€¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance...

40
Supporting Information | Turcotte et al. New Phytologist Supporting Information The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events Martin M. Turcotte, Nash E. Turley and Marc. T. J. Johnson The following Supporting Information is available for this article: Methods S1–S3, Fig. S1, Tables S1–S4 Methods S1 Methodological details of the characterization of plant traits To understand how domestication affects the expression of putative defensive traits we measured 10 plant traits. From each plant we measured average leaf toughness from two fully expanded leaves as the grams of force required to penetrate a leaf surface using a force gauge penetrometer (Type 516; Chatillon, USA). We measured leaf wet weight to 10 -6 g from a single leaf disc (7.91 mm 2 ) collected from a fully expanded leaf using an ultra micro balance (XP2U, Mettler Toledo, USA). Leaf discs were removed adjacent to the main veins. We calculated trichome density by averaging counts on each side of the discs. We dried leaf discs for three weeks at room temperature and measured their dry mass to 10 -6 g. Specific leaf area (SLA) was calculated as area of the hydrated leaf disc surface (mm 2 ) divided by dry mass (mg). We calculated leaf dry matter content (LDMC) as dry weight (mg) divided by its wet weight (g). S1

Transcript of €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance...

Page 1: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

New Phytologist Supporting Information The impact of domestication on resistance to two generalist herbivores across 29

independent domestication events Martin M. Turcotte, Nash E. Turley and Marc. T. J. Johnson

The following Supporting Information is available for this article: Methods S1–S3, Fig. S1, Tables

S1–S4

Methods S1 Methodological details of the characterization of plant traits

To understand how domestication affects the expression of putative defensive traits we measured

10 plant traits. From each plant we measured average leaf toughness from two fully expanded

leaves as the grams of force required to penetrate a leaf surface using a force gauge penetrometer

(Type 516; Chatillon, USA). We measured leaf wet weight to 10-6 g from a single leaf disc (7.91

mm2) collected from a fully expanded leaf using an ultra micro balance (XP2U, Mettler Toledo,

USA). Leaf discs were removed adjacent to the main veins. We calculated trichome density by

averaging counts on each side of the discs. We dried leaf discs for three weeks at room

temperature and measured their dry mass to 10-6 g. Specific leaf area (SLA) was calculated as area

of the hydrated leaf disc surface (mm2) divided by dry mass (mg). We calculated leaf dry matter

content (LDMC) as dry weight (mg) divided by its wet weight (g).

Phloem sugars were quantified by first collecting phloem samples using an EDTA

extraction procedure from each plant (Wilkinson & Douglas, 2003). Given the variety of growth

forms we inserted either a large leaf with its petiole or a portion of the stem with its attached

shoots into 300 µL of 5 mM Na2EDTA solution at pH 7.0 for 45 minutes. The extraction was

carried out in a cooler at room temperature that contained beakers filled with saturated KH2PO4

solution to maintain high humidity. Extracts were filtered using 4 mm nylon filters (0.45 µm, Cat#

02542903, Perkin Elmer, USA). Analyses of plant traits treated plant species as the unit of

replication, and so we combined 10 µL of each replicate plant extract and measured phloem

sucrose concentration for each species using methods similar to Wilkinson and Douglas (2003).

We first converted sucrose to glucose by adding 10 µL of extract to 10 µL of 40 U / mL invertase

(Cat. # 9458402; Ward’s Science, USA). We then assayed glucose concentration by combining

S1

Page 2: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

this solution with 155 µL of assay reagent and incubated at 37°C using the GAGO20-KIT (Sigma-

Aldrich; USA). The reaction was stopped after 30 minutes with 150 µL of 12N H2SO4 and the

absorbance of samples were measured at 450 nm at room temperature on a microplate

spectrophotometer (Multiskan GO, Thermo Scientific, USA). Concentrations were calculated by

comparison to glucose standards.

To measure phenolic, carbon, and nitrogen concentration, we harvested all aboveground

plant tissue, flash froze it in liquid nitrogen, and homogenized the tissue using a spatula. This

approach estimates whole plant-level concentrations of metabolites. We placed approximately 60

mg of tissue into 2 mL tubes with several 2.3 mm zirconium beads and further homogenized using

a Powergen High Throughput Homogenizer (Fisher Scientific, USA) until samples were a fine

powder. We combined equal parts powder by weight from each replicate (10 mg) to get one

sample per species. Percent carbon and nitrogen were measured at the Ecosystem Analysis

Laboratory at University of Nebraska-Lincoln using an HCN elemental combustion analyzer (ECS

4010 CHNSO Analyzer, Costech Analytical Technologies, Valencia, USA). We extracted

phenolics by adding 10 mg of powdered tissue to 600 µL of 70% acetone for 45 minutes with

vortexing every 15 minutes. We centrifuged samples at 19000 RCF for 10 minutes, removed 500

µL of the supernatant and added 500 µl of fresh 70% acetone. These steps were repeated four

times resulting in 2 mL of extract from each sample. Acetone was then evaporated off in a vacuum

centrifuge and remaining extract was freeze-dried. Each sample was re-diluted with 200 µL of

distilled water.

Total phenolics and phenolic oxidative capacity were measured following the methods of

Salminen & Karonen (2011). We used a colorimetