums,

andviolets,tonameafew—eachexperimentusedadifferentspecies)toan eclectic collection of recordings, including music by Bach,Schoenberg, JimiHendrix, and Led Zeppelin, and thenmonitored theirgrowth. She reported that the plants exposed to soft classical music

thrived (even when she exposed them toMuzak, that sublime elevatormusicweallknowand love)while thoseexposed toLedZeppelin II orHendrix’sBandofGypsyswerestunted in theirgrowth.Toshowthat itwas in fact thedrumbeats of the likes of the legendarydrummers JohnBonham and Mitch Mitchell that were harming the plants, Retallackrepeatedherexperimentsusing recordingsof the samealbumsbutwiththepercussionblockedout.Asshehypothesized,theplantswerenotasdamagedastheyhadbeen

whentheywereblastedwiththefullversions,drumsincluded,of“WholeLotta Love” and “Machine Gun.” Could this mean that plants have apreferred musical taste that overlapped with Retallack’s? And on aworrisome note, as someone who grew up studying with Zeppelin andHendrixblaringfrommystereosystematall times, IwonderedwhenIfirstencounteredthisbookiftheseresultsimpliedthatItoocouldhavebeendamaged,asRetallackextrapolatesfromherresultstotheeffectofrockmusiconyoungpeople.FortunatelyformeandforthehordesofotherZeppelinfansoutthere,

Retallack’s studies were fraught with scientific shortcomings.Forexample,eachexperimentincludedonlyasmallnumberofplants(fewerthan five).Thenumber of replicates in her studieswas so small that itwas not sufficient for statistical analysis. The experimental designwaspoor—some of the studieswere carried out in her friend’s house—andparameters,suchassoilmoisture,weredeterminedbytouchingthesoilwith a finger.While Retallack cites a number of experts in her book,almostnoneof themarebiologists.Theyareexperts inmusic,physics,andtheology,andquiteafewcitationsarefromsourceswithnoscientificcredentials.Mostimportant,however,isthefactthatherresearchhasnotbeenreplicatedinacrediblelab.IncontrasttoIanBaldwin’sinitialstudiesonplantcommunicationand

volatile chemicals (encountered in chapter two), which were originallymet with resistance by the mainstream science community butsubsequently validated in many labs, Retallack’s musical plants havebeen relegated to the garbage bin of science.While her findings werereported in a newspaper article, attempts to publish her results in a

reputable scientific journal were unsuccessful, and her book waseventuallypublishedasNewAgeliterature.Thisofcoursehasn’tstoppedthebookfrombecomingpartoftheculturalzeitgeist.Retallack’s results also contradicted an important study published in

1965. Richard Klein and Pamela Edsall, scientists from the NewYorkBotanicalGarden,decidedtorunseveralteststodetermineifplantsweretrulyaffectedbymusic.TheydidthisinresponsetostudiescomingoutofIndiaclaimingthatmusicincreasedthenumberofbranchesthatwouldsprout in different plants, one of which was the marigold (Tageteserecta). In an attempt to recapitulate these studies, Klein and Edsallexposedmarigolds toGregorianchant,Mozart’sSymphonyno.41 inCmajor, “Three to Get Ready” by Dave Brubeck, “The Stripper”by theDavid Rose Orchestra, and the Beatles’ songs “I Want to Hold YourHand”and“ISawHerStandingThere.”

Marigold(Tageteserecta)

Klein and Edsall concluded from their study (which employed strictscientific controls) that music did not influence the growth of the

marigolds. As they reported, using humor to convey their generalindignation at this line of research, “There was no leaf abscissiontraceable to the influence of ‘The Stripper’ nor could we observe anystemnutation inplantsexposed toTheBeatles.”13Howcanweexplainthe contradiction between these results and Retallack’s subsequentstudies?EitherKleinandEdsall’smarigoldshaddifferentmusical tastefromRetallack’s plants, or,more likely, themajormethodological andscientificdiscrepanciesinRetallack’sstudyledtounreliableresults.While Klein and Edsall’s research was published in a respected

professional science journal, it was basically unseen by the generalpublic, and research likeRetallack’s continued todominate thepopularpressinthe1970s.ItisalsofeaturedprominentlyinPeterTompkinsandChristopher Bird’s iconic book from 1973,The Secret Life of Plants,whichwasmarketedasa“fascinatingaccountofthephysical,emotional,and spiritual relations between plants and man.” In a very lively andbeautifully written chapter titled “The Harmonic Life of Plants,” theauthors reported thatnotonlydoplants respondpositively toBachandMozart but they actually have amarked preference for the Indian sitarmusicofRaviShankar.14MuchofthesciencefeaturedinTheSecretLifeofPlantsreliedonsubjectiveimpressionsbasedononlyasmallnumberof test plants. The renowned plant physiologist, professor, and knownskepticArthur Galston put it succinctly when he wrote in 1974: “Thetrouble withThe Secret Life of Plants is that it consists almostexclusively of bizarre claims presented without adequate supportingevidence.”Butthishasn’tkeptTheSecretLifeofPlantsfrominfluencingmoderncultureeither.More recent datasupporting any significant plant response to sound

are lacking. However, careful examination of the scientific literaturerevealsresultspepperedthroughoutarticlesreportingotherfindingsthatdebunktheideathatplantscanhear.InJanetBraam’soriginalpaperonthe identification of theTCH genes (thegenes thatwereactivatedupontouching a plant), she explained that she checked if in addition tophysicalstimulation,thesegeneswereinducedbyexposuretoloudmusic

(which forher was provided by Talking Heads). Alas, they were not.Similarly, inPhysiology and Behaviour of Plants, the researcher PeterScott reported a series of experiments thatwere set up to testwhethercorn is influenced by music, specifically Mozart’sSymphonieConcertanteandMeatLoaf’sBatOutofHell. (It’samazingwhatthesetypesofexperimentscantellusaboutascientist’sownmusicaltaste.)Inthe first experiment, the seeds exposed to Mozart or Meat Loafgerminatedmorerapidlythanthoseleftinsilence.ThiswouldbeaboontothosewhohaveclaimedthatmusicaffectsplantsandabanetothosewhothinkMozartisqualitativelybetterthanMeatLoaf.

Corn(Zeamays)

But this is where the importance of proper experimental controlscomes into play. The experiment continued, but this time a small fancirculatedanyheatedairfromthespeakersawayfromtheseeds.Inthisnew set of experiments, there was no differencein germination ratesbetween the seeds left in silence and those exposed to music. The

scientists discovered in the first set of experiments that the speakersplaying the music had apparently radiated heat, which improvedgerminationefficiency;theheatwasthedeterminingfactor,notMozart’sorMeatLoaf’smusic.Keeping a skeptic’s view, let’s look again at Retallack’s conclusion

that the intensedrumbeatsof rockmusic aredetrimental toplants (andalso to people). Could there be an alternative, scientifically validexplanation for loud drumming having a negative effect on plants?Indeed, as I highlighted in the previous chapter, both Janet Braam andFrankSalisburyclearlyshowedthatsimplytouchingaplantanumberoftimes led todwarfed, stuntedplants,oreven toaplant’sdeath.So it isconceivable that heavy rock percussion, if pumped through the properspeakers,leadstosuchpowerfulsoundwavesthatplantsvibrateandareliterally“rocked”backandforthasifinawindstorm.InsuchascenariowewouldexpecttofindreducedgrowthinplantsexposedtoZeppelin,asisthecasereportedbyRetallack.Maybeit’snotthattheplantsdon’tlikerockmusic;maybetheyjustdon’tlikebeingrocked.Alas,untilitisprovenotherwise,itlooksasifallevidencetellsusthat

plantsareindeed“deaf,”whichisinterestingifyouconsiderthatplantscontainsomeofthesamegenesknowntocausedeafnessinhumans.

DeafGenesTheyear2000wasahallmarkfortheplantsciences.Itwastheyearthatthe sequence of the entireArabidopsis thaliana genome was finallycommunicatedtoscientistsaroundtheworld,andtheywerealleager tohear the results. More than three hundred researchers based atuniversities and biotechnology companies worked over four years todeterminetheorderofapproximately120millionnucleotidesthatmakeuptheDNAofthearabidopsis.Italsocostapproximatelyseventymilliondollars.(Themoneyandthecollectiveeffortassociatedwiththisprojectareunfathomabletoday,astechnologyhasprogressedtothepointwhere

asingle labcansequenceanarabidopsisgenomeina littleoveraweekforlessthan1percentoftheoriginalcost.)Arabidopsis was chosen by theNational Science Foundation back in

1990asthefirstplantthatwouldhaveitsgenomesequencedthankstoanevolutionary quirk that resulted in its having relatively little DNAcomparedtootherplants.Whilearabidopsishasalmostthesamenumberofgenes (twenty-five thousand) asmostplants andanimals, it containsvery little of a type of DNA called noncoding DNA, which madedeterminingitssequencerelativelyeasytodo.NoncodingDNAisfoundall over the genome, separating between genes, at the ends ofchromosomes,andevenwithingenes.Toputthingsinperspective:whilearabidopsis contains about twenty-five thousand genes in 120 millionnucleotides, wheat has the same number of genes in 16billionnucleotides (and human beings have about twenty-two thousand genes,fewerthanthepetitearabidopsis,in2.9billionnucleotides).15Becauseofits small genome, small size, and fast generation time, arabidopsisbecamethemostwidelystudiedplantinthelatetwentiethcentury,andasa result, research on this common weed has led to importantbreakthroughs in many fields. Almost all of the twenty-five thousandgenes found in ara-bidopsisarealsopresent inplants thatare importantagriculturally and economically, such as cotton and potato.Thismeansthat any gene identified in arabidopsis (say, a gene for resistance to aparticularplant-attackingbacteria)could thenbeengineered intoacroptoimproveitsyield.The sequencing of the arabidopsis and human genomes led tomany

surprising findings. Most relevant to our discussion here is that thearabidopsisgenomewasfoundtocontainmorethanafewgenesknownto be involved in diseases and disabilities in humans. (The humangenome,ontheotherhand,containsseveralgenesknowntobeinvolvedin plant development, such as a group of genes called the COP9signalosome that mediate plant responses to light.) As scientistsdeciphered the arabidopsis DNA sequence, they discovered that thegenomecontainstheBRCAgenes(whichareinvolvedinhereditarybreast

cancer),CFTR(whichisresponsibleforcysticfibrosis),andanumberofgenesinvolvedinhearingimpairments.An importantdistinctionmustbemade:whilegenes areoftennamed

for diseases associated with them, the gene doesn’t exist tocause thediseaseorimpairment.Adiseaseoccurswhenthegenedoesn’tfunctionproperlyasaresultofamutation,whichisachangein thesequenceofnucleotides thatbuilds thegene thatdisrupts theDNAcode.To refreshourunderstandingofbasichumanbiology:ourDNAcodeiscomprisedofonlyfourdifferentnucleotides,whichareabbreviatedA,T,C,andG.Thespecificcombinationofthesenucleotidesprovidesthecodefordifferentproteins. A mutation or a deletion of a few nucleotides cancatastrophically alter the code.TheBRCA aregenes that,whenmutatedor disrupted, can cause breast cancer, but under normal circumstancestheyplayakeyroleindetermininghowcellsknowwhentodivide.WhentheBRCAgenesdon’t functionnormally,cellsdividetoooften,andthiscan lead to cancer.CFTR isagene that,whenmutated,whendisrupted,causes cystic fibrosis but normally regulates the transport of chlorideionsacrossthecellmembrane.Whenthisproteindoesn’tworkproperly,chlorideiontransportinthelungs(andotherorgans)isblocked,leadingto the accumulation of thick mucus, which manifests clinically as arespiratoryailment.The names of these genes have nothing to do with theirbiological

functions, only their clinical outcome. What are these genes doing ingreenplants?ThearabidopsisgenomecontainsBRCA,CFTR,andseveralhundred other genes associated with human disease or impairmentbecause they are essential for basic cellular biology. These importantgeneshadalreadyevolvedsome1.5billionyearsagointhesingle-celledorganismthatwasthecommonevolutionaryancestortobothplantsandanimals.Ofcourse,mutationsinthearabidopsisversionsofthesehuman“disease genes” also disrupt the way the plant functions. For example,mutations in the arabidopsis breast cancer genes lead to a plantwhosestem cells (yes, arabidopsis has stem cells) divide more than normalcells,andthewholeplantishypersensitivetoradiation,bothofwhicharealsohallmarksofhumancancer.

This puts in perspective what a “deaf” gene is: a gene that—whenmutated—leads to deafness in humans. More than fifty human “deaf”geneshavebeenidentifiedbyvariouslabsworldwide,andatleasttenofthese fifty also show up in arabidopsis. Just because deaf genes werediscovered in the arabidopsis genome doesn’t mean that the plant canhear, just as the presence ofBRCA in arabidopsis doesn’t mean plantshavebreasts.Thehuman“deaf”geneshaveacellularfunctionnecessaryfor the ear to work properly, and when any of these genes contain amutation,theresultishearingloss.Fourofthearabidopsisgenesconnectedtohearingimpairmentencode

very similar proteins called myosins. Myosins are known as motorproteins, because they work as “nanomotors” that literally carry andmove different proteins and organelles around the cell.16 One of themyosins involved in hearing helps form the hair cells in the inner ear.Whenthismyosincontainsamutation,ourhaircellsdon’tformproperly,and theydon’t respondtosoundwaves. In theplantworld,wefind thatplants havehairlike appendageson their roots, aptly referred to as roothairswhichhelprootssoakupwaterandmineralsfromthesoil.Whenamutationoccursinoneofthefourarabidopsis“deaf”myosingenes,theroot hairs don’t elongate properly, and consequently the plants are lessefficientatabsorbingwaterfromthesoil.Myosin and the other genes found in both plants and humans have

similar functions at the cellular level. But when you put all the cellstogether, the function for the particular organism is different: we needmyosin to facilitate the proper functioning of our inner-ear hairs and,ultimately,tohear;plantsneedmyosinfortheproperfunctioningoftheirroothairs,whichallowsthemtodrinkwaterandfindnutrientsfromthesoil.

TheDeafPlantSeriousandreputablescientificstudieshaveconcludedthatthesoundsof

music are truly irrelevant to a plant.But are there sounds that, at leasttheoretically,couldbeadvantageousforaplanttorespondto?ProfessorStefano Mancuso, director of theInternational Laboratory of PlantNeurobiology at the University of Florence, has recently been usingsoundwavestoincreaseyieldinavineyardintheTuscanywineregion.Butthebasicbiologybehindthisagriculturaluseofsoundwavesisstillunclear.Dr.LilachHadany,atheoreticalbiologistatTelAvivUniversity,uses

mathematical models to study evolution. She proposes that plants dorespond to sounds but that we have yet to carry out the correctexperimentstodetecttheirdoingso.Indeedinscienceingeneral,lackofexperimental evidence does not equate to a negative conclusion. In hermind,wewouldhavetoconstructastudyinwhichwewoulduseasoundfromthenaturalworldknowntoinfluenceaspecificplantprocess.Onesuchsoundcouldbethebuzzingofbees.Inaprocessreferredtoasbuzzpollination,bumblebeesstimulateaflowertoreleaseitspollenbyrapidlyvibrating their wing muscles without actually flapping their wings,leadingtoahigh-frequencyvibration.Whilethisvibrationcanbeheard(it’sthebuzzwehearwhenabeefliesby),thepollenreleasenecessitatesa physical contact between the vibrating bee and the flower. So just asdeafpeoplecanfeelandrespondtovibrationsinmusic,flowersfeelandrespond tobumblebeevibrations,withoutnecessarilyhearing them.Butconceivably, the soundof the vibrations could also affect the flower insomeyetundetectedway.In a similar vein, Roman Zweifel and Fabienne Zeugin from the

University of Bern in Switzerland have reported ultrasonic vibrationsemanating from pine and oak trees during a drought. These vibrationsresultfromchangesinthewatercontentofthewater-transportingxylemvessels.Whilethesesoundsarepassiveresultsofphysicalforces(inthesameway thata rockcrashingoffacliffmakesanoise),perhaps theseultrasonicvibrationsareusedasasignalbyothertreestopreparefordryconditions?If scientists are going to properly study plant responses to sound

waves, we need to understand thatif a plant needs to hear, then its

auditory system would be much different from what has evolved inanimals. In addition to the few examples above, perhaps some plantssenseminuscule sounds that might be created by tiny organisms. Thatkindofsystemmaybeofftheradarscreenofmostphysiologicaltools.Whilethesepossibilitiesareinterestingtoponder,inlieuofanyhard

data to the contrarywemust conclude fornow thatplants aredeaf andthat they did not acquire this sense during evolution. The greatevolutionary biologist Theodosius Dobzhansky wrote, “Nothing inbiologymakessenseexcept in the lightofevolution.”Considering this,perhapswecanunderstandwhyhearing, asopposed to theother senseswe’vecovered,isn’treallyneededbyplants.Theevolutionaryadvantagecreatedfromhearinginhumansandother

animals serves asonewayourbodieswarnusof potentiallydangeroussituations. Our early human ancestors could hear a dangerous predatorstalking them through the forest. We notice the faint footsteps ofsomeone following us late at night on a poorly lit street.We hear themotorofanapproachingcar.Hearingalsoenablesrapidcommunicationbetweenindividualsandbetweenanimals.Elephantscanfindeachotheracross vast distances by vocalizing subsonicwaves that rumble aroundobjectsandtravelformiles.Adolphinpodcanfindadolphinpuplostintheocean through itsdistresschirps, andemperorpenguinsusedistinctcallstofindtheirmates.What’scommoninallofthesesituationsisthatsound enables a rapid communication of information and a response,which is often movement—fleeing from a fire, escaping from attack,findingfamily.Aswe’veseen,plantsaresessileorganisms,securedtothegroundby

their roots.While they cangrow toward the sun andbendwithgravity,theycan’tflee.Theycan’tescape.Theydon’tmigratewiththeseasons.They remain anchored in the face of an ever-changing environment.Plants also operate on a different timescale from animals. Theirmovements, with the conspicuous exception of plants likeMimosa andtheVenusflytrap,arequiteslowandarenoteasilynotedbythehumaneye.Assuch,plantshavenoneedfordetailedcommunicationthatcouldallowforaquickretreat.Therapidaudiblesignalswe’reusedto inour

worldare irrelevant toaplant.Plants lack the structures forpurposefulvocalization,and thesoundsof leaves in thewindorbranchescrackingunderourfeetdonotcommunicateanythingtotheplant.Forhundredsofmillions of years plants have thrived on earth, and the nearly 400,000species of plants have conquered every habitat without ever hearing asound.Butalthoughtheymaybedeaf,plantsareacutelyawareofwheretheyare,whatdirectionthey’regrowing,andhowtheymove.

FIVEHowaPlantKnowsWhereItIs

Ineversawadiscontentedtree.Theygripthegroundasthoughtheylikedit,andthoughfastrootedtheytravelaboutasfaraswedo.Theygowanderingforthinalldirectionswitheverywind,goingandcominglikeourselves,travelingwithusaroundthesuntwomillionmilesaday,andthroughspaceheavenknowshowfastandfar!

—JohnMuir

Shootsgrowup;rootsgrowdown.Thatseemssimpleenough,buthowdoplantsknowwhereupis?Youmightthinkit’sallduetosunlight,butiflight isaplant’smainsignal forup,howwould itknowwhereup isatnight?Orwhenit’smerelyaseedgerminatingunderneaththesoil?Andyoumight think thatdownhas todowith touchingdarkmoistsoil.Buttheaerialrootsofthebanyanandmangrovetreesalsoalwaysgrowdown,eventhoughtheystartseveralmetersupintheair.Scientistshavedocumented thatwhenaplanthasbeen turnedupside

down,itwillreorientitselfinaslow-motionmaneuver—likewhenacatisfallingandrightsitselfbeforeitlands—sothatitsrootsgrowdownanditsshootsgrowup.17Andnotonlydoplantsknowwhen they’reupsidedown,butexperimentshavealsoproventhatthey’reconstantlyawareofwheretheirbranchesare;theyknowifthey’regrowingperpendiculartothegroundoratanangleofftooneside,andtendrilsalwayshaveaprettygoodideaofwherethenearestsupport is tograbonto.Just thinkof thedodderplantthatmakescirclesintheairwhileitsearchesforasuitableplanttoparasitize.Buthowdoesaplantreallyknowwhereitisinspace?

Howisitthatweknow?Weknowbecauseofoursixthsense,andcontrarytopopularbeliefthe

sixthsense isnotESP; it’sproprioception.Proprioceptionenablesus toknow where different body parts are relative to each other, withouthaving to look at them.While our other senses areoutwardly oriented,receiving signals like light, odor, and sound from external sources,proprioceptionprovidesuswithinformationbasedsolelyontheinternalstatus of the body. It enables you to move your legs in a coordinatedfashiontowalk,toswingyourarmtocatchabaseball,andtoscratchanitchonthebackofyourneck.Withoutproprioception,asimpletasklikebrushingyourteethwouldbepracticallyimpossible.It’sthekindofsensethatwedon’tmuchconsiderunlessweloseit.If

you’ve ever been even slightly inebriated, you’ve experiencedcompromisedproprioception.It’swhypoliceofficersuseafieldsobrietytestondriverssuspectedofintoxication;thetest,whichinvolvessimplephysical“hand-eyecoordination”tasks,easilyrevealswhohasimpairedproprioceptionandwhodoesnot.Whenyou’resober,touchingyournosewith your eyes closedis a simple task. But people who are evenmoderatelydrunkwillfindthiseasytestmuchmoredifficult.Understandingproprioception is less intuitive thanunderstandingour

other senses because it lacks a clear focus organ. Vision is perceivedthrough the eyes; olfaction through the nose; and hearing through theears.Eventactilesensationthroughthenervesintheskiniseasyenoughto grasp. Proprioception, on the other hand, involves the coordinatedinputofsignals fromthe innerear,whichcommunicatesbalance,alongwithsignalsfromspecificnervesthroughoutthebodythatcommunicateposition.Adjacenttotheinner-earstructuresnecessaryforhearingisacomplex

system of miniature chambers called the semicircular canals and thevestibule,whichwork together to sense the position of your head. Thesemicircularcanals lieatrightangles toeachother,formingastructurethatresemblesagyroscope.Thecanalsarefilledwithfluid,andwhenourhead changes position, the fluid moves. Sensory nerves at the base ofeachcanalrespondtothewavesinthefluid,andbecausethecanalsare

situatedinthreedistinctplanes,they’reabletocommunicatemovementin all directions. The vestibule is also filledwith fluid, and it containssensory hairs as well as otoliths, small crystalline stones that literallysinkinresponsetogravity,addingextrapressure(andthusstimulation)on thesensoryhairs in thevestibule.This informsus ifweareupright,horizontal,orupsidedown.Thepressureoftheotolithsonthenervesindifferentareasofthevestibulehelpsusdifferentiateupfromdown.Thisfunction is thrown out of whack on some amusement park rides thatshaketheotolithsaroundsomuch,wehavenoideawhereweare.While the workings of the inner ear help us keep our balance, the

proprioceptivenerves throughoutourbodykeepeverythingcoordinated,and theproprioceptive receptors inform thebrainof thepositionofourlimbs.Thesenervesaredistinctfromtactilenervesthatsensepressureorpain and are located deepwithin our bodies in ourmuscles, ligaments,andtendons.Theanteriorcruciateligamentintheknee,forexample(alsoknownasACL),containsnerves thatcommunicateproprioceptive inputfrom the lower leg. A few years ago, I tore my ACL after beingchallengedbymysonontheskislopes.IwasverysurprisedtodiscoveraftertheaccidentthatIhadtroublewalking:Ikepttrippingovermyownfoot.Ihadlosttheproprioceptivepositioningsignalingofmyfoot—andeventuallyregaineditasmybrainbegantoreintegrateinformationfromothernervesinmylowerleg.Two main interrelated bodily processes depend on proprioception—

being aware of the relative position of parts of the body while at rest(staticawareness),andbeingawareoftherelativepositionofpartsofthebodywhileinmotion(dynamicawareness).Proprioceptionencompassesnotonlyoursenseofbalancebutourcoordinatedmotionaswell—fromthe simple wave of a hand, to the more complicated integration ofmovement and balance you need to walk down the street, to the verycomplexmovementsofanOlympicgymnastperformingasomersaultonabalancebeam.These twoprocesses—staticanddynamicawarenessofbody position—are also interrelated in plants and have been a focus ofmanybotanistsforyears.

KnowingUpfromDownIn1758—morethanacenturybeforeDarwin’slandmarkbookThePowerof Movement in Plants—Henri-Louis Duhamel du Monceau, a Frenchnavalinspectorandardentbotanist,observedthatifheturnedaseedlingupsidedown,itsrootwouldreorientitself inordertogrowdown,whileits shoot would bend and grow up toward the sky. This simpleobservation of roots growing as if pulled down by gravity (positivegravitropism) and shoots growing in the opposite direction against thispull(negativegravitropism)ledtoanumberofquestionsandhypothesesthathavecontinued to influence researchcarriedout in labsaround theworld.ManyscientistswhoreadwhatDuhamelhadtosayconcludedthatthewaysinwhichtherootsreorientedthemselveshadtodowithgravityindeed. But Thomas Andrew Knight, a fellow of the Royal Society,pointed out about fifty years later that “the hypothesis [of gravityaffectingplantgrowth]doesnotappeartohavebeenstrengthenedbyanyfacts.”WhilemanyscientistsinterpretedDuhamel’sobservationasproofthat gravity influences the ways a plant grows, none had carried outrigorousscientificexperimentationtotestthisidea,whichiswhatKnightsetouttodo.KnightwaspartofthelandedgentryandlivedinacastleintheWest

MidlandsregionofEngland,surroundedbyextensivegardens,orchards,andgreenhouses.Hewasnot trainedasa scientist,but aswascommonfor nineteenth-century aristocrats, he used his leisure time to pursuescientific knowledge, and he soon became especially skilled inhorticulture. In fact, he turned out to be one of the leading plantphysiologists of his time. For his studies on how plants know up fromdown,Knightdevelopedaverysophisticatedexperimentalapparatusthatnegated the effect of Earth’s gravity on plant growth whilesimultaneously applying a new centrifugal force that would act on theroots.Heconstructedawaterwheel thatwas turnedbyastreamrunningthroughhisestate,andheattachedawoodenplatetothewheelsothattheplate turnedwith thewheel.He fastened several beanseedlings aroundthe plate in various positions so that their root tips were facing in all

possibledirections—intothecenter,out,atanangle,andsoon.He let thewheel spin at the nauseating speed of 150 revolutions per

minuteforseveraldays.Theseedlingssomersaultedwitheachspinoftheplate.At the end of the treatment,Knight saw that all of the roots hadgrownoutfromthecenterofthewheel,whilealltheshootsgrewtowardthecenter.

ThisillustrationdepictsKnight’swaterwheelwithseedlingsonitbeforetheexperimentstartedandatitsend.

With his makeshift centrifuge, Knight had applied a force on theseedlings that mimicked gravitation and demonstrated that the rootsalwaysgrew in thedirectionof thiscentrifugal force—while the shootsgrew in the opposite direction. Knight’s work provided the firstexperimentalcorroborationforDuhamel’sobservations.Heshowedthatrootsandshootsrespondnotonlytonaturalgravity,asDuhamelshowed,but also to an artificial gravitational force supplied by hiswaterwheel-poweredcentrifuge.But thisstilldidn’texplainhowaplantcouldsensegravity.Interestinhowplantssensegravitypickedupagaintowardtheendof

thenineteenthcentury.Aswithsomanyquestionsintheplantsciences,itwas Darwin and his son Francis who performed the definitiveexperiments in the field,and in trueDarwinian fashion theycarriedout

an extremely detailed, exhaustive study, in this case to determinepreciselywhichpartof theplantsensesgravity.Their initialhypothesiswas that “gravireceptors” (analogous to photoreceptors for light) werelocated in the tip of the root. To test their hypothesis, they sliced offdifferentlengthsoftheroottipsofbeans,peas,andcucumbersandthenplacedtherootsontheirsidesoverdampsoil.Whiletherootscontinuedto elongate, they no longer had the ability to reorient their growth andbenddownintothesoil.Eventheamputationofonly0.5mmofthetipwas enough to obliterate the plant’s overall sensitivity to gravity! TheDarwins also noticed that if the tip of a root grew backwithin severaldays of the amputation, the root would regain its ability to respond togravityandwouldgobacktoitsoldways,bendingdownintothesoil.ThisresultwassimilartowhatDarwindiscoveredwhenheconducted

hisresearchinphototropism.Inhisphototropismexperiment,heshowedthat the tipofashootseesthelightandtransfers this informationtoitsmidsection to tell it tobend toward the light.Here,Darwinandhis sonshowedthatthetipoftherootfeelsthegravity,eventhoughthebendingoccursfartheruptheroot.FromthisDarwinfurtherhypothesizedthattheroot tip somehowsent a signalup the restof the root to tell it togrowdownwiththegravityvector.Totestthishypothesis,Darwinplacedabeanseedlingonitssideand

immobilizeditwithapinonthetopofsomesoil,butthistimehewaitedninety minutes before he amputated the root tip (with a normal plantplaced on its side, it usually takes severalhours before the root’sreorientation is obvious). He found that the root still reorienteddownwardeventhoughitwas“tipless.”Duringtheninetyminutesbeforehesevered the tip,Darwinassumed thebeanplanthadsent instructionsuptherootthattoldtheplanttobenddown.Darwinandhissonwitnessedthesameresultsinsimilarexperimentswithsixdifferenttypesofplantsand in cases inwhich they burned the tipwith silver nitrate instead ofamputating it.Theyconcluded that the root tipmust immediatelysensegravity and then pass this information along, telling the plant whichdirectionisoptimalforitsgrowth.

Darwinsecuredbean(Viciafaba)seedlingsontheirsideswithpinsfortwenty-threehoursandthirtyminutes.InA,B,andC,hecauterizedtheroottipswithsilvernitrate(ratherthansimplyamputatingtheroottip).TherootsinD,E,andFwereleftuntreated.

Our understanding of how a plant knows up from down progressedremarkably over the course of the eighteenth and nineteenth centuries.FirstDuhamelrevealedthatseedlingsreorienttheirgrowthsothatrootsgrowdownandshootsup,thenKnightdemonstratedthatgravitywasthereasonforthis“up-downgrowth,”andthentheDarwinsshowedthattheroot tip contains the mechanism that senses the gravity. More than acentury would pass before modern molecular genetic studies wouldconfirmDarwin’sresults,demonstratingthatthecellsintheextremeendoftheroot(inaregioncalledtherootcap)sensegravityandhelpaplantknowwheredownis.Ifaplantneedsitsroottipstobeintactinordertogrowdowntothe

ground, you might expect (as Darwin did) that the tip of the shoot isessential for the plant to grow up toward the sky. After all, Darwinshowedthatcuttingoffthetoppartofaplantcausesittoloseitsabilitytoseeandbendto lightcomingfromtheside.Butsurprisingly, it turnsoutthataplantthat’shadthetipofitsshootchoppedoffwillstillgrowup; it retains itsability fornegativegravitropism.Could thismean thattherootandtheshootsensegravityindifferentways?Much of our current understanding of the ways in which plants

perceive gravity has come from studies that use everyone’s favoritelaboratory plant, arabidopsis. Just as Maarten Koornneef and hiscolleagues isolated “blind” plants that were defective in differentphotoreceptors(aswesawinchapterone),manyscientistshaveisolatedmutantarabidopsisplantsthatdon’tknowupfromdown.Theprocedureisactuallyquitesimple:scientistsgrowthousandsofmutantarabidopsisseedlings for a week and then flip their containers by ninety degrees.Almostalltheseedlingswillreorientsothattheshootgrowsupandtherootsdown.Buttheraremutantthatdoesn’tsensethegravitywillkeepgrowingwithoutanychangeinitsdirection.18Many of these mutants have defects in their roots as well as their

shoots,and they’ve lost theability toknowupfromdown.But inothermutantarabidopsis,onlytherootortheshootisaffected,whichsuggeststhat they detect gravity in different ways. For example, an arabidopsismutant in the gene termedscarecrow has shoots that don’t knowwhenthey’ve been placed on their side, so themutant plant stays horizontal(it’sdefectiveinnegativegravitropismintheshoot).19Butsurprisingly,rootsinthismutantknowhowtogrowdown(therootsmaintainpositivegravitropism).A Japanesemorning glory cultivar calledShidareasagao(whichmeans“weeping”)hasshootsthatdon’tknowupfromdown;sure,itmakesforanattractiveornamentalhangingplant,butitalsoprovidesscientists with a great mutant to study gravitropism.What makes thisplant’s stems and leaves grow in varied directions? Recent geneticstudies demonstrate thatShidare-asagao contains a mutation in itsscarecrow gene, in fact. Which begs the question: Do these mutantsultimately prove that the mechanism for sensing gravity differs in thepartsoftheplantabove-andbelowground?Actually, this mutant doesn’t tell us that themechanism for sensing

gravity is different in the root and stems, but it does tell us that thespecificsiteisdifferent(whichwealreadyknewfromDarwin’sstudies).Scientists in Phil Benfey’s lab at New York University used thescarecrow mutant to figure out which part of the stem senses gravity.Around the turn of the twenty-first cen-turythey discovered that the

scarecrowgeneisnecessaryfortheformationoftheendodermis,agroupofcellsthatwraparoundthevasculartissuesoftheplant.Intheroots,theendodermisacts as a selectivebarrier that actively regulateshowmuchandwhichcompounds(suchaswater,minerals,andions)enterthexylemtubes for transport to the green parts of the plant. Plants that have amutatedscarecrow gene don’t have any endodermis.While thismakesforrathershortandweakroots,theystillknowhowtogrowdown.Theyknow this because the root’s gravisen-sors in the tip do not containendodermiscells.Thescarecrowmutantstillhasanormalroottip,soitknowswheredownis.

Morningglory(Pharbitisnil)

Butifshootsdon’thaveanendodermis,theycan’tknowwhereupis,andthat’sasdetrimentaltoaplant’ssenseofdirectionasamputatingtheroot tip. In other words, two distinct planttissues detect gravity in thelower andaerial partsof theplant. In the roots, it’s the root tip; in thestem, it’s theendodermis.Sowhileour“gravireceptors”areonly in the

innerear,plantshavetheminmanyplacesintheirroottipsandintheirstems.Howdo these specificgroupsofplantcells in the root tipand in the

endodermis sense gravity? The first answers came from studies of therootcapusingamicroscopetoseetheirincrediblesubcellularstructures.Cellsinthecentralareaoftherootcapcontaindenseball-likestructurescalledstatoliths(derivedfromtheGreekfor“stationarystone”),which—similartotheotolithsinourears—areheavierthanotherpartsofthecellandfalltothebottomsideofthecellsoftherootcap.20Whenarootisplacedonitsside,thestatolithsfalltothenewbottomofthecelljustasmarbles would roll to the bottom part of a jar on its side. Notsurprisingly, the only aerial plant tissue that contains statoliths is theendodermis. Just as in the root cap, when a plant is on its side, thestatoliths in theendodermis fallontowhatwas thesideof thecell, andthis part becomes the new bottom of the plant. Theways inwhich thestatoliths responded togravity led scientists topropose that they are infactthegravityreceptors.If statoliths are the plant gravity receptors, then the simple

displacementofstatolithsshouldbesufficienttocauseaplanttochangeitsdirectionofgrowthasifithadbeenaffectedbygravity.Onlywiththeadvent of molecular genetics and, interestingly enough, spaceflight—whichI’llgettoinamoment—havescientistsbeenabletocarryouttheexperimentsthatengagewiththisquestion.For the past twenty years, John Kiss and his colleagues atMiami

UniversityinOhiohavebeenusingsomeofthecoolesttoysinsciencetodetermine whether statoliths really are what sense gravity in a plant.Usingahigh-gradientmagneticfieldthatsimulatesgravity,Kissinducedhis statoliths tomigrate laterallyas ifhehad turned theplantson theirsides.When this happens, the roots start to bend in the same directionthatthestatolithsmove:ifthestatolithsmovetotheright,therootbendsto theright; if thestatolithsmove to the left, the rootbends to the left.These results really supported the idea that the position of statoliths iswhattellsaplantwheredownis.TheyalsoledKisstopredictthatinthe

absence of gravity, statolithswouldn’t fall to the bottomof a cell, andthus a plant won’t know where down is. Of course to test such ahypothesis,Kisswouldneedconditionswithnogravity,asinaspacecraftorbitingEarth.Aboardthespaceshuttle,whereplantsobviouslydon’texperiencethe

effects of gravity, the statoliths can’t fall, and they remain naturallydistributed throughout the cell.Under theseweightless conditions,Kisscould not detect any gravitropic bending in the plants thatwere out inspace.Thesestudiesrevealedafascinatingclue towhyplantsmovetheway they do: a plant needs statoliths to sense gravity, just as we needotolithsinourearstostimulateourbalancereceptors.

TheMovementHormoneThewaysinwhichaninvertedbeanrootrespondstogravity,andatulipin awindowboxmoves toward the sun, and aCuscuta sidles up to theneighboring tomato are similar: the plants sense a change in theirenvironments (gravity, light, or smell) and bend in response to thestimulus.Thestimuliarediverse,buttheresponsesaresimilar—growthinaparticulardirection.We’vedealtalotwithhowaplantsensesgravity(and light and smells), but we haven’t explored how this sensoryinformation tells a plant to grow and bend. Let’s reexamine Darwin’sexperimentsonphototropismfromthefirstchapter.Heshowedthat thetipofthegrassseedling“sees”thelightandtransfersthisinformationtoitsmidsectioninordertotellittobendtowardthelight.Thisissimilartotherootcap“feeling”thegravityandthentransferringtheinformationupthe root to induce the plant to grow downward, or to theCuscuta thatsmellsthetomatoandthenbendstowardit.At the beginning of the twentieth century, the Danish plant

physiologistPeterBoysen-JensenexpandedontheDarwins’experimentsonphototropism.LikeDarwin,hecutoffthetipsofhisoatseedlings,butbeforereturningthetipstotheirplantstumps,hedidsomethingunusual

butquitebrilliantinitsway.Heplacedeitherathinslabofgelatinoratinypieceofglassbetween thestumpand the tip.Whenhe illuminatedtheseplantsfromtheside,theonewiththegelatinslicebenttowardthelight,whiletheonewiththeglassstayedstraight.ThisprovedtoBoysen-Jensenthat thebendingsignalcomingfromthetipoftheplantmustbesoluble since it couldclearlypass through thegelatinbutnot theglass.YetBoysen-Jensendidn’tknowwhatthechemicalwasthattraveledfromthetipdowntothestalktomakeitbend.In the early 1930s scientists finally identified the growth-promoting

chemicalthatpassedfromthetipthroughthegelatinanddownthestockandcalleditauxin,whichderivesfromtheGreekfor“toincrease.”Whileplantshavemanydifferenthormones,noneareasprevalentor involvedinasmanyprocessesandfunctionsasauxin.Oneofthesefunctionsistotellcellstoincreasetheirlength.Lightcausesauxintoaccumulateonthedark side, causing the stem to elongate on the dark side only,whichresults in the stem bending toward the light. Gravity makes the auxinappearonthe“upside”ofroots,whichcausesthemtogrowdown,andonthe “down side” of stems and leaves, causing them to grow up.Whiledifferentstimulationsactivatedifferentplantsenses,manyoftheplant’ssensorysystemsconvergeonauxin,themovementhormone.

Oats(Avenasativa)

DancingPlantsAs mentioned earlier in this chapter, proprioception is more than justknowingupfromdown;it’salsoknowingwherethebodypartsarewhenyou are moving. When Mikhail Baryshnikov leaps across a stage andlands inanarabesque,he’snotonlyperfectlybalancedbutalsoacutelyawareofthepositionofeverypartofhisbody.Heknowshowfarhislegisstretchedoutbehindhim,howhighhishandisfromhisshoulder,theexacttiltofhistorso.Ofcourse,it’snosurprisethatweregardplantsasstationarybeings;theyaresessileorganismsthatareeternallyrootedandincapableoflocomotion.Butwhenweobservethempatientlyoveralongperiod of time, this stationary stature gives way to an intricatelychoreographedfestivalofmovement,muchlikeBaryshnikovspringingtolifeinthefirstsceneofaballet.Leavescurlandunfold,flowersopenandclose,andstemscircleandbend.Thesemovementsarebestseenintime-lapsephotography,andoneof

the first uses of time-lapse photography was, in fact, to do just this.

ProfessorWilhelmPfeffer,whotrainedwithDarwin’sfriendJuliusvonSachs, filmed a variety of plants in motion, from tulips toMimosa tobroadbeans.Hisearlymoviesaregrainyyetfascinatingtowatch.21Longbefore time-lapse photography came into play, however, the persistentand dogged Darwin studied plant movements using a very time-consuming,low-techprocedure:hesuspendedaglassplateaboveaplantandmarked on the glass the position of the tip of the plant every fewminutes for several hours. By connecting the dots, he mapped out theexact movements of his subject. (An insomniac, Darwin undoubtedlyspent more than a few nights meticulously monitoring the more thanthree hundred different species that he eventually recorded in thisfashion,includingthewildcabbagedepictedonthefollowingpage.)Darwin found that all plants move in a recurring spiral oscillation,

whichhetermed“circumnutation”(Latinfor“circle”or“sway”).22Thisspiral pattern varies between species and can range from a repeatingcircletoanellipsetoatrajectoryofinter-lockingshapesmuchliketheimages from a Spirograph. Some plants have surprisingly largemovements, such as bean shoots, which circle in a radius of up to tencentimeters.Othersmoveinmillimeters,likestrawberrybranches.Speedisanothervariable;tulipscircumnutateataratherfixedspeed(theytakeaboutfourhours),whileotherplantsvarysignificantly:arabidopsisstemstake between fifteenminutes and twenty-fourhours for one circle, andwheatusuallycompletesarotationonceeverytwohours.Wedon’tknowwhatthebasisforthisindividualityinmovementis,butwedoknowthatboth environmental and internal factors can influence speed. As thePolishscientistMariaStolarzfound,ifsheusedasmallflametoburnasunflower leaf for only three seconds, the circling time of the plantalmostdoubledforonerotation.Thenthesunflowerwouldbouncebacktoitsinitialrate.

Darwin’straceofthemovementsofthetipofawildcabbage(Brassicaoleracea)seedlingovertenhoursandforty-fiveminutes

Darwin was fascinated by these movements, and he came to theconclusionnotonlythatcircumnutationwashardwiredintothebehaviorofallplantsbutthatthesespiralingoscillatorydanceswereactuallythedrivingforceforallplantmovements.Heproposedthatphototropismandgravitropism were just modified circumnutations aimed in a specificdirection.Thishypothesisremainedunchallengeduntilsomeeightyyearslater,whenDonaldIsraelssonandAndersJohnssonattheLundInstituteofTechnologycameupwithanalternativehypothesisthattheoscillatorymovements of plantswere simply aresult of gravitropism (and not thecause).Asaplantgrows,theyargued,aslightchangeinthepositionofthestem(whethercausedbywind,light,oraphysicalbarrier)willresultinthedisplacementofthestatoliths,whichinturnwilltriggerthestemtobendup,evenasexternalfactorspushitspositionaroundabit.

Sunflower(Helianthusannuus)

This bending, however, often overshoots its goal. Just like those oldBozotheClownpunchingbagsthatkeepbouncingbackupatyou,whenastem reorients itself vertically, it first overshoots straight up and downand bends somewhat in the opposite direction.Now that the stem isn’tstraight again, but oriented in the other direction, the statolithsredistribute a second time, initiatinga gravitropic response toward theoppositesideof theplant.Thisnewgrowthwillalsoovershoot,andthecycle repeats, leading to the classic oscillatory movement that Darwindocumented for cabbage and clover and that we see in tulips andcucumbers.JustasBozotheClowngoesbackandforthincirclestryingtofinditscenter,thestemoftheplantcirclesintheairasitsearchesforbalance.SoDarwinhypothesizedthatthesedancesareabuilt-inbehaviorofall

plants, while Israelsson and Johnsson believed that gravity powers thecirclingdancesofplants.Andfinally, the twocompeting theoriescouldbeput tothetestbytheendof thetwentiethcenturywiththeadventofspaceflight. If Darwin’s theory is correct, circumnutations wouldcontinue unimpeded in the absence of gravity; if Israelsson andJohnsson’s statolith-centered model is correct, the circumnutation inplantswouldnotoccurinspace.

Backintheinfancyofthespaceprograminthe1960s,AllanH.Brown,awell-knownandrespectedplantphysiologist,conceivedoneofthefirstexperimentswitharabidopsisinspaceinwhatwaspartoftheBiosatelliteIII program. Brown wanted to test whether plant movements wouldcontinueintheabsenceofgravity.23Whentheprogramwascanceledduetobudget cuts,Brownhad towait until 1983,whenhis experimentsonplantswere among the first to be carried out on the space shuttle. TheastronautsonboardthespaceshuttleColumbiamonitoredthemovementsofsunflowerseedlingswhiletheywereinorbitandtransmittedthedatatoscientistsonEarth.SunflowerseedlingsexhibitrobustmovementsonEarth,sotheyweretheidealplanttolobupwiththeshuttletoseewhatwouldhappen in space.AboardColumbia,milesandmilesaboveEarth,almost100percentoftheseedlingsexhibitedrotationalgrowthpatterns;even in the near absence of gravity, the sunflower seedlings continuedtheir gyrations in the same way they did on Earth. This stronglysupportedDarwin’stheory.But let’s revisit the second hypothesis: that spiraling is intimately

connected to gravity. A few years ago, Hideyuki Takahashi and hiscolleagues at the Japan Aerospace Exploration Agency monitoredcircumnutationinthemorningglorymutantthatlackedagravity-sensingendodermisinitsshoot.Themorningglorymutantthatdidn’trespondtogravity also didn’t move in the spiraling style that a normal morningglorydoes.Furthermore,arabidopsismutantsthathavesmallordefectivestatoliths also didn’t spiral. These results wouldn’t have made Darwinhappy: they strongly support the idea that circumnutation andgravitropism are intimately connected (of course, Darwin would likelyhave appreciated the science here, modified his own hypotheses, anddevelopednewexperimentstotestthem).Takahashi explained the contradiction between his results and those

garnered onColumbia by suggesting that since the experiments on theshuttle were carried out on seedsgerminated on Earth, this may havebeenenoughtoperpetuatecircumnutationoutinspace.Indeed,itwouldmake sense that a seed formed on Earth would have different

characteristicsfromoneformedinspace,andifso,thetimelimitationofthe experiments carried out onColumbia (about ten days) may haveinfluencedtheoutcomeoftheexperiment.TheInternationalSpaceStation,whichbeganoperationin2000,finally

providedafacilityforlong-termexperimentsontheeffectofgravityonplants.AndersJohnssoncouldputhisnearlyforty-year-oldhypothesistothe testwhenheandhisNorwegiancolleaguescarriedoutan importantexperimentaboard thespacestationoverseveralmonths in2007.Theirsetup consisted of arabidopsis plants that germinated aboard the spacestationandweregrown ina special chamberdesigned foruse in space.They were automatically photographed every few minutes in order tomonitor their exact positions and detect any movements. In the near-weightless conditions of the space station, the arabidopsis plantsexhibited spiral patterns of movement, albeit very minute ones,demonstratingthemovementsthatDarwinhadpredictedandconfirmingBrown’sownobservations.Buttheradiusofthecircularmovement,andthespeedofmovement,werelessthanthosefoundonEarth,suggestingthatgravitywasessentialforamplifyingthebuilt-inmovement.Theseweightlessplantswereplacedonalargerotatingcentrifugethat

mimickedgravitation,muchasKnight’swaterwheelhadyearsandyearsearlier. The plants could be continuouslymonitored by a camerawhilethey rotated. Very soon after feeling the g-force, the plants startedmoving inmoreexaggeratedcircles.Both the sizeand the speedof themovementsof thespinningplantsweresimilar to thosedetectedon thearabidopsis plants grown on Earth. This revealed that gravity is notnecessary for the movements, but rather modulates and amplifies theendogenousmovements in the plant. Darwin was correct: as far as weknow, circumnutation is a built-in behavior of plants, but this behaviorneedsgravitytoreachitsfullexpression.24

TheBalancedPlant

Aplantcanbepulledinmanydirectionsatonce.Sunlighthittingaplantatananglecausesittobendtowardtherays,whilethesinkingstatolithswithin theplant’sbendingbranches tell it to straightenup.Theseoftenconflicting signals enable a plant to situate itself in a position that isoptimal for its environment. The tendrils of a vine, searching for asupport to grab onto, will be attracted to the shade of the neighboringfence,andgravitywillenablethevinetorapidlytwirlaroundit.Aplantonawindowsillwillbepulledbythelightandgrowtooneside,towardthe sunnypartof the sill,while the forceofgravitywill influence it togrowupat thesame time.Thesmellof the tomatowillpullCuscuta tothe side, while gravitropismwill push it to keep growing upward. Justlike Newtonian physics, the position of any part of the plant can bedescribedasasumoftheforcevectorsactinguponitthattellaplantbothwhereitisandwhichdirectiontogrow.Humansandplantsrespondtogravityinsimilarwaysandrelyonour

sensorstoinformusofourpositionsandbalance.Butwhenwemove,wenot only know where our body parts are in relation to others but alsorememberthemovement,whichallowsustorepeatthemovementagainandagain.Canaplantrememberitspastmovementstoo?

SIXWhataPlantRemembers

Theoaksandthepines,andtheirbrethrenofthewood,haveseensomanysunsriseandset,somanyseasonscomeandgo,andsomanygenerationspassintosilence,thatwemaywellwonderwhat“thestoryofthetrees”wouldbetousiftheyhadtonguestotellit,orweearsfineenoughtounderstand.

—MaudvanBuren,QuotationsforSpecialOccasions

Memories often take up a good portion of an average person’s dailymental wanderings.We may remember an especially savory feast, thegamesweplayedaschildren,oraparticularlyhumorous incidentat theofficefromthedaybefore.Wecanenvisionabreathtakingsunsetthatweoncesawonthebeach,andwealsoremembersignificantlytraumaticandscaryexperiences.Ourmemoryisdependentonsensoryinput:afamiliarsmell or a favorite song can trigger a wave of detailed memory thattransportsusbacktoaparticulartimeandplace.Aswe’ve seen, plants benefit from rich andvaried sensory inputs as

well.Butplantsobviouslydon’thavememories in thewaywedo: theydon’tcoweratthethoughtofadroughtordreamaboutthesunbeamsofsummer. They don’tmiss being encased inside a seedpod, nor do theyfeelanxiousaboutprematurepollenrelease.UnlikeGrandmotherWillowin Disney’sPocahontas, old trees don’t remember the history of thepeople who have slept in their shade. But as we’ve seen in earlierchapters,plantsclearlyhavetheabilitytoretainpasteventsandtorecall

thisinformationatalaterperiodforintegrationintotheirdevelopmentalframework: Tobacco plants know the color of the last light they saw.Willowtreesknowiftheirneighborshavebeenattackedbycaterpillars.These examples, and many more, illustrate a delayed response to apreviousoccurrence,whichisakeycomponenttomemory.Mark Jaffe, the same scientist who coined the term

“thigmomorphogenesis,” published one of the first reports of plantmemoryin1977,thoughhedidn’tcallitassuch(instead,hetalkedaboutone- to two-hour retention of the absorbed sensory information). Jaffewantedtoknowwhatmakespeatendrilscurlwhentheytouchanobjectsuitabletowrapthemselvesaround.Peatendrilsarestem-likestructuresthatgrowinastraightlineuntiltheyhappenuponafenceorapoletheycanuseforsupport,andthentheyrapidlycoilaroundtheobjecttograbontoit.Jaffedemonstratedthatifhecutatendriloffofapeaplantbutkeptthe

excised tendril in awell-lit,moist environment, he could get it to coilsimplybyrubbingthebottomsideofthetendrilwithhisfinger.Butwhenheconductedthesameexperimentinthedark,theexcisedtendrilsdidn’tcoilwhenhetouchedthem,whichindicatedthatthetendrilsneededlighttoperformtheirmagic twirling.Butherewas the interestingcatch: ifatendriltouchedinthedarkwasplacedinthelightanhourortwolater,itspontaneouslycoiledwithout Jaffehaving to rub it again.Somehow, herealized, the tendril that had been touched in the dark had stored thisinformation and recalled it once he placed it in the light. Should thisstorageandlaterrecollectionofinformationbeconsidered“memory”?In fact, research on human memory conducted by the renowned

psychologistEndelTulvingprovides uswith an initial foundation fromwhich to explore plants and their unique “recollections.” Tulvingproposed that humanmemory exists on three levels. The lowest level,proceduralmemory,referstononverbalrememberingofhowtodothingsand is dependent on the ability to sense external stimulation (likerememberingtoswimwhenyoujumpinapool).Onthesecondlevelissemanticmemory,thememoryofconcepts(likemostofthesubjectswelearnedinschool).Andthethirdlevelisepisodicmemory,whichrefers

to remembering autobiographical events, like funny costumes fromchildhoodHalloweenpartiesorthelosswefeltatthedeathofadearpet.Episodicmemoryisdependentonthe“self-awareness”oftheindividual.Plants clearly do notmake the cut for semantic and episodicmemory:these are thememories that define us as human beings. But plants arecapableofsensingandreacting toexternalstimulation,sobyTulving’sdefinitionplants should be capable of proceduralmemory.And indeed,Jaffe’speaplantsillustratethis.TheysensedJaffe’stouch,rememberedit,andcoiledinresponse.Neurobiologists know quite a bit about the physiology of memories

andcanpinpointthedistinct(butstill interconnected)areasofthebrainthatare responsible fordifferent typesofmemory.Scientistsknow thatelectricsignalingbetweenneuronsisessentialformemoryformationandstorage.Butweknowmuchlessaboutthemolecularandcellularbasisofmemory.What’s fascinating is that the latest research hints that whilememoriesareinfinite,onlyaverysmallnumberofproteinsareinvolvedinmemorymaintenance.Weneedtobeaware,ofcourse,thatwhatwerefertoas“memory”for

people is actually a term that encompasses many distinct forms ofmemory, beyond the ones described by Tulving. We have sensorymemory,whichreceivesandfiltersrapidinputfromthesenses(inablinkofaneye);short-termmemory,whichcanholduptoaboutsevenobjectsin our consciousness for several seconds; andlong-termmemory, whichreferstoourabilitytostorememoriesforaslongasalifetime.Wealsohavemusclemotor memory, a type of procedural memory that is anunconsciousprocessoflearningmovementssuchasmovingfingerstotiea shoelace; andimmune memory, which is when our immune systemsrememberpast infections inorder to avoid futureones.Allbut the lastaredependentonbrain functions. Immunememory isdependenton theworkingsofourwhitebloodcellsandantibodies.What’s common to all forms of memory is that they include the

processes of forming thememory (encoding information), retaining thememory(informationstorage),andrecallingthememory(retrievaloftheinformation). Even computer memory employs exactly these three

processes. Ifwe’regoing to look for theexistenceofeven the simplestmemoriesinplants,thesearetheprocessesweneedtoseehappening.

TheShort-TermMemoryoftheVenusFlytrapAswesawbackinchapterthree,theVenusflytrapneedstoknowwhenan ideal meal is crawling across its leaves. Closing itstrap requires ahugeexpenseofenergy,andreopeningthetrapcantakeseveralhours,soDionaea only wants to spring closed when it’s sure that the dawdlinginsectvisitingitssurfaceislargeenoughtobeworthitstime.Thelargeblackhairson their lobesallowtheVenusflytraps to literallyfeel theirprey,andtheyactastriggersthatspringthetrapclosedwhentheproperpreymakesitswayacrossthetrap.Iftheinsecttouchesjustonehair,thetrapwill not spring shut; but a large enough bugwill likely touch twohairs within about twenty seconds, and that signal springs the Venusflytrapintoaction.Wecanlookatthissystemasanalogoustoshort-termmemory.First,

the flytrapencodes the information (forms thememory) that something(it doesn’t knowwhat) has touched one of its hairs. Then it stores thisinformation for a number of seconds (retains the memory) and finallyretrieves this information (recalls the memory) once a second hair istouched.Ifasmallanttakesawhiletogetfromonehairtothenext,thetrap will have forgotten the first touch by the time the ant brushes upagainst the next hair. In other words, it loses the storage of theinformation, doesn’t close, and the ant happilymeanders on.Howdoesthe plant encode and store the information from the unassuming bug’sencounterwith the first hair?How does it remember the first touch inordertoreactuponthesecond?Scientists have been puzzled by these questions ever since John

Burdon-Sanderson’searly reporton thephysiologyof theVenusflytrapin 1882. A century later, Dieter Hodick and Andreas Sievers at theUniversity of Bonn in Germany proposed that the flytrap stored

informationregardinghowmanyhairshavebeentouchedintheelectricchargeofitsleaf.Theirmodelisquiteelegantinitssimplicity.Intheirstudies,theydiscoveredthattouchingatriggerhairontheVenusflytrapcausesanelectricactionpotentialthatinducescalciumchannelstoopeninthetrap(thiscouplingofactionpotentialsandtheopeningofcalciumchannels is similar to the processes that occur during communicationbetween human neurons), thus causing a rapid increase in theconcentrationofcalciumions.Theyproposedthatthetraprequiresarelativelyhighconcentrationof

calciuminordertocloseandthatasingleactionpotentialfromjustonetriggerhairbeingtoucheddoesnotreachthislevel.Therefore,asecondhair needs tobe stimulated topush the calciumconcentrationover thisthresholdandspring the trap.Theencodingof the information is in theinitial rise in calcium levels. The retention of the information requiresmaintaining a high enough level of calcium so that a second increase(triggeredbytouchingthesecondhair)pushesthetotalconcentrationofcalciumover the threshold.As thecalcium ionconcentrationsdissipateover time, if the second touch and potential don’t happen quickly, thefinalconcentrationafterthesecondtriggerwon’tbehighenoughtoclosethetrap,andthememoryislost.Subsequent research supports this model.Alexander Volkov and his

colleaguesatOakwoodUniversity inAlabamafirstdemonstrated that itis indeed electricity that causes theVenus flytrap to close. To test themodel they rigged up very fine electrodes and applied an electricalcurrenttotheopenlobesofthetrap.Thismadethetrapclosewithoutanydirecttouchtoitstriggerhairs(whiletheydidn’tmeasurecalciumlevels,thecurrentlikelyledtoincreases).Whentheymodifiedthisexperimentbyalteringtheamountofelectricalcurrent,Volkovcoulddeterminetheexactelectricalchargeneededfor the trap toclose.As longas fourteenmicrocoulombs—a tinybitmore than the static electricitygenerated byrubbing two balloons together—flowed between the two electrodes, thetrapclosed.Thiscouldcomeasonelargeburstorasaseriesofsmallerchargeswithin twenty seconds. If it took longer than twenty seconds toaccumulatethetotalcharge,thetrapwouldremainopen.

Here,then,liestheproposedmechanismoftheshort-termmemoryintheVenusflytrap.Thefirsttouchofahairactivatesanelectricpotentialthatradiatesfromcelltocell.Thiselectricchargeisstoredasanincreasein ion concentrations for a short time until it dissipates within abouttwentyseconds.Butifasecondactionpotentialreachesthemidribwithinthistime,thecumulativechargeandionconcentrationspassthethresholdand the trapcloses. If toomuch timeelapsesbetweenactionpotentials,thentheplantforgetsthefirstone,andthetrapstaysopen.This electric signal in the Venus flytrap (and the electric signals in

otherplantsforthatmatter)aresimilartotheelectricsignalsinneuronsin humans and indeed all animals. The signal in both neurons andDionaea leaves can be inhibited by drugs that block the ion channelswhich open in themembranes as the electric signal passes through thecell. When Volkov pretreated his plants with a chemical that inhibitspotassiumchannelsinhumanneurons,forexample,thetrapsdidn’tclosewhentheyweretouchedorwhentheyreceivedtheelectriccharges.

Long-TermMemoryofTraumaIn themid-twentiethcentury,someratherobscureworkwascarriedoutby the Czech botanist Rudolf Dostál, who studied whathe termed“morphogeneticmemory”inplants.Morphogeneticmemoryisatypeofmemory that later influences the shape or form of the plant. In otherwords,aplantcanexperienceastimulusat somepoint, likea rip in itsleafora fractureofabranch,andbeunaffectedby itat first,butwhenenvironmental conditions change, the plant may remember the pastexperienceandrespondbychangingitsgrowth.Dostál’s experiments on flax seedlings illustrate what he meant by

morphogeneticmemory.TofullyappreciateDostál’sexperimentsinthisarea, we have to understand a bit more about plant anatomy. Flaxseedlings emerge from the ground with two large leaves calledcotyledons.Inthecenterofthetwocotyledonsiswhat’scalledanapical

bud,whichgrowsupfromthecentralstemoftheplant.Asthisbudgrowsup,twolateralbudsemergebelowitoneachside,eachfacingtowardoneleaf. The lateral buds are dormant—they don’t grow—under normalconditions. However, if the apical bud is damaged or cut off, then thelateral ones will start to grow and extend, and each one forms a newbranchwhereeachlateralbudbecomestheapicalbud.Thisrepressionofthe lateral buds by the apical bud is called apical dominance, andreleasing this repression is the basis of plant pruning.When you see agardenerpruning thehedges in frontof ahouse,he is actually—ifhe’spruning correctly—removing the apical buds from each branch,encouragingmorelateralbuds,andnewbranches,togrow.

Thisillustrationshowsthreeflax(Linumusitatissimum)seedlings.Theimageontheleftshowsatwo-week-oldseedlingwithtwocotyledonsandanapicalbud(thesmallbumpbetweenthetwoleaves).Themiddlepictureshowsasimilarseedlingbutaftertheapicalbudhasbeendecapitatedandthetwolateralbudshavebeengrowingforaboutaweek.Thepictureontherightshowsaseedlingwiththeleftcotyledonremovedpriortodecapitatingtheapicalbud.

Flax(Linumusitatissimum)

Undernormalconditions, if theapicalbud isprunedoff,both lateralbuds grow evenly. But Dostál noticed that if he removed one of thecotyledons prior to decapitation of the apical bud, the only lateral budthat would growwas the one near the remaining leaf. This result mayseemlikeaclassiccaseofastimulusfollowedbyaresponse.Buthere’swherethingsgetreallyinteresting.WhenDostálrepeatedtheexperimentand illuminated the plant with red light, the lateral bud closest to theabsentcotyledongrew,whichrevealedthateachbudretainsthepotentialtogrow.Dostál’sresearchwaspickedupbyMichelThellierattheUniversityof

RoueninupperNormandy.Thellier,amemberoftheFrenchAcademyofSciences,noticedthatafterhedecapitatedtheapicalbudonhisplantofchoice,Bidenspilosa (alsoknownasSpanishneedle), both lateralbudsstartedtogrowmoreorlessevenly.Butifhesimplywoundedoneofthecotyledons, then only the lateral bud closest to the healthy leaf would

grow.Thellierdidn’thavetomanglethecotyledontogettheresponse;hewouldjustpricktheleaffourtimeswithaneedleatthesametimeasthedecapitation, and this minor wound was enough to get asymmetricalgrowthofthelateralbuds.Sowhere does plantmemory come in inwhat appears to be another

classic stimulus-response phenomenon? Well, sometimes during theseexperimentsThellierwouldextendtheamountoftimebetweenwoundingthe leafanddecapitating themainbud—evenup to twoweeks.And, loand behold, the lateral bud farthest from the pricked cotyledon wouldgrowout,andnotbothlateralbuds.ThellierknewtherehadtobesomewaythattheSpanishneedlestoredthis“traumatic”experienceandhadamechanismforrecallingitoncethecentralbudwasremoved,evenifthathappenedmanydayslater.

Spanishneedle(Bidenspilosa)

The following experiment really sealed the idea that the bud of theSpanish needle remembered which of its neighboring leaves had beendamaged. This time, Thellier stabbed one of the cotyledons as he hadbefore, but then he removedboth cotyledons severalminutes later. Hefoundthattheplantretainedthememoryofthestabbing:oncethecentralbud was removed, the lateral bud opposite the original woundedcotyledongrewmorethantheoneonthesideofthewoundedcotyledon.Thejuryisstilloutonhowthisinformationisstoredinthecentralbud,but one promising option is that the signal is somehow connected toauxin—thesamehormonethatwemetinchapterfive.

TheBigChillTrofimDenisovichLysenkowasnotorious for his impact on science intheSovietUnion.He rejected classicMendeliangenetics (basedon theprinciple that all characteristics are the result of inheritedgenes)whilechampioning the idea that theenvironment leads to thedevelopmentofadaptive characteristics (such as blindness in moles living in constantdarkness) that can be passed on to successive generations. Thisevolutionarytheory,originallyputforwardbythenotedFrenchnaturalistJean-BaptisteLamarckintheearlynineteenthcentury,fitperfectlywiththeprevailingideologyatthetimeofLysenko’sresearch,whichheldthatthe proletariat could be modified by the environment. The SovietestablishmentwassoenamoredofLysenkothatfrom1948to1964itwasillegal in the Soviet Union to express any dissent from his theories.Politics aside, Lysenko made a landmark discovery in 1928 thatinfluencesplantbiologytothisday.Sovietfarmersgrowwhatiscalledwinterwheat—wheatthatisplanted

in the fall, sprouts before freezing temperatures in the winter, andbecomes dormant until the soil warms in the spring, when it flowers.Winterwheatisn’tabletoflowerandsubsequentlyproducegraininthespringunless it experiencesaperiodofcoldweather in thewinter.Thelate1920sweredisastrousforSovietagriculturebecauseunusuallywarmwinters destroyed most of the winter wheat seedlings—seedlings thatfarmersreliedontoproducethegrainthatwouldfeedmillions.Lysenkoworked nonstop in an effort to savewhat little harvest they

wouldhaveandtofindwaysofensuringthatwarmwinterswouldn’tleadtofamineinthefuture.Hediscoveredthatifhetookwinterwheatseedsandputtheminafreezerbeforeplantingthem,hecouldinducetheseedstosproutandflowerwithouthavingactuallyenduredaprolongedwinter.Inthisway,heenabledfarmerstoplantwheatinthespringtime,andheultimatelysavedwheatyieldsinhiscountry.Lysenkocalledtheprocess“vernalization,”which has been embraced now as the general term foranycoldtreatment,beitnaturalorartificial.

Wheat(Triticumaestivum)

Other scientists also knew that some plants needed cold weather inorder to flower (oneof the first reports cameout of theOhioBoardofAgriculturein1857),butLysenkowasthefirsttoshowthattheprocesscould be artificially manipulated. Many plants rely on the coldtemperatures of winter to cultivate their harvest; many fruit trees willonly flower and set fruit following acold winter, and lettuce andarabidopsis seedsonlygerminate following a cold snap.The ecologicaladvantageofvernalization isclear: itensures that followingthecoldofwinter, a plant will sprout or flower in the spring or summer, and notduringothertimesoftheyearwhentheamountoflightandtemperaturecouldalsosupportplantgrowth.Forexample, thecherrytreesinWashington,D.C.,usuallyhavetheir

firstbloomoftheyeararoundApril1,whenthereareabouttwelvehoursofdaylight.Washington,D.C., also sees approximately twelvehoursof

sunlightinmid-September,butthesamecherrytreesneverbloominthefall; if they did, their fruitwould never fully develop as itwould soonfreezeintheapproachingwinter.Bloomingintheearlyspring,thecherryblossoms are able to give their fruit an entire five months to mature.Althoughtheday’slengthisexactlythesameinAprilandSeptember,thetrees are able to differentiate between the two. They know it’s Aprilbecausetheyremembertheprecedingwinter.Thebasisforawheatseedlingorcherrytreerememberingwinterhas

only been elucidated over the past decade or so, primarily throughresearch involving the tried-and-true arabidopsis. Arabidopsis growsnaturally inawidevarietyofnaturalhabitats, fromnorthernNorwaytotheCanaryIslands.ThedifferentpopulationsofArabidopsisthalianaarecalled ecotypes. Arabidopsis ecotypes that grow in northern climatesneedvernalizationtoflower,whilethosethatgrowinwarmerclimatesdojustfinewithoutit.Thisneedforvernalizationisencodedinthegenesofthenorthernecotypes. Ifyoucrossaplant thatneedswinter inorder toflowerwith a plant that doesn’t, the offspring still need a cold snap inordertoflower;genetically,theneedforcoldisadominanttrait(justasbrown eyes is a dominant trait relative to blue eyes in people). ThespecificgeneinvolvedisFLC,whichstandsforfloweringlocusC.Initsdominantversion,FLCinhibitsfloweringuntiltheplanthasundergoneavernalizationperiod.Oncetheplantgoesthroughaperiodofcoldweather,theFLCgeneis

no longer transcribed; thegene is turnedoff.But thatdoesn’tmean theplants will immediately start to flower; it only means that the plantscouldflowerifotherconditions,suchaslightandtemperature,cooperate.SotheplantmusthaveawayofrememberingthatitonceexperiencedacoldclimatetokeepFLCturnedoff,eventhoughtemperatureshavesincewarmedup.Manyresearchershavetriedtounderstandjusthowvernalizationturns

o f fFLC and how it stays this way once it’s turned off. Theseinvestigations have highlighted how epigenetics is intertwined with aplant’smemoryofwinter.Epigeneticsreferstochangesingeneactivitythatdon’trequirealterationsintheDNAcode,asmutationsdo,yetthese

changesingeneactivityarestillpasseddownfromparenttooffspring.25Inmanycases,epigeneticsworksthroughchangesinthestructureoftheDNA.Incells,DNAisorganizedinchromosomes,whicharemuchmorethan

simple strings of nucleotides. The double helix of DNA wraps aroundproteins called histones, forming what is known as chromatin. Thischromatincan twistevenmore, just likeanoverly twisted rubberband,compacting the DNA and proteins into highly condensed and packedstructures.Thesestructuresaredynamic:differentpartsofthechromatincanunravelorpackupagain.Activegenes(thosethataretranscribed)arefound inareasof thechromatin thatareunraveled,while inactivegeneslieinregionsthataremorecondensed.26The histone proteins are one of the key factors that determine how

tightly knit the chromatin gets, and this is very important forunderstandinghowFLCisactivated.Scientistshavediscoveredthatcoldtreatment triggers a change in the structure of the histones (a processcalledmethylation)aroundtheFLCgene,whichenablesthechromatintobetightlypacked.ThisturnsoffFLC,andtheplantisabletoflower.Thisepigeneticchange (the typeofhistonearound thegene) ispasseddownfromparent to daughter cells over successive generations, and theFLCgene remains inactive in all cells evenafter the coldweather subsides.Once theFLCgenehasbeenturnedoff,theplantscanwaituntiltherestof the environmental conditions are ideal for flowering. In perennialplants like oak trees and azaleas, which flower once per year, theFLCgene has to be reactivated once the plant has blossomed to inhibitpromiscuous flowering that might occur out of season until the nextwinter has passed. This involves the cells reprogramming their histonecode, which opens the chromatin around theFLC gene, reactivating it.Howthisoccurs,andhowit’sregulated,aremattersofcurrentresearch.Thisepigeneticmechanismofcellularmemoryisnotspecifictoplants

and is the basis of a great many biological processes and diseases.Epigenetics has caused a paradigm shift in biology because it goesagainst the classic genetic concept that the only changes that can be

passedonfromcelltocellarethoseintheDNAsequence.What’strulyamazing about epigenetics is that itfacilitates memory not only fromseason to season within a single organism but from generation togeneration.

InEveryGeneration…Memories are actively handed down from one generation to the nextthrough rituals, storytelling, and more. But transgenerational memoryinvolving epigenetics is completely different. This type of memoryusually involves information about an environmental or physical stressthat’spasseddownfromparentstooffspring.BarbaraHohn’slaboratoryin Basel, Switzerland, was the first to provide evidence for suchtransgenerationalmemory.Hohnandhercolleaguesknewthatconditionsthatcreatestressonaplant,likeultravioletlightorpathogenattack,leadtochangesintheplantgenomethatresultinnewcombinationsofDNA.These stress-induced changesmake sense ecologically because—like

anyotherorganism—aplantneeds tofindways tosurviveunderstress.One of the ways a plant does this is through new genetic variations.Hohn’s astounding study showed that not only do the stressed plantsmakenewcombinationsofDNAbut their offspring alsomake thenewcombinations, even though they themselves had never been directlyexposedtoanystress.Thestressintheparentscausedastableheritablechangethatwaspassedontoalltheiroffspring:theplantsbehavedasifthey’d been stressed. They remembered that their parents had beenthroughthisstressandreactedsimilarly.This use of theword “remembered”may seem unorthodox, but let’s

analyzethisinlightofthethreestepsofmemoryweencounteredatthebeginningof thischapter: theparents formed thememoryof the stress,retainedit,andpasseditontotheirchildren,andthechildrenrecalledtheinformationandreactedaccordingly,inthiscase,withincreasedgenomicchanges.

Theimplicationsofthisstudyarevast.Anenvironmentalstresscausesaheritable change that ispassedon to successivegenerations.This fitsexcellentlywiththetheoriesofJean-BaptisteLamarck,who,asyoumayrecall, claimed that evolutionwas based on the inheritance of acquiredcharacteristics. Hohn’s plants, following the UV or pathogen stress,acquiredthecharacteristicofincreasedgeneticvariationandpasseditontoalloftheirprogeny(andasinglearabidopsisplantproducesthousandsofseeds!).Thiscannotbeexplainedbymutations in theDNAsequenceofthestressedplants,becausethiscouldatmostbepassedontoonlyavery small percentage of the progeny. On the other hand, if the stressinducedanepigeneticchange, thiscouldhappen inall thecellsatonce,including pollen and egg cells, and be passed on to the entire nextgeneration,aswellasmanyfutureones.Whilescientistsspeculateastothe nature of the epigenetic change involved in these memories, itremainsundiscovered.IgorKovalchukcreateda follow-upstudy inwhichhe includedother

stresses on genetic variation in plants and their progeny including heatand salt. He showed that these different environmental insults increasethe frequency of genomic rearrangements not only in the parentalgeneration but also in the second generation. Kovalchuk’s results werefascinatingbecause theyrevealedevenmore than this.Notonlydid thesecondgenerationofplantsshowincreasedgeneticvariation,confirmingHohn’sresults,buttheywerealsomoretoleranttothevariousstresses.Inotherwords,stressedparentsgaverisetooffspringthatgrewbetterunderharsh conditions compared with regular plants. The various stressesalmostcertainly induceepigeneticchangesinchromatinstructurein theparents, which they pass on to their progeny.We believe this becauseKovalchuk’s group showed that if they treated the offspring with achemical that wiped out epigenetic information, these same plants losttheirabilitytothriveundertheenvironmentalstress.Hohn’sresultswerenot universally accepted, as is the case with many paradigm-shiftingstudiesinscience.Thegrowingconsensus,however,isthatherresults,aswell as others, have heralded a new era in genetics. The idea of stressleadingtomemoriesthatarepasseddownfromonegenerationtothenext

issupportedbyanincreasingnumberofstudies,notonlyinplants,butinanimals aswell. In all cases, this “memory” is based on some formofepigeneticheredity.

IntelligentMemory?Plantsclearlyhavetheabilitytostoreandrecallbiologicalinformation.Intuitively, we know that this is quite different from the detailed andemotion-filledmemories we recall every day. But at a basic level, thebehaviorsofdifferentplantsdescribedinthischapterareremedialtypesof memory. The tendril’s coiling, the Venus flytrap’s closing, and thearabidopsis’srememberingenvironmentalstressallincludetheprocessesof forming thememory of the event, retaining thememory for distincttimeperiods,andrecallingthememoryatalaterpointinordertogetaspecificdevelopmentalresponse.Manyofthemechanismsinvolvedinplantmemoryarealsoinvolved

inhumanmemory, includingepigeneticsandelectrochemicalgradients.These gradients are the bread and butter of neural connections in ourbrains, the seat of memory as most ofus understand it. Over the pastseveralyears,plantscientistshavediscoveredthatnotonlydoplantcellscommunicatewithelectricalcurrents(aswesawinseveralchapters)butplants also contain proteins known in humans and other animals asneuroreceptors.Aperfect example is theglutamate receptor.Glutamatereceptors in the brain are very important for neural communication,memory formation, and learning, and a number of neuroactive drugstargetglutamatereceptors.Itwasagreatsurprise, then,forscientistsatNewYorkUniversitytodiscoverthatplantscontainglutamatereceptorsand that arabidopsis plants are sensitive to neuroactive drugs that alterglutamatereceptoractivity.At thispointwestilldon’t fullyunderstandwhatglutamatereceptorsdoinplants,butveryrecentworkcarriedoutbyJoséFeijóandhisgroupinPortugalshowsthatthesereceptorsinplantsfunction in cell-to-cell signaling in a way that’s very similar to how

humanneuronscommunicatewitheachother.Thisleavesustomarvelatthe evolutionary role of “brain receptors” in plants. Perhaps thesimilaritiesbetweenhumanbrainfunctionandplantphysiologymaybegreaterthanwe’veassumed.Plant memories, like human immune memory, are not semantic or

episodic memories, as Tulving defined them, but rather proceduralmemories,memoriesofhowtodothings;thesememoriesdependontheability tosenseexternalstimulation.Tulvingfurtherproposed thateachof the three levels ofmemory is associatedwith an increasing level ofconsciousness. Procedural memory is associated with anoeticconsciousness,semanticmemoryisassociatedwithnoeticconsciousness,andepisodicmemoryisassociatedwithautonoeticconsciousness.Plantsclearlydonotfitthedefinitionofconsciousnessassociatedwithsemanticor episodic memories. But as stated in a recent opinion article, “Thelowest level of consciousness characteristic for procedural memory—anoeticconsciousness—referstotheabilityoforganismstosenseandtoreact to external and internal stimulation, which all plants and simpleanimalsarecapableof.”Thisleadsustothemostintriguingquestionofall: If plants exhibit different types of memory and have a form ofconsciousness,shouldtheybeconsideredintelligent?

Epilogue:TheAwarePlant“Intelligence”isaloadedterm.EveryonefromAlfredBinet,theinventorof the much-debated IQ test, to the renowned psychologist HowardGardner has had a different understanding of just what it means toclassify someone as “intelligent.” While some researchers considerintelligenceauniquepropensityofhumanbeings,wehaveseen reportsthat animals—fromorangutans tooctopuses—possessqualities that fallunder some definitions of “intelligence.” Applying definitions ofintelligence to plants, however, is much more contentious, though thequestion of intelligent plants is hardly a new one. Dr.William LauderLindsay,who doubled as a physicianand a botanist,wrote in 1876: “Itappears to me thatcertain attributes ofmind, as it occurs inMan, arecommontoPlants.”Anthony Trewavas, an esteemed plant physiologist based at the

University of Edinburgh in Scotland and one of the early modernpurveyorsofplantintelligence,pointsoutthatwhilehumansareclearlymore intelligent than other animals, it is unlikely that intelligence as abiologicalpropertyoriginatedonlyinHomosapiens.Inthisveinheseesintelligence as a biological characteristic no different from, say, bodyshapeandrespiration—allofwhichevolvedthroughthenaturalselectionofcharacteristicspresentinearlierorganisms.WesawthisquiteclearlyinChapterFourinthe“deaf”genessharedbyplantsandhumans.Thesegeneswerepresentinacommonancientancestorofplantsandanimals,and Trewavas has proposed that rudimentary intelligence was presentthereaswell.Controversy arose among plant biologistswhen a group of scientists

whostudyvariousaspectsofplantfunctiondefinedanewfield in2005that they called “plant neurobiology,” which aims to study theinformation networks present in plants. These scientists saw manysimilarities between plant anatomy and physiology and the neuralnetworksinanimals.Someofthesesimilaritiesareobvious,suchastheelectrical signaling we encountered in the Venus flytrap andMimosa

plants, and somemore divisive, such as the architecture of plant rootsbeing similar to the architecture of neural networks found in variousanimals.This latter hypothesis was originally put forward in the nineteenth

century byCharlesDarwin and has been picked up again over the pastfew years, particularly by Stefano Mancuso from the University ofFlorenceandFrantiöekBaluökafromtheUniversityofBonn,twoofthepioneers in the field of plant neurobiology.Many other biologistswhostudyplants, includinganumberofveryprominentscientists,criticizedtheideasbehindplantneurobiology,claimingthatitstheoreticalbasisisflawedandthatithasnotaddedtoourunderstandingofplantphysiologyorplantcellbiology.Theystronglyfeltthattheplantneurobiologistshadgonetoofarindrawingparallelsbetweenplantandanimalbiology.Manyproponents of plant neurobiologywouldbe the first to explain

that the term itself is provocative and therefore useful for encouragingmoredebateanddiscussionabout theparallelsbetween thewaysplantsandanimalsprocessinformation.Metaphors,aspointedoutbyTrewavasandothers,helpusmakeconnectionsthatwemightnotnormallymake.If by using the term “plant neurobiology” we challenge people toreevaluate their understanding of biology in general, and plant biologyspecifically,thenthetermisvalid.Butwemustbeclear:nomatterwhatsimilaritieswemayfindatthegeneticlevelbetweenplantsandanimals(and, as we have seen, they are significant), they are two very uniqueevolutionaryadaptationsformulticellularlife,eachofwhichdependsonuniquekingdom-specificsetsofcells, tissues,andorgans.Forexample,vertebrate animals developed a bony skeleton to support weight, whileplantsdevelopedawoody trunk.Both fill similar functions,yet each isbiologicallyunique.27Whilewe could subjectively define “vegetal intelligence” as another

facet of multiple intelligences, such a definition does not further ourunderstanding of either intelligence or plant biology. The question, Iposit,shouldnotbewhetherornotplantsareintelligent—itwillbeagesbeforeweallagreeonwhatthattermmeans;thequestionshouldbe,“Are

plantsaware?”and,infact,theyare.Plantsareacutelyawareoftheworldaround them. They are aware of their visual environment; theydifferentiate between red, blue, far-red, and UV lights and respondaccordingly.Theyareawareofaromassurroundingthemandrespondtominutequantitiesofvolatilecompoundswafting in theair.Plantsknowwhentheyarebeingtouchedandcandistinguishdifferenttouches.Theyareawareofgravity: theycanchange theirshapes toensure thatshootsgrowupand rootsgrowdown.Andplants are awareof their past: theyrememberpast infectionsandtheconditionsthey’veweatheredandthenmodifytheircurrentphysiologybasedonthesememories.If a plant is aware, what does this mean for us regarding our own

interactionswiththegreenworld?Ononehand,an“awareplant”isnotawareofusasindividuals.Wearesimplyoneofmanyexternalpressuresthatincreaseordecreaseaplant’schancesforsurvivalandreproductivesuccess.ToborrowtermsfromFreudianpsychology:theplantpsycheisdevoid of an ego and a superego, though it may contain an id, theunconscious part of the psyche that gets sensory input and worksaccordingtoinstinct.Aplantisawareofitsenvironment,andpeoplearepartofthisenvironment.Butit’snotawareofthemyriadgardenersandplant biologists who develop what they consider to be personalrelationships with their plants. While these relationships may bemeaningful to the caretaker, they are not dissimilar to the relationshipbetween a child and her imaginary friend; the flow of meaning isunidirectional. I’ve heard world-famous scientists and undergraduateresearch students alike use anthropomorphic language with abandon astheydescribe their plants as “not looking toohappy”whenmildewhastakenovertheirleavesoras“satisfied”afterthey’vebeenwatered.These terms represent our own subjective assessment of a plant’s

decidedlyunemotionalphysiologicalstatus.Foralltherichsensoryinputthat plants and people perceive, only humans render this input as anemotional landscape. We project on plants our emotional load andassume that a flower in full bloom is happier than a wilting one. If“happy”canbedefinedasan“optimalphysiologicalstate,”thenperhapsthe term fits. But I think that for all of us, “happy” depends onmuch

more than being in perfect physical health. In fact, we’ve all knownpeopleafflictedwithvariousailmentswhoconsideredthemselveshappy,and otherwisehealthyindividualswhoaregenerallymiserable inmood.Happiness,wecanagree,isastateofmind.A plant’s awareness also does not imply that a plant can suffer. A

seeing, smelling, feeling plant can no more suffer pain than can acomputerwith a faulty hard drive. Indeed, “pain” and “suffering,” like“happy,”areverysubjectivetermsandareoutofplacewhendescribingplants.TheInternationalAssociationfortheStudyofPaindefinespainas“anunpleasant sensoryandemotionalexperienceassociatedwithactualor potential tissue damage, or described in terms of such damage.”Perhaps “pain” for a plant could be defined in terms of “actual orpotentialtissuedamage,”aswhenaplantsensesphysicaldistressthatcanlead to cell damage or death. A plant senses when a leaf has beenpuncturedbyaninsect’sjaws;aplantknowswhenit’sbeenburnedinaforestfire.Plantsknowwhentheylackwaterduringadrought.Butplantsdonotsuffer.Theydon’thave,toourcurrentknowledge,thecapacityforan“unpleasant…emotional experience.” Indeed, even inhumans,painandsufferingareconsideredseparatephenomena,interpretedbydifferentparts of the brain. Brain-imaging studies have identified pain centersdeepwithinthehumanbrainthatradiateoutfromthebrainstem,whilethecapacity forsuffering, scientistsbelieve, is located in theprefrontalcortex. So if suffering from pain necessitates highly complex neuralstructuresandconnectionsofthefrontalcortex,whicharepresentonlyinhighervertebrates,thenplantsobviouslydon’tsuffer:theyhavenobrain.Theconstructofabrainlessplantisimportantformetoaccentuate.If

wekeepinmindthataplantdoesn’thaveabrain,itfollowsthenthatanyanthropomorphicdescription isat itsbaseseverely limited. Itallowsusto continue to anthropomorphize plant behavior for the sake of literaryclaritywhilerememberingthatallsuchdescriptionsmustbetemperedbythe idea of a brainless plant. While we use the same terms—“see,”“smell,” “feel”—we also know that the overall sensual experience isqualitativelydifferentforplantsandpeople.Without this caveat, anthropomorphism of plant behavior left

unchecked can lead to unfortunate, if not humorous, consequences. Forexample,in2008theSwissgovernmentestablishedanethicscommitteeto protect the “dignity” of plants.28 A brainless plant likely does notworryaboutitsdignity.Andyetifaplantisaware,itmeanseverythingforusregardingourowninteractionswiththevegetalworld.MaybetheSwissattemptatbestowingdignityonplantsmirrorsourownattemptatdefiningour relationshipwith theplantworld.As individuals,weoftenseekourplaceinsocietybycomparingourselveswithotherpeople.Asaspecies,we seekourplace innaturebycomparingourselveswithotheranimals.It’seasyforustoseeourselvesintheeyesofachimpanzee;wecan identifywith a baby gorilla clinging to hermother. JohnGrogan’sdog,Marley, likeLassieandRinTinTinbeforehim,evokesverydeepfeelingsofempathy,andevenpeoplewhoarenotnecessarilydogloverscan see human characteristics in our canine friends. I’ve known birdkeeperswhoclaimtheirparrotsunderstandthem,andfishloverswhoseehuman behavior in theirmarine life. These examples clearly show that“human”maybeonlyaflavor,albeitaninterestingone,ofintelligence.Soifhumansandplantsaresimilarinthatbothareawareofcomplex

light environments, intricate aromas, different physical stimulations, ifhumansandplantsbothhavepreferences,andifbothremember,thendoweseeourselveswhenlookingattheplant?Whatwemust see is thatonabroad levelwe sharebiology not only

withchimpsanddogsbutalsowithbegoniasandsequoias.Weshouldseea very long-lost cousin when we gaze at our rosebush in full bloom,knowing that we can discern complex environments just as it can,knowingthatwesharecommongenes.Whenwelookativyclingingtoawall, we are looking at what, save for some ancient stochastic event,couldhavebeenourfate.Weareseeinganotherpossibleoutcomeofourownevolution,onethatbranchedoffsometwobillionyearsago.A shared genetic past does not negate eons of separate evolution.

Whileplantsandhumansmaintainparallelabilitiestosenseandbeawareof the physicalworld, the independent paths of evolution have led to auniquelyhumancapacity,beyondintelligence,thatplantsdon’thave:the

abilitytocare.So the next timeyou find yourself on a stroll through a park, take a

second toaskyourself:Whatdoes thedandelion in the lawnsee?Whatdoes thegrasssmell?Touchthe leavesofanoak,knowingthat the treewill remember itwas touched.But itwon’t rememberyou.You,on theotherhand,canrememberthisparticulartreeandcarrythememoryofitwithyouforever.

NotesPROLOGUE3 Inmy research : DanielA. Chamovitz et al., “The COP9Complex, aNovel Multisubunit Nuclear Regulator Involved in Light Control of aPlantDevelopmentalSwitch,”Cell86,no.1(1996):115–21.3Muchtomysurprise:DanielA.ChamovitzandXing-WangDeng,“TheNovel Components of the Arabidopsis Light Signaling Pathway MayDefine a Group of General Developmental Regulators Shared by BothAnimalandPlantKingdoms,”Cell82,no.3(1995):353–54.3Manyyears later:AlysonKnowles et al., “TheCOP9Signalosome IsRequired for Light-Dependent Timeless Degradation andDrosophilaClock Resetting,”Journal of Neuroscience 29, no. 4 (2009): 1152–62;Ning Wei, Giovanna Serino, and Xing-Wang Deng, “The COP9Signalosome:MoreThanaProtease,”TrendsinBiochemicalSciences33,no.12(2008):592–600.5As the renowned plant physiologist: Peter Tompkins andChristopherBird,TheSecretLifeofPlants(NewYork:Harper&Row,1973);ArthurW.Galston, “TheUnscientificMethod,”NaturalHistory 83 (1974):18,21,24.ONE.WHATAPLANTSEES1 0“the physical sense by which light”: “Sight,”Merriam-Webster,www.merriam-webster.com/dictionary/sight.12“Thereareextremelyfew” :CharlesDarwinandFrancisDarwin,ThePowerofMovementinPlants(NewYork:D.Appleton,1881),p.1.13“couldnotseetheseedlings”:Ibid.,p.450.16In1918:A brief history of light research atUSDA can be found atwww.ars.usda.gov/is/timeline/light.htm.17This phenomenon, called photoperiodism:WightmanW.Garner andHarryA.Allard,“Photoperiodism,theResponseofthePlanttoRelativeLengthofDayandNight,”Science55,no.1431(1922):582–83.18theplants,andit:MarionW.Parkeretal.,“ActionSpectrumforthePhotoperiodic Control of Floral Initiation in Biloxi Soybean,”Science

102,no.2641(1945):152–55.1 8Then, in the early 1950s: Harry Alfred Borthwick, Sterling B.Hendricks, and Marion W. Parker, “The Reaction Controlling FloralInitiation,”Proceedings of the National Academy of Sciences of theUnited States of America 38, no. 11 (1952): 929–34; Harry AlfredBorthwick et al., “A Reversible Photoreaction Controlling SeedGermination,”Proceedings of theNational Academy of Sciences of theUnitedStatesofAmerica38,no.8(1952):662–66.19WarrenL.Butlerandcolleagues :WarrenL.Butleretal.,“Detection,Assay, and Preliminary Purification of the Pigment ControllingPhotoresponsive Development of Plants,”Proceedings of the NationalAcademyofSciencesof theUnitedStatesofAmerica45,no.12(1959):1703–8.20Theapproach spearheaded :MaartenKoornneef, E.Rolff, andCarelJohannes Pieter Spruit, “Genetic Control of Light-Inhibited HypocotylElongation inArabidopsisthaliana (L)Heynh,”Zeitschrift fürPflanzen-physiologie100,no.2(1980):147–60.2 2To make a long : Joanne Chory, “Light Signal Transduction: AnInfiniteSpectrumofPossibilities,”PlantJournal61,no.6(2010):982–91.24Theseeyespotshavebeen:GeorgKreimer,“TheGreenAlgalEyespotApparatus:A Primordial Visual System and More?,”Current Genetics55,no.1(2009):19–43.25Thename“cryptochrome”isactually: JonathanGressel,“Blue-LightPho-toreception,”Photochemistry and Photobiology 30, no. 6 (1979):749–54.2 5cryptochrome is no longer: Margaret Ahmad and Anthony R.Cashmore, “HY4 Gene ofA. thaliana Encodes a Protein withCharacteristics of a Blue-Light Photoreceptor,”Nature 366, no. 6451(1993):162–66.2 6The plant cryptochrome: Anthony R. Cashmore, “Cryptochromes:Enabling Plants andAnimals to Determine Circadian Time,”Cell 114,no.5(2003):537–43.TWO.WHATAPLANTSMELLS

27“toperceiveodororscent”:AvailableatMerriam-Webster.com.3 0Frank E. Denny, a scientist: Frank E. Denny, “Hastening theColorationofLemons,”AgriculturalResearch27(1924):757–69.3 0Gane analyzed the air: Richard Gane, “Production of Ethylene bySomeRipeningFruits,”Nature134(1934):1008;andWilliamCrocker,A.E.Hitchcock, andP.W.Zimmerman, “Similarities in theEffects ofEthylene and the Plant Auxins,”Contributions from Boyce ThompsonInstitute7(1935):231–48.33Oneofherprojectscenteredon :JustinB.Runyon,MarkC.Mescher,and Consuelo M. De Moraes, “Volatile Chemical Cues Guide HostLocationandHostSelectionbyParasiticPlants,”Science313,no.5795(2006):1964–67.35asRhoadesdiscovered:DavidF.Rhoades, “Responses ofAlder andWillow to Attack by Tent Caterpillars and Webworms: Evidence forPheromonal Sensitivity of Willows,” inPlant Resistance to Insects,editedbyPaulA.Hedin(Washington,D.C.:AmericanChemicalSociety,1983),pp.55–66.36DartmouthresearchersIanBaldwinandJackSchultz :IanT.BaldwinandJackC.Schultz,“RapidChangesinTreeLeafChemistryInducedbyDamage:EvidenceforCommunicationBetweenPlants,”Science221,no.4607(1983):277–79.38Theseearlyreportsofplantsignaling:SimonV.FowlerandJohnH.Lawton, “Rapidly Induced Defenses and Talking Trees: The Devil’sAdvocatePosition,”AmericanNaturalist126,no.2(1985):181–95.38thepopularpressembracedtheidea:“ScientistsTurnNewLeaf,FindTrees Can Talk,”Los Angeles Times, June 6, 1983, A9; “Shhh. LittlePlants Have Big Ears,”MiamiHerald, June 11, 1983, 1B; “Trees Talk,Respond to Each Other, Scientists Believe,”Sarasota Herald-Tribune,June6,1983;and“WhenTreesTalk,”NewYorkTimes,June7,1983.39MartinHeilandhisteam:MartinHeilandJuanCarlosSilvaBueno,“Within-PlantSignalingbyVolatilesLeadstoInductionandPrimingofan Indirect Plant Defense in Nature,”Proceedings of the NationalAcademyofSciencesoftheUnitedStatesofAmerica104,no.13(2007):5467–72.

43HeilcollaboratedwithcolleaguesfromSouthKorea:Hwe-SuYietal.,“Airborne Induction andPrimingofPlantDefensesAgainst aBacterialPathogen,”PlantPhysiology151,no.4(2009):2152–61.4 5supported work done a decade earlier: Vladimir Shulaev, PaulSilverman,andIlyaRaskin,“AirborneSignallingbyMethylSalicylateinPlantPathogenResistance,”Nature385,no.6618(1997):718–214 5Plants can convert soluble salicylic acid:Mirjana Seskar, VladimirShulaev, and IlyaRaskin, “EndogenousMethyl Salicylate in Pathogen-InoculatedTobaccoPlants,”PlantPhysiology116,no.1(1998):387–92.4 7the author Michael Pollan infers: Michael Pollan,The Botany ofDesire: A Plant’s-Eye View of theWorld (NewYork: Random House,2001).47Arecent(andprovocative)study :ShaniGelsteinetal.,“HumanTearsContainaChemosignal,”Science331,no.6014(2011):226–30.THREE.WHATAPLANTFEELS55“oneof themostwonderful[plants]”: CharlesDarwin,InsectivorousPlants(London:JohnMurray,1875),p.286.55“Duringthesummerof1860”:Ibid.,p.1.56“Dropsofwater”:Ibid.,p.291.5 6John Burdon-Sanderson made the crucial: John Burdon-Sanderson,“On theElectromotivePropertiesof theLeafofDionaea in theExcitedand Unexcited States,”Philosophical Transactions of theRoyal Society173(1882):1–55.57electric stimulation itself:AlexanderG.Volkov, TejumadeAdesina,andEmilJovanov,“ClosingofVenusFlytrapbyElectricalStimulationofMotorCells,”PlantSignaling&Behavior2,no.3(2007):139–45.57Volkov’sworkandearlierresearch :Ibid.;DieterHodickandAndreasSievers,“TheActionPotentialofDionaeamuscipula Ellis,”Planta174,no.1(1988):8–18.58Thiswasnoticedby:VirginiaA.Shepherd,“FromSemi-conductorstotheRhythmsofSensitivePlants:TheResearch of J.C.Bose,”CellularandMolecularBiology51,no.7(2005):607–19.5 9Unfortunately, Burdon-Sanderson was : Subrata Dasgupta, “JagadisBose,AugustusWaller, and the Discovery of ‘Vegetable Electricity,’”

NotesandRecordsoftheRoyalSocietyofLondon52,no.2(1998):307–22.6 1“We were confronted with” : Frank B. Salisbury,The FloweringProcess, International Series of Monographs on Pure and AppliedBiology,Division:PlantPhysiology(NewYork:PergamonPress,1963).6 2He coined the cumbersome: Mark J. Jaffe, “Thigmomorphogenesis:The Response of Plant Growth and Development to MechanicalStimulation—withSpecialReferencetoBryoniadioica,”Planta114,no.2(1973):143–57.6 4Braam understood that: Janet Braam and RonaldW. Davis, “Rain-Induced, Wind-Induced, and Touch-Induced Expression of Calmodulinand Calmodulin-Related Genes in Arabidopsis,”Cell 60, no. 3 (1990):357–64.66Thankstothecontinuingwork:DennisLee,DianaH.Polisensky,andJanet Braam, “Genome-Wide Identification of Touch- and Darkness-Regulated Arabidopsis Genes: A Focus on Calmodulin-Like andXTHGenes,”NewPhytologist165,no.2(2005):429–44.67Anamazingexampleof:DavidC.Wildonetal.,“ElectricalSignalingand Systemic Proteinase-Inhibitor Induction in the Wounded Plant,”Nature360,no.6399(1992):62–65.FOUR.WHATAPLANTHEARS7 2Many of us have heard: For example, “Plants and Music,”www.miniscience.com/projects/plantmusic/index.html.72Typically, though,much :RossE.Koning,ScienceProjectsonMusica n dSound, Plant Physiology Information website,http://plantphys.info/music.shtml;www.youth.net/nsrc/sci/sci048.html#anchor992130;http://jrscience.wcp.muohio.edu/nsfall05/LabpacketArticles/Whichtypeofmusicbeststimu.htmlhttp://spider2.allegheny.edu/student/S/sesekj/FS%20Bio%20201%20Coenen%20Draft%20Results-Discussion.doc.72Acommondefinitionof“hearing”:HearingImpairment Information,www.disabled-world.com/disability/types/hearing.74“fool’s experiment” : Francis Darwin, ed.,CharlesDarwin:His LifeTold in an Autobiographical Chapter and in a Selected Series of His

PublishedLetters(London:JohnMurray,1892).7 4An example of one: Katherine Creath and Gary E. Schwartz,“MeasuringEffects ofMusic,Noise, andHealingEnergyUsing aSeedGermination Bioassay,”Journal of Alternative and ComplementaryMedicine10,no.1(2004):113–22.7 4Schwartz founded the VERITAS: The Veritas Research Program,http://veritas.arizona.edu.7 4Obviously, studying consciousness after: Ray Hyman, “How Not toTest Mediums: Critiquing the Afterlife Experiments,”www.csicop.org/si/show/how_not_to_test_mediums_critiquing_the_afterlife_experiments//Robert Todd Carroll, “Gary Schwartz’s Subjective Evaluation ofM e d i u m s :Veritas or Wishful Thinking?,”http://skepdic.com/essays/gsandsv.html.74“biologiceffectsofmusic”:CreathandSchwartz,“MeasuringEffectsofMusic,Noise,andHealingEnergy.”7 5who used ultrasonic waves: Pearl Weinberger and Mary Measures,“TheEffectofTwoAudibleSoundFrequenciesontheGerminationandGrowthofaSpringandWinterWheat,”CanadianJournalofBotany46,no.9(1968):1151–58.PearlWeinbergerandMaryMeasures,“Effectsofthe Intensity of Audible Sound on the Growth and Development ofRideau Winter Wheat,”Canadian Journal of Botany 57, no. 9 (1979):1151036–39.7 5“doctor’s wife, housekeeper” : Dorothy L. Retallack,The Sound ofMusicandPlants(SantaMonica,Calif.:DeVorss,1973).75sheenrolledasafreshman :AnthonyRipley,“RockorBachanIssuetoPlants,SingerSays,”NewYorkTimes,February21,1977.76Retallackexplainedthatshe:FranklinLoehr,ThePowerofPrayeronPlants(GardenCity,N.Y.:Doubleday,1959).77Retallack’sstudieswere fraught :LindaChalker-Scott,“TheMythofAbsolute Science: ‘If It’s Published, It Must Be True,’”www.puyallup.wsu.edu/~linda%20chalker-scott/horticultural%20myths_files/Myths/Bad%20science.pdf.7 8contradicted an important study: Richard M. Klein and Pamela C.Edsall, “On the Reported Effects of Sound on the Growth of Plants,”

Bioscience15,no.2(1965):125–26.79“Therewasnoleafabscission”:Ibid.80It isalso featured:PeterTompkins andChristopherBird,TheSecretLifeofPlants(NewYork:Harper&Row,1973).8 0“The trouble with The Secret Life”: Arthur W. Galston, “TheUnscientificMethod,”NaturalHistory83,no.3(1974):18,21,24.80InJanetBraam’soriginal :JanetBraamandRonaldW.Davis,“Rain-Induced, Wind-Induced, and Touch-Induced Expression of Calmodulinand Calmodulin-Related Genes in Arabidopsis,”Cell 60, no. 3 (1990):357–64.8 1Similarly, in Physiology: Peter Scott,Physiology and Behaviour ofPlants(Hoboken,N.J.:JohnWiley,2008).8 3More than three hundred researchers : The Arabidopsis GenomeInitiative, “Analysis of the Genome Sequence of the Flowering PlantArabidopsisthaliana,”Nature408,no.6814(2000):796–815.84Mostrelevanttoour:AlanM.Jonesetal.,“TheImpactofArabidopsisonHumanHealth: DiversifyingOur Portfolio,”Cell 133, no. 6 (2008):939–43.84Thehumangenome:DanielA.ChamovitzandXing-WangDeng,“TheNovel Components of the Arabidopsis Light Signaling Pathway MayDefine a Group of General Developmental Regulators Shared by BothAnimalandPlantKingdoms,”Cell82,no.3(1995):353–54.8 5mutations in the arabidopsis breast cancer: Kiyomi Abe et al.,“Inefficient Double-Strand DNA Break Repair Is Associated withIncreased Fascination inArabidopsis BRCA2 Mutants,”Journal ofExperimentalBotany70,no.9(2009):2751–61.86Whenamutationoccurs:ValeraV.Peremyslovetal.,“TwoClassXIMyosinsFunction inOrganelleTraffickingandRootHairDevelopmentinArabidopsis,”PlantPhysiology146,no.3(2008):1109–16.8 6Professor Stefano Mancuso: “Phonobiologic Wines,”www.brightgreencities.com/vl/en/bright-green-book/italia/vinho-fonobiologico.8 7In a similar vein, Roman: Roman Zweifel and Fabienne Zeugin,“UltrasonicAcousticEmissions inDrought-StressedTrees—MoreThan

SignalsfromCavitation?,”NewPhytologist179,no.4(2008):1070–79.88Thegreat evolutionarybiologist:TheodosiusDobzhansky, “Biology,MolecularandOrganismic,”AmericanZoologist4,no.4(1964):443–52.FIVE.HOWAPLANTKNOWSWHEREITIS9 4Henri-Louis Duhamel du Monceau: Henri-Louis Duhamel duMonceau,La physique des arbres où il est traité de l’anatomie desplantesetdel’économievégétale:Pourservird’introductionau“Traitécomplet des bois& des forests,” avec une dissertation sur l’utilité desméthodes debotanique & une explication des termes propres à cettescience& qui sont en usage pour l’exploitation des bois & des forêts(Paris:H.L.Guérin&L.F.Delatour,1758).95“thehypothesis”: ThomasAndrewKnight, “On theDirection of theRadicle and Germen During the Vegetation of Seeds,”PhilosophicalTransactionsoftheRoyalSocietyofLondon96(1806):99–108.97Aswithsomanyquestions:CharlesDarwin andFrancisDarwin,ThePowerofMovementinPlants(NewYork:D.Appleton,1881).99More thanacentury:RyujiTsugeki andNinaV.Fedoroff, “GeneticAblationofRootCapCellsinArabidopsis,”ProceedingsoftheNationalAcademyofSciencesof theUnitedStatesofAmerica96,no.22(1999):12941–46.9 9many scientists have isolated: Miyo Terao Morita, “DirectionalGravity Sensing in Gravitropism,”Annual Review of Plant Biology 61(2010):705–20.100For example, an arabidopsis: Joanna W. Wysocka-Diller et al.,“Molecular Analysis of SCARECROW Function Reveals a RadialPatterningMechanismCommon to Root and Shoot,”Development 127,no.3(2000):595–603.100Recentgeneticstudiesdemonstrate:DaisukeKitazawaetal.,“ShootCircumnutation andWindingMovements Require Gravisensing Cells,”ProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica102,no.51(2005):18742–47.101 scarecrowgene is necessary: Wysocka-Diller et al., “MolecularAnalysisofSCARECROWFunction.”1 0 3Using a high-gradient: Sean E. Weise et al., “Curvature in

ArabidopsisInflorescenceStemsIsLimitedtotheRegionofAmyloplastDisplacement,”PlantandCellPhysiology41,no.6(2000):702–9.103Under theseweightless conditions: JohnZ.Kiss,W. JiraKatembe,andRichardE.Edelmann,“GravitropismandDevelopmentofWild-Typeand Starch-Deficient Mutants of Arabidopsis During Spaceflight,”PhysiologiaPlantarum102,no.4(1998):493–502.104Peter Boysen-Jensen expanded on: Peter Boysen-Jensen, “Über dieLeitungdesphototropischenReizesinderAvenakoleoptile,”BerichtedesDeutschenBotanischenGesellschaft31(1913):559–66.1 0 7As the Polish scientist Maria Stolarz: Maria Stolarz et al.,“Disturbances of Stem Circumnutations Evoked by Wound-InducedVariation Potentials inHelianthus annuus L.,”Cellular & MolecularBiologyLetters8,no.1(2003):31–40.108Thishypothesisremainedunchallenged:AndersJohnssonandDonaldIsraelsson, “Application of a Theory for Circumnutations to GeotropicMovements,”PhysiologiaPlantarum21,no.2(1968):282–91.109Brown had to wait: Allan H. Brown et al., “Circumnutations ofSunflower Hypocotyls in Satellite Orbit,”Plant Physiology 94 (1990):233–38.109Sunflowerseedlingsexhibitrobust:JohnZ.Kiss,“Up,Down,andAllAround: How Plants Sense and Respond to Environmental Stimuli,”ProceedingsoftheNationalAcademyofSciencesoftheUnitedStatesofAmerica103,no.4(2006):829–30.11 0A few years ago: Kitazawa et al., “Shoot Circumnutation andWindingMovementsRequireGravisensingCells.”111AndersJohnssoncouldput:AndersJohnsson,BjarteGeesSolheim,and Tor-Henning Iversen, “Gravity Amplifies and MicrogravityDecreasesCircumnutations inArabidopsisthalianaStems:Results fromaSpaceExperiment,”NewPhytologist182,no.3(2009):621–29.111Theoverallmechanismof:Morita, “DirectionalGravity Sensing inGravitropism.”SIX.WHATAPLANTREMEMBERS11 4Mark Jaffe, the same scientist: Mark J. Jaffe, “ExperimentalSeparation of Sensory and Motor Functions in Pea Tendrils,”Science

195,no.4274(1977):191–92.115Tulving proposed that humanmemory : EndelTulving, “HowManyMemorySystemsAreThere?,”AmericanPsychologist40,no.4 (1985):385–98.While Tulving’s models of memory are well recognized, theyshould not be accepted as monolithic, and within the field of memorynumerous models and theories exist, not all of which are mutuallyexclusive.1 1 5But plants are capable of sensing: Fatima Cvrckova, HelenaLipavska, and Viktor Zarsky, “Plant Intelligence: Why, Why Not, orWhere?,”PlantSignaling&Behavior4,no.5(2009):394–99.116What’s fascinating is that the latest : ToddC. Sacktor, “HowDoesPKMz Maintain Long-Term Memory?,”Nature Reviews Neuroscience12,no.1(2011):9–15.117Scientists have been puzzled: John S. Burdon-Sanderson, “On theElectromotive Properties of the Leaf ofDionaea in the Excited andUnexcited States,”Philosophical Transactions of the Royal Society ofLondon173(1882):1–55.117Acentury later,DieterHodickandAndreasSievers :DieterHodickandAndreasSievers,“TheActionPotentialofDionaeamuscipulaEllis,”Planta174,no.1(1988):8–18.1 1 8Alexander Volkov and his colleagues : Alexander G. Volkov,Tejumade Adesina, and Emil Jovanov, “Closing of Venus Flytrap byElectricalStimulationofMotorCells,”PlantSignaling&Behavior2,no.3(2007):139–45.119WhenVolkovpretreatedhisplants:Ibid.11 9In the mid-twentieth century: Rudolf Dostál,On Integration inPlants,translatedbyJanaMoravkovaKiely(Cambridge,Mass.:HarvardUniversityPress,1967).1 2 2But Dostál noticed that if he: Described in Anthony Trewavas,“AspectsofPlantIntelligence,”AnnalsofBotany92,no.1(2003):1–20.122Thellier, a member of the French : Michel Thellier et al., “Long-DistanceTransport,Storage,andRecallofMorphogeneticInformationinPlants:TheExistenceof aSort ofPrimitivePlant ‘Memory,’”ComptesRendusdel’AcadémiedesSciences,SérieIII323,no.1(2000):81–91.

124TrofimDenisovichLysenkowasnotorious :E.W.CaspariandR.E.Marshak,“TheRiseandFallofLysenko,”Science149,no.3681(1965):275–78.125Other scientists also knew: John H. Klippart,Ohio State Board ofAgricultureAnnualReport12(1857):562–816.1 2 7These investigations have highlighted: Ruth Bastow et al.,“Vernalization Requires Epigenetic Silencing ofFLC by HistoneMethylation,”Nature427,no.6970(2004):164–67;YuehuiHe,MarkR.Doyle, and Richard M. Amasino, “PAF1-Complex-Mediated HistoneMethylation ofFlowering Locus C Chromatin Is Required for theVernalization-Responsive, Winter-Annual Habit in Arabidopsis, ”Genes&Development18,no.22(2004):2774–84.1 2 8How this occurs, and how it’s regulated : Pedro Crevillen andCaroline Dean, “Regulation of the Floral Repressor GeneFLC: TheComplexity ofTranscription in aChromatinContext,”CurrentOpinioninPlantBiology14,no.1(2011):38–44.1 2 9Barbara Hohn’s laboratory in Basel : Jean Molinier et al.,“Transgeneration Memory of Stress in Plants,”Nature 442, no. 7106(2006):1046–49.1 3 0Igor Kovalchuk created a follow-up: Alex Boyko et al.,“Transgenerational Adaptation ofArabidopsis to Stress Requires DNAMethylationandtheFunctionofDicer-LikeProteins,”PLoSOne5,no.3(2010):e9514.131Hohn’s results were not : Ales Pecinka et al., “TransgenerationalStressMemoryIsNotaGeneralResponseinArabidopsis,”PLoSOne4,no.4(2009):e5202.1 3 1The growing consensus, however: Eva Jablonka and Gal Raz,“TransgenerationalEpigeneticInheritance:Prevalence,Mechanisms,andImplicationsfortheStudyofHeredityandEvolution,”QuarterlyReviewof Biology 84, no. 2 (2009): 131–76; Faculty of 1000, evaluations,dissents,andcommentsforMolinieretal.,“TransgenerationMemoryofStress in Plants,” Faculty of 1000, September 19, 2006,F1000.com/1033756; Ki-Hyeon Seong et al., “Inheritance of Stress-Induced,ATF-2-Dependent Epigenetic Change,”Cell145,no.7 (2011):

1049–61.131Inall cases, this“memory”:TiaGhose, “HowStress Is Inherited,”Scientist (2011),http://the-scientist.com/2011/07/01/how-stress-is-inherited.132Itwasagreatsurprise:EricD.Brenneretal.,“ArabidopsisMutantsResistant to S(+)-Beta-Methyl-Alpha, Beta-Diaminopropionic Acid, aCycad-DerivedGlutamateReceptorAgonist,”PlantPhysiology124,no.4(2000):1615–24;Hon-MingLametal.,“Glutamate-ReceptorGenesinPlants,”Nature396,no.6707(1998):125–26.132At this pointwe still: ErwanMichard et al., “GlutamateReceptor–LikeGenesFormCa2+Channels inPollenTubesandAreRegulatedbyPistilD-Serine,”Science332,no.434(2011).132Tulving further proposed : Tulving, “How Many Memory SystemsAreThere?”1 3 3“lowest level of”: Cvrckova, Lipavska, and Zarsky, “PlantIntelligence.”EPILOGUE:THEAWAREPLANT135Everyone from Alfred Binet : Alfred Binet, Théodore Simon, andClara Harrison Town,AMethod of Measuring the Development of theIntelligence of Young Children (Lincoln, Ill.: Courier, 1912); HowardGardner,Intelligence Reframed: Multiple Intelligences for the 21stCentury(NewYork:BasicBooks,1999);StephenGreenspanandHarveyN. Switzky, “Intelligence Involves Risk-Awareness and IntellectualDisability Involves Risk-Unawareness: Implications of a Theory ofCommon Sense,”Journal of Intellectual andDevelopmentalDisability,inpress(2011);RobertJ.Sternberg,TheTriarchicMind:ANewTheoryofHumanIntelligence(NewYork:Viking,1988).135Whilesomeresearchersconsider:ReuvenFeuerstein,“TheTheoryofStructural Modifiability,” inLearning and Thinking Styles: ClassroomInteraction, edited by Barbara Z. Presseisen (Washington, D.C.: NEAProfessional Library, National Education Association, 1990); ReuvenFeuerstein, Refael S. Feuerstein, and Louis H. Falik,Beyond Smarter:Mediated Learning and the Brain’s Capacity for Change (New York:TeachersCollegePress,2010);BinyaminHochner,“Octopuses,”Current

Biology 18, no. 19 (2008): R897–98;BrittAnderson, “TheG Factor inNonhuman Animals,”Novartis Foundation Symposium 233 (2000): 79–90,discussion90–95.135“It appears to me”: William Lauder Lindsay, “Mind in Plants,”BritishJournalofPsychiatry21(1876):513–32.135Anthony Trewavas, an esteemed : Anthony Trewavas, “Aspects ofPlantIntelligence,”AnnalsofBotany92,no.1(2003):1–20.136Controversy arose among plant biologists : Eric D. Brenner et al.,“PlantNeurobiology:AnIntegratedViewofPlantSignaling,”Trends inPlantScience11,no.8(2006):413–19.136Some of these similarities: Frantiöek Baluöka, Simcha Lev-Yadun,and Stefano Mancuso, “Swarm Intelligence in Plant Roots,”Trends inEcologyandEvolution25,no.12 (2010):682–83;FrantiöekBaluökaetal., “The ‘Root-Brain’ Hypothesis of Charles and Francis Darwin:RevivalAfterMoreThan125Years,” PlantSignaling&Behavior4,no.12(2009):1121–27;ElisaMasietal.,“SpatiotemporalDynamicsoftheElectrical Network Activity in the Root Apex,”Proceedings of theNationalAcademyofSciencesoftheUnitedStatesofAmerica106,no.10(2009):4048–53.136Manyotherbiologistswho:AmedeoAlpietal.,“PlantNeurobiology:NoBrain,NoGain?,”TrendsinPlantScience12,no.4(2007):135–36.139TheInternationalAssociationfortheStudyofPain:JohnJ.Bonica,“NeedofaTaxonomy,”Pain6,no.3(1979):247–52.Seealsowww.iasp-pain.org/AM/Template.cfm?Section=Pain_Definitions&Template=/CM/HTMLDisplay.cfm&ContentID=1728#Pain1 3 9Indeed, even in humans: Michael C. Lee and Irene Tracey,“Unravelling the Mystery of Pain, Suffering, and Relief with BrainImaging,”CurrentPainandHeadacheReports14,no.2(2010):124–31.140Forexample,in2008:AlisonAbbott,“Swiss‘Dignity’LawIsThreattoPlantBiology,”Nature452,no.7190(2008):919.

Acknowledgments

WhataPlantKnowswouldneverhavebeenpublishedwithouttheinputofthreeamazingwomen.First, my wife, Shira, who encouraged me to push the envelope, do

something beyond academic research andwriting, and, finally, to press“send.” Without her love and belief, this book would never havehappened.Second, my agent, Laurie Abkemeier. Her experience, tenacity,

support,andboundlessoptimismmadeanaiveauthorfeellikeaPulitzerPrize–winningveteran.Iwasfortunateinfindingnotonlyanagentbutafriend.Third,my editor at ScientificAmerican / Farrar, Straus andGiroux,

Amanda Moon, who had the daunting task of turning my academicwordingintoreadableprose.Amandaworkedtirelesslytoeditandreediteachchapter,and thendo itagaina third,a fourth,anda fifth time,allwithutmostpatience.Many scientists from around the world helped me craft this into a

scientifically validwork. Professors IanBaldwin (MaxPlanck InstituteforChemicalEcology),JanetBraam(RiceUniversity),JohnKiss(MiamiUniversity),ViktorZarsky(AcademyofSciencesoftheCzechRepublic),andEricBrenner(NewYorkUniversity)werekindenoughtotaketimefromtheirbusyschedulestoreadpartsofthisbookandtomakesurethatthe sciencewas fairly presented. The idea for this book originated indiscussions with Eric, and I will be forever thankful for his insight,encouragement, and friendship. I also thankProfessor JonathanGressel(Weizmann Institute of Science), Dr. Lilach Hadany (Tel AvivUniversity), Professor Anders Johnsson (Norwegian University ofScience and Technology), Professor Igor Kovalchuk (University ofLethbridge), and Dr. Virginia Shepherd (the University of New SouthWales) for input at various stages of this project. The influence ofmymentors,ProfessorJosephHirschbergandProfessorXing-WangDeng,is

feltinallthescienceIdoandwrite.IthankKarenMaineforhereditsanddiligenceinkeepingmeontime,

Ingrid Sterner for an amazing copyedit, and the team at ScientificAmerican/Farrar,StrausandGiroux,whowerewonderfultoworkwith.I am lucky to have fabulous colleagues at TelAviv University who

providedmanyhelpfulhallwaydiscussionsandideas.Inparticular,manyoftheideasinthisbookwereexploredfirstwithProfessorsNirOhadandShaulYalovsky in our course Introduction to Plant Sciences. Iwant tothankmylabmates,Ofra,Ruti,Sophie,Elah,Mor,andGiri,foracceptingmy absences in overseeing their research while I wrote this book andespeciallyDr.TallyYahalom,whocoveredformeinrunningthelab.Mydailyinteractionwiththemisaconstantreminderofwhyresearchissoexciting. I’m also indebted to the benefactor of theManna Center forPlantBioscienceswho has helped showme howmodesty coupledwithfocuscansynergizetoreachimportantgoals.Iwish to thankAlanChapelski for theportrait, andDeborahLuskin,

whohelpedmestarttowrite.Myimmediateandextendedfamilieshavebeen a source of unending support. From my sister, Raina, to Ehud,Gitama, Yanai, Phyllis, and my mother, Marcia, who were the firstreaders of the manuscript, I am forever thankful. My children, Eytan,Noam,andShani,areconstantsourcesofjoyandwereevenavailabletoprovide me with a missing word. And lastly, my father, David, whoofferedmeeditsandconstantsupport,andlivedvicariouslythroughthebook’spublication.

IndexTheindexthatappearedin theprintversionof this titledoesnotmatchthepagesofyoureBook.PleaseusethesearchfunctiononyoureReadingdevicetosearchfortermsofinterest.Foryourreference,thetermsthatappearintheprintindexarelistedbelow.Pagenumbersinitalicsrefertoillustrations.acneremediesAdvilAge,TheAgricultureDepartment,U.S.alderalgae;greenAllard,HarryA.Amorphophallustitanum,seecorpsefloweramplitudeamyloplastsanimals:geneticmakeupofplantsvs.;intelligencein;pheromonesin;plants’ communication with; as prey for carnivorous plants; in seeddispersal;senseoftouchin;tactilestressonplantsfromanoeticconsciousnessanteriorcruciateligament(ACL)anthropomorphism;cautionsabout;media’ssensationalpromotionofapicalbudsapicaldominanceapples, ripening experiment on arabidopsis (Arabidopsis thaliana;mustard plant); in blindmutant plant experiment; circumnutation in;effect of neuroactive drugs on; genome of; in gravity experiment; inhearing;asidealplantforresearch;namingofmutantsin;spaceflightexperimentson;vernalizationinArizona,Universityof

aspirin(acetylsalicylicacid)auditorynerveautonoeticconsciousnessautumn;inplantcycleauxin(movementhormone)Avenasativa,seeoatsavocadosazaleas

Bach,JohannSebastianbacteriabalance,senseofBaldwin,IanBaluöka,FrantiöekbananasbanyantreesbarleyBaryshnikov,MikhailBash ,Matsuobassoonmusicbatsbattery,cellanalogytobeanseedlings,inorientationexperimentbeansprouts:circumnutationin;inlightexperimentBeatlesbees,buzzingofbeetle-eatingarthropodsbeetlesBenfey,PhilBengayointmentBern,Universityofbeta-myrceneBidenspilosa,seeSpanishneedleBinet,Alfred

biology,parallelsbetweenplantandhumanBiosatelliteIIIBird,Christopherbirdsblindmutantplantexperimentblindness:inhumans;inmoles;inplantsbluelight;incircadianrhythms;inphototropismBonham,JohnBonn,UniversityofBose,JagadishChandraBowles,DiannaBoysen-Jensen,PeterBozotheClown,plantmovementcomparedtoBraam,Janetbrain: in hearing; as lacking in plants; in memory formation andstorage; painvs. suffering in; inproprioception; in senseof sight; insenseofsmell;insenseoftouchbrainstemBrassicaoleracea,seewildcabbageBRCAgenesBrown,AllanH.Brubeck,DaveBurdon-Sanderson,John;ascriticalofBoseburrcucumber(Sicyosangulatus)burrsButler,WarrenL.buzzpollination

cabbagecalcium:inelectrochemicalsignaling;insenseoftouchcalcium-bindingproteinscalciumsignalingcalmodulin(calcium-modulatedprotein)canarygrass(Phalariscanariensis)

cancer;breastcapsaicincardiacmonitorsCarolinascaterpillarscells:biologyofplant;differentiationof;discoveryof;divisionof;inears;inelectrochemicalsignaling;elongationofcellwallCenterforResearchandAdvancedStudiescentrifugeexperimentsCFTRgeneschemicalsignalingcherrytreeschilipepperschimpanzeesChinese,ancientchlorophyllchromatinchromosomeschrysanthemumsciliacircadianclockcircadianrhythmscircumnutation;andgravitropism;speedofcitrus,ripeningofclassicalmusicclovercocklebur(Xanthiumstrumarium)coiling:memoryincoldtreatments,artificial,seevernalizationcolor:humanperceptionof;plantperceptionofColoradoStateUniversitycolor-blindnessColumbiaspaceshuttle

commonancientancestorcomputermemoryconesconsciousnessCOP9signalosomecorn(Zeamays)CornellUniversity,BoyceThompsonInstituteatcorpseflower(Amorphophallustitanum)cotyledonsCreath,KatherinecryptochromecryptogamicplantsCSI(TVshow)cucumbersCusuctapentagona,seedodderplantcysticfibrosis

darkness:asmeasuredbyplants;plants’perceptionofDarwin,Charles:evolutionarytheoryof;gravityexperimentof;musicexperiment of; phototropism studies of; plant motion study of; andplant neurobiology hypothesis; seedling tip phototropism experimentof;studyofVenusflytrapbyDarwin,Francis;gravityexperimentofDavidRoseOrchestraDavyFaradayResearchLaboratorydaylight,plants’perceptionof“deaf”genesdeafness:inhumans;inplantsdefensehormonesDeMoraes,ConsueloDenny,FrankE.depolarizationdigestion,inVenusflytrapDionaeamuscipula,seeVenusflytrap

diseasegenesDNA;ofarabidopsis;epigeneticsand;“jumpinggenes” in;mutationsin;noncoding;inplantcells;intransgenerationalmemoryDobzhansky,Theodosiusdodderplant(Cuscutapentagona);culinarypreferencesof;experimentondogsdolphins“don’ttouchme”plantDostál,RudolfdoublehelixDroserarotundifolia,seesun-dewplantdrought;effectontreesofdrugs,neuronsignalsinhibitedbyDuhamelduMonceau,Henri-Louisdynamicawareness

ears;ofbats;ascomparedtoroots;ofdogs;inhumandeafness;inner;aslackinginplants;inproprioceptionecotypesEdinburgh,UniversityofEdsall,Pamelaego,aslackinginplantsEgyptians,ancientelectricity:inneuralcommunication,seeelectrochemicalsignaling;intriggeringofMimosapudica;intriggeringofVenusflytrapelectrochemicalgradientselectrochemicalsignalingelectromagneticwaveselephantsemotions:aslackinginplants;physicalsensationsand;senseofsmellin;seealsoanthropomorphismendodermisenvironment: animals and humansmodified by; genes controlled by;

plants’adaptationto;plants’awarenessof;plants’optimizationofepigenetics;seealsotransgenerationalmemoryepisodicmemoryethylenegas,inripeningethylenereceptorseyes;photoreceptorsin“eyes,”ofplanteyespots

falsedeathfar-redlightfeeling,senseofFeijó,Joséfernsfigsfishflax seedlings (Linum usitatissimum), morphogenetic memoryexperimentsonFLC(floweringlocusC)genefliesFlorence,UniversityofFlorida,farminginflowering:artificialmanipulationoflighttoinduce;effectofcoldon;effectoftouchon;partofplantthatregulatesflowers,inpollinationfood: for carnivorous plants; plants’ use of light to produce,seephotosynthesisFrenchAcademyofSciencesfrequency,ofsoundwavesfrogsfrost,effectontobaccooffruit:artificialripeningof;ethyleneemittedby;seealsoripeningfruitfliesfungi

Galston,ArthurGane,RichardGardner,HowardGarner,WightmanW.gaschromatography-massspectrometrygenes: definition of; disease; function of; mutation in; naming of;scarecrow;sharedbyplantsandanimals;sharedbyplantsandhumans;TCH;transcribed;transpositionofgenome:arabidopsis;humangermination; incircumnutation;ofdodder;heat in;musicexperimentforglutamatereceptorsgorillasGrandmotherWillowgravireceptorsgravitropismgravity:C. and F.Darwin’s bean seedling experiment in;Duhamel’sbean seedling experiment in; in reorientation; root caps in; root vs.shoot in;scarecrow gene experiment in; spaceflight experiments ineffectsof;seealsocircumnutation;gravitropismGreece,ancientgreenhouses,plantsgrowningreenlightGregorianChantGressel,Jonathan

Hadany,Lilachhaircells;inearshand-eyecoordinationhappinesshealingenergyexperimenthearing, sense of: in animals; dearth of research on; definition of;dubious evidence for; in forest sounds; in humans; necessity of; inplants;plantvs.human

heartfunctionHeil,MartinHelianthusannuus,seesunflowerHendrix,Jimihertz(Hz)HippocrateshistonesHodick,DieterHohn,BarbaraHooke,Roberthormones,planthostplantshumans: calcium in; calmodulin in; as caring; color perception in;deafnessin;anddependenceonplants;empathyforanimalsby;genesindiseasesof;genomeof; intelligencein; ininteractionswithplants;memoryin;nervoussystemof;painperceptionby;proprioceptionin;senseofhearingin;senseofsightin;senseofsmellin;senseoftouchin;intactilestressonplants;treatmentofillnessin;seealsobrain

idimmunememoryincenseIndiainebriationinfraredlightinnerearInsectivorousPlants(C.Darwin)insects:plantsattackedby;aspreyforcarnivorousplantsintelligence:inhumans;naturalselectionin;inplants;plantvs.animalandhuman;vs.awarenessinternalclocksInternationalAssociationfortheStudyofPainInternationalLaboratoryofPlantNeurobiologyInternationalSpaceStation,gravityexperimentson

IQtestirisesIsraelsson,Donald

Jaffe,MarkJapanAerospaceExplorationAgencyjasmonicacidjetlagJohnsson,AndersJournalofAlternativeandComplementaryMedicine,The“jumpinggenes,”

Kennedy,JohnF.kerosene,inripeningKiss,JohnKlein,RichardkneesKnight,ThomasAndrew“know,”author’suseoftermKoornneef,MaartenKovalchuk,Igor

Lamarck,Jean-Baptistelateralbudsleaf movement, in carnivorous plants,see Mimosa pudica; Venusflytrapleafsenescence,ethyleneasregulatorofleaves: cells in; death of; insect damage to; as lacking in dodder;moving,seeMimosapudica;Venus flytrap;negativeeffectsof touchon; in photoperiodism; in plant communication; of Venus flytrap;whitespotson;woundedLedZeppelinLeeds,Universityoflemons

lettuceleukemialichenslight: activation switch for; artificial manipulation of; in circadianrhythms; in coiling; in flowering; as food for plants,seephotosynthesis;asperceivedbyplants;inplantdevelopment;responseofseedlingtipsto;seealsophototropismlightwaveslimabeans(Phaseoluslunatus);communicationexperimentsonlimbicsystemLindsay,WilliamLauderLinumusitatissimum,seeflaxseedlings“long-day”plantslong-termmemory;oftraumainplantsLosAngelesTimesLundInstituteofTechnologyLysenko,TrofimDenisovich

MacbethMcClintock,BarbaraMancuso,Stefanomangrovetreesmarigold(Tageteserecta);musicexperimentonMarylandMarylandMammothtobaccoMaxPlanckInstituteforChemicalEcologyMeatLoafmechanoreceptors;forhearing;fortouchmemory: of cold; computer; delayed response as component of;encoding(forming)of;epigeneticsin;inflowering;human;inplants;plant vs. human; processes of; recalling (retrieval) of; retaining(storage)of;senseofsmell in;sensory input in; transgenerational; inVenusflytrapMendel,Gregor

MendeliangeneticsmenstrualcyclesmentholMerkel’sdisksMetamorphosis(Ovid)methylationmethyljasmonatemethylsalicylateMiamiUniversitymicemicrogravitymicrowavesMiddleEast,ancientMimosapudica;leafmovementin;nicknamesfor;researchonMitchell,Mitchmitochondriamoleculargeneticsmoles,blindnessinmorningglory(Pharbitisnil);gravityexperimentonmorphogeneticmemorymossesMother’sDaymotorproteinsmouthmovementhormone(auxin)Mozart,WolfgangAmadeusMuir,Johnmuscle-motormemorymuscles:inhumans;movementwithoutmusic, effect on plant growth of; C. Darwin’s experiment with; asirrelevant to plants; Klein and Edsall’s experiment with; lack ofscientific evidence for; Retallack’s experiment with; Scott’sexperimentwithMuzak

myosins

nanomotorsNativeAmericansnectar;asattractivetoinsectsnegativegravitropismnervoussystem:human;aslackinginplantsneucleotides;A,T,C,andGneuroreceptorsneurotransmittersNewAgeNewYorkBotanicalGardenNewYorkTimes,TheNewYorkUniversityNicotianatabacum,seetobacconitrogennociceptorsnoeticconsciousnessnosenoxiousweedsnucleotidesnucleusnutation

oaktreesOakwoodUniversityoats(Avenasativa)octopusesOhioBoardofAgricultureOhioUniversityokraseedsolfaction,seesmell,senseofolfactoryeavesdroppingolfactorynerves

olfactoryreceptorsOntheOriginofSpecies(C.Darwin)orangelightorangutansOrians,GordonotolithsOvid

pain:humanperceptionof;asnotexperiencedbyplants;vs.touchpainreceptors,seenociceptorsparasiticplants;seealsododderplantpeaplantspearspeaspeatendrils,memoryexperimentinpenguinsPennStateUniversitypeppermintpercussion,effectonplantsofperennialsperfumes;limabean;tomato;wheatpetiolePfeffer,WilhelmPhalariscanariensis,seecanarygrassPharbitisnil,seemorninggloryPhaseoluslunatus,seelimabeansphenolicchemicalspheromonesphloemphosphorusphotoperiodismphotopsinsphotoreceptors:ineyes;fiveclassesof;pairsof;inplantsphotosynthesis

phototropinsphototropism; Boysen-Jensen’s experiment on; Darwin’s experimentonPhysiologyandBehaviorofPlants(Scott)phytochemicalsphytochromepictures,plantsinabilityto“see”inpinetreespitchplace,senseof;seealsogravity;proprioception;reorientationplantcommunication;betweenplantsandanimals;experiments in; insignalingdanger;withinvs.betweenplantsplantneurobiologyhypothesisplants: adaptation to environment by; anatomy of; awareness vs.intelligencein;inbendingtowardlight,seephototropism;carnivorous;seealsoVenusflytrap;chemicalsextractedfrom;colorperceptionof;dancing in; as deaf; “dignity” of; effect of vibration on; geneticcomplexity of; genetic makeup of animals vs.; genetic research on;human dependence on; information networks in; intelligence in;interaction of humans on; light perception of; medicinal use of;movementin;nervoussystemlackingin;painnotexperiencedby,plants(cont.)139;parasitic;perennial;reorientationin;roleofleavesin; scents emitted by; in self-protection against damage; in self-protection against disease; senses of,see specific senses; sharedbiology between humans and; stationary (sessile) nature of; tactileinteraction with; tactile stresses on; tallness in; temperaturedifferentiationby;tracingthemotionpatternsof“plant-specificgenes,”“plantvision,”PocahontasPollan,Michaelpollination:bybees;scentsinPopulusalba,seewhitepoplarpositivegravitropism

potassium:inelectrochemicalsignaling;inwiltingpotatoesPowerofMovementinPlants,The(C.Darwin)PowerofPrayeronPlants,TheprefrontalcortexprionsproceduralmemoryProceedingsoftheRoyalSocietyofLondonproprioception;plantvs.human;vs.senseoftouch;seealsogravityproteinaseinhibitorsproteins; calcium-binding; in coding of genes; in memorymaintenance;motorprotoplastpruningpulvinuscellspurplelightputrescine

QuotationsforSpecialOccasions(vanBuren)

radioantennasradiowavesrain:astactilestress;onVenusflytrapleavesrainbowsRaskin,Ilyaredlightreorientation;centrifugeexperimentfor;overshootinginRetallack,Dorothy;scientificshortcomingsofmusicresearchbyretinaRhoades,DavidrhodopsinRiceUniversityripening; artificial methods of; experiment in; smell in; traditionalmethodsof

RNArockmusic;seealsospecificartistsrodsrootcaproothairsroots:aerial;cellsin;ascomparedtoears;reorientationof;vs.neuralnetworksroottips,ingravityrosesRouen,UniversityofRutgersUniversity

sagebrushsalicylicacidSalisbury,FrankSalixalba,seewhitewillowsaltbalanceSarasotaHerald-TribunescarecrowgeneSchoenberg,ArnoldSchultz,JackSchwartz,GaryScienceScott,PeterSecretLifeofPlants,The(TompkinsandBird);author’scriticismof;plantresearchstymiedbyseeddispersalseedlingtipphototropismexperimentsemanticmemorysemicircularcanalssenses:inmemory;ofplantsvs.animals;seealsospecificsenses“sensitiveplant,”sensorymemory

sensoryneuronssequoiasShakespeare,WilliamShankar,RaviShidare-asagao,see“weeping”morninggloryshoots,inreorientationofplantsshoottip,ofdodder;seealsoseedlingtipexperiment“short-day”plantsshort-termmemory;inVenusflytrap“shyvirgin”plantSicyosangulatus,seeburrcucumberSievers,Andreassight,senseof:definitionof;inhumans;plantascomparedtohuman;inplants;vs.senseofsmellsilvernitratesixthsense,seeproprioceptionskinsmell, senseof: definitionof; inhumans;humanvs. plant; lock-and-key analogy for; in plants; plant-to-plant communication through;receptorsfor;socialramificationsof;vs.senseofsightsmellreceptorssmoke,inripeningsnow,astactilestressSocietyforPlantNeurobiologySocietyofPlantSignalingandBehaviorsodium,inelectrochemicalsignalingSolanumlycopersicum,seetomatoessonarSoundofMusicandPlants,The(Retallack)soundwaves;agriculturaluseofSovietUnionsoybeansspaceflight,ingravityexperiments

Spanishneedle(Bidenspilosa),morphogeneticmemoryexperimentonspinalcordspinedamagespiraling,seecircumnutationspring,inplantcycleStanfordUniversitystaticawarenessstatoliths;gravityexperimentwithstems:ingravitystereociliaStolarz,Mariastomatastrawberriesstress,intransgenerationalmemorysuffering,seepainsugarmaplessun-dewplant(Droserarotundifolia)sunflower(Helianthusannuus);spaceflightexperimentsonsuperego,aslackinginplantsSusquehannocktribeSwissFederalConstitution

tactilesensation,seetouch,senseoftactilestressTageteserecta,seemarigoldTakahashi,HideyukiTalkingHeads“talkingtrees,”tannicchemicalstaste,senseof,asconnectedtosmellTaxolTCH(touch-activated)genestearsTelAvivUniversity

TempleBuellCollegeterminology,ofhumanexperienceasappliedtoplantstestosteroneThellier,Michelthigmomorphogenesisthornsthoughts,plantgrowthpurportedlyaffectedbytime-lapsephotographytobacco(Nicotianatabacum);memoryintomatoes (Solanum lycopersicum); dodder’s preference for; inenvironmentaladaptationexperimentTompkins,Petertonguetouch,senseof:emotionalconnotationsof;inhumans;negativeeffectso f ,see tactile stress; plant growth inhibited by; in plants; plants’geneticmakeupchangedby;plantvs.human;subjectivityin;vs.pain;vs.proprioceptiontransgenerationalmemory;stressstudyontrees;environmentaladaptationofTrewavas,AnthonyTriticumaestivum,seewinterwheattrunks,vs.skeletontulips;circumnutationofTulving,EndelTuscanyTylenol

ultraviolet(UV)lightUniversityCollege

vanBuren,MaudvegetalintelligenceVenus flytrap (Dionaea muscipula); leaves of; naming of; preyevaluated by hairs of; short-termmemory in; triggering experiments

on;triggeringthetrapofVERITASResearchProgramvernalization;FLCinvestibulevibrationvines;touchinvineyardsvirusesvision,seesight,senseof,inhumans“visualspectra,”Volkov,AlexandervolumevonSachs,JuliusVortexHealing

WageningenUniversity,HollandWashington,D.C.,cherrytreefloweringinWashington,Universityofwater:absorptionof;inleafmovement;inxylemvesselswaterwheel,incentrifuge“weeping”morningglory(Shidare-asagao)Weinberger,PearlWeizmannInstitutewheat; circumnutation in; in dodder experiment; genes in;see alsowinterwheat“WhenTreesTalk,”whitelightwhitepoplar(Populusalba)whitewillow(Salixalba);memoryinwildcabbage(Brassicaoleracea)willowbarkwilting,droopingwind,astactilestressWindsorStar,The

winter,inplantcyclewinterwheat(Triticumaestivum)WorldWarIIwounding

Xanthiumstrumarium,seecockleburX-raywavesxylemvessels

yellowlight

(Z)-3-HexenylacetateZeamays,seecornZeugin,FabiennezucchiniseedsZweifel,Roman

ILLUSTRATIONCREDITS13 Amédée Masclef,Atlas des plantes de France (Paris: Klincksieck,1891).14VardaWexler.16 Ernst Gilg and Karl Schumann,Das Pflanzenreich, Hausschatz desWissens(Neudamm:Neumann,ca.1900).22 USDA-NRCS PLANTS Database / Nathaniel Lord Britton andAddison Brown,An Illustrated Flora of the Northern United States,Canada, and the British Possessions, 3 vols. (New York: CharlesScribner’sSons,1913),2:176.32 USDA-NRCS PLANTS Database / Nathaniel Lord Britton andAddison Brown,An Illustrated Flora of the Northern United States,Canada, and the British Possessions, 3 vols. (New York: CharlesScribner’sSons,1913),3:49.36 Prof. Dr. OttoWilhelm Thomé,Flora vonDeutschland,Österreich,undderSchweiz(Gera:Köhler,1885).37WalterHoodFitch, IllustrationsoftheBritishFlora(London:Reeve,1924).40 Francisco Manuel Blanco,Flora de Filipinas [Atlas II] (Manila:Plana,1880–83).42Modifiedfromfigures2and3,inMartinHeilandJuanCarlosSilvaBueno, “Within-Plant Signaling by Volatiles Leads to Induction andPriming of an Indirect Plant Defense in Nature,”Proceedings of theNationalAcademyofSciencesoftheUnitedStatesofAmerica104,no.13(2007): 5467–72. Copyright © 2007 National Academy of Sciences,U.S.A.46 Illustration from a photograph ofAmorphophallus titanum inWilhelmabyLotharGrünz(2005).51 USDA-NRCS PLANTS Database,http://plants.usda.gov, accessedAugust 25, 2011, National Plant Data Team, Greensboro, N.C., 27401-4901U.S.A.54 Taken from figure 12, in Charles Darwin,Insectivorous Plants

(London:JohnMurray,1875).59 Paul Hermann Wilhelm Taubert,Natürliche Pflanzenfamilien(Leipzig:Engelmann,1891),3:3.61 USDA-NRCS PLANTS Database / Nathaniel Lord Britton andAddison Brown,An Illustrated Flora of the Northern United States,Canada, and the British Possessions, 3 vols. (New York: CharlesScribner’sSons,1913),3:345.67 USDA-NRCS PLANTS Database / Nathaniel Lord Britton andAddison Brown,An Illustrated Flora of the Northern United States,Canada, and the British Possessions, 3 vols. (New York: CharlesScribner’sSons,1913),3:168.76 George Crouter, in Dorothy L. Retallack,The Sound of Music andPlants(SantaMonica,Calif.:DeVorss,1973),p.6.79FranciscoManuelBlanco,FloradeFilipinas,book4(Manila:Plana,1880–83).81 Prof. Dr. OttoWilhelm Thomé,Flora vonDeutschland,Österreich,undderSchweiz(Gera:Köhler,1885).96VardaWexler.98 Taken from figure 196, in CharlesDarwin and Francis Darwin,ThePowerofMovementinPlants(NewYork:D.Appleton,1881).101WalterHoodFitch,Curtis’sBotanicalMagazine vol.94,ser.3,no.24(1868),plate5720.105USDA-NRCSPLANTSDatabase/A.S.Hitchcock,revisedbyAgnesChase,ManualoftheGrassesoftheUnitedStates,USDAMiscellaneousPublicationno.200(Washington,D.C.:U.S.GovernmentPrintingOffice,1950).107 Taken from figure 6, in Charles Darwin and Francis Darwin,ThePowerofMovementinPlants(NewYork:D.Appleton,1881).108 USDA-NRCS PLANTS Database / USDA Natural ResourcesConservation Service,Wetland Flora: FieldOffice IllustratedGuide toPlantSpecies.120VardaWexler.121 USDA-NRCS PLANTS Database / Nathaniel Lord Britton andAddison Brown,An Illustrated Flora of the Northern United States,

Canada, and the British Possessions, 3 vols. (New York: CharlesScribner’sSons,1913),2:436.123 USDA-NRCS PLANTS Database / Nathaniel Lord Britton andAddison Brown,An Illustrated Flora of the Northern United States,Canada, and the British Possessions, 3 vols. (New York: CharlesScribner’sSons,1913),3:497.125USDA-NRCSPLANTSDatabase/A.S.Hitchcock,revisedbyAgnesChase,ManualoftheGrassesoftheUnitedStates,USDAMiscellaneousPublicationno.200(Washington,D.C.:U.S.GovernmentPrintingOffice,1950).

ANOTEABOUTTHEAUTHORDanielChamovitz, Ph.D., is the director of theMannaCenter forPlantBiosciences at Tel Aviv University. He grew up in Aliquippa,Pennsylvania, and studied at Columbia University before receiving hisPh.D.ingeneticsfromtheHebrewUniversityofJerusalem.HehasbeenavisitingscientistatYaleUniversityandattheFredHutchinsonCancerResearch Center in Seattle, and has lectured at universities worldwide.His research on plants and fruitflies has appeared in leading scientificjournals. Chamovitz lives with his wife and three children in HodHaSharon,Israel.Hiswebsiteiswww.danielchamovitz.com.

Notes

1Morespecifically,arabidopsishasatleastelevendifferentphotoreceptorsthat fall into five distinct classes (phototropins, phytochromes, andcryptochromes, plus two additional classes). Other plants also containthesefiveclasses,butmayhavemoreorfewermembersofeachclass.

2Greenalgae,themostprimitiveformsofplants,haveanorganelletermedtheeyespotthatallowsthealgalcellstosensechangesinlightdirectionandintensity.Theseeyespotshavebeenconsideredthesimplestformsofeyesinnature.

3The name “cryptochrome” is actually the result of a joke made byJonathanGressel of theWeizmann Institute.Gressel hadbeen studyingblue-lightresponsesinagroupoforganismsthatincludelichens,mosses,ferns,andalgae,whicharealsocalledcryptogamicplants(thisnamewillbe significant, as we’ll see in a second). But like all other researchersstudying theeffectsofblue lightondifferent creatures,hedidn’tknowwhat the receptor was for blue light. Despite various attempts overdecades,noonehadsucceededinisolatingthisreceptor;ithadacrypticnature.Anunabashedpunster,Gresselsuggestedcallingtheunidentifiedphotoreceptor“cryptochrome.”Tothechagrinofmanyofhiscolleagues,his joke has become enshrined in scientific nomenclature, even thoughcryptochromeisnolongercryptic,asitwasfinallyisolatedin1993.

4To fully appreciate this, you really have to see it with your own eyes:www.youtube.com/watch?v=NDMXvwa0D9E.

5Baldwin now directs theDepartment ofMolecular Ecology at theMax

PlanckInstituteforChemicalEcologyinJena,Germany.

6Manyinsect-eatingarthropodshavecoevolvedwithplantsandrecognizethe volatile signals emitted by herbivore-attacked plants and use thissignalasafood-findingcue.

7If you’rewondering aboutmethyl jasmonate, the story is quite similar.Methyljasmonateisavolubleformofjasmonicacid,adefensehormonethatplantsemituponleafdamageinflictedbyherbivorouscreatures.

8The “Venus” part of the plant’s name has little to dowith science andmuch to do with the rather lewd imaginations of nineteenth-centuryEnglishbotanists.Seewww.sarracenia.com/faq/faq2880.html.

9Seewww.youtube.com/watch?v=ymnLpQNyI6g for a great example oftheVenusflytrapinaction.

10Soundwaves aremeasured in hertz (Hz),where 1Hz equals onewavecyclepersecond.Wecanhearsoundwavesintherangeof20Hzforlowpitchestoupto20,000Hzfor thehighestpitches.Thelowestnoteonacontrabass,forexample(thelowE),vibratesat41.2Hz,whilethehighestnoteonaviolin(highE)vibratesat2,637Hz.ThehighestConapianovibratesat4,186Hz,andtheCtwooctavesabovethisvibratesatabout16,000Hz.Adog’searrespondstosoundwavesabove20,000Hz(whichis why we can’t hear dog whistles), and bats even emit and detectrebounding soundwaves up to 100,000Hz for their internal sonar thatmapsoutthelandscapeaheadofthem.Attheotherendofthespectrum,an elephant can hear and vocalize soundsbelow 20 Hz, which humanbeingsalsocan’tdetect.

11It’s interesting that they chose “gentle” sounds as they cite Pearl

Weinberger from theUniversity ofOttowa,who used ultrasonicwaves(whicharedefinitelynotgentle)inherstudiesinthe1960sand1970s.

12Creath was trained in VortexHealing, which is described as “a Divinehealingartandpathforawakening.Itisdesignedtotransformtherootsofemotionalconsciousness,healthephysicalbody,andawakenfreedomwithin the human heart. This is the Merlin lineage.” Seewww.vortexhealing.com.

13Nutation is the cyclical swaying or bending movement displayed bydifferentplantparts.

14SomeoftheshortcomingsofRetallack’sresearcharealsopointedoutinTheSecretLifeofPlants.15These numbers should be taken with a grain of salt as the precisedefinitionof“gene”isevolvingandwithitthenumbers.Butthegeneraltrendsandscalesarecorrect.

16This website illustrates myosin in action:www.sci.sdsu.edu/movies/actin_myosin_gif.html.

17This clip,http://phytomorph.wisc.edu/assets/movies/gravitropism.swf,showsa time-lapsemovieofa root that’splacedon its sideandslowlybut surely turns to grow down. Other great movies can be found athttp://plantsinmotion.bio.indiana.edu.

18Inthesetypesofstudies,theseedsareoftenfirsttreatedwithachemicalthatcausesmutations in theDNA.Thechanceof thechemicalworkingonaspecificgeneneededforgravitropismisverysmall,sothousandsofseedlingshavetobetested.Luckily,arabidopsisseedlingsareminuscule,

soscreeningthroughsuchalargenumberispossible.

19Naming mutants in arabidopsis, and indeed in other organisms, is theprerogativeofthescientistwhofirstisolatesthemutant.Thenameofthemutantispresentedinlowercaselettersinitalicsandcorrespondstothename of the mutant gene. Some scientists are more conservative andname their mutants after their obvious characteristics (such as theshortroot mutant of arabidopsis, which has, no surprise, short roots).Others are more creative. Examples of names of arabidopsis mutantsincludescarecrow,toomany-mouths,andwerewolf.20Statoliths in higher (flowering) plants are also known as amyloplasts,modified forms of chloroplasts that contain starch rather thanchlorophyll.

21For examples, seewww.dailymotion.com/video/xlhp9q_wilhem-pfeffer-plant-movement_shortfilms#from=embed.

22For a good example of circumnutation, look at this movie:www.pnas.org/content/suppl/2006/01/11/0510471102.DC1/10471Moviel.mov

23Actually, referring to orbit we say “microgravity” rather than “nogravity”asthereisstillasmallgravitationalpull,ofabout0.001percent.

24Theoverallmechanismofsensinggravityismorecomplexthansimplystatolithsfallingwithinthecell.

25Epigenetics encompasses a wide range of heritable changes that areindependent of DNA sequence. These include chemical changes inhistones,chemicalchangesof theDNA(forexample,DNAmethylation

—see p. 128), different types of small RNAs, and infectious proteinsknownasprions.

26Amajordifferentiatorofcelltypes,likebloodcellsversuslivercellsinpeople, or pollen versus leaf cells in plants, is the structure of theirchromatin,whichaffectswhichgenesareactivated.

27Following the initial controversy, and after much discussion, the plantneurobiologists changed the name of their professional organization in2009 from the Society for Plant Neurobiology to the more acceptedSociety of Plant Signaling and Behavior (though “behavior” is also aninterestingtermnotintuitivelyconnectedtoplants).

28Thiscommitteewasformedtofurtherdefinedignity in termsofplants,as the Swiss Federal Constitution requires “account to be taken of thedignity of living beings when handling animals, plants and otherorganisms.” Seewww.ekah.admin.ch/en/topics/dignity-of-living-beings/index.html.

Copyright©2012byDanielChamovitzAllrightsreserved

ScientificAmerican/Farrar,StrausandGiroux18West18thStreet,NewYork10011

Aportionofchapter2originallyappeared,inslightlydifferentform,inScientificAmerican.www.fsgbooks.com

DesignedbyJonathanD.Lippincott

eISBN9781429946230FirsteBookEdition:April2012

Firstedition,2012LibraryofCongressCataloging-in-PublicationData

Chamovitz,Daniel,1963–

Whataplantknows :a fieldguide to thesenses /DanielChamovitz.—1sted.p.cm.Includesbibliographicalreferencesandindex.

ISBN978-0-374-28873-0(alk.paper)

1.Plants.2.Plantphysiology.I.Title.

QK50.C452012571.2—dc23

2011040179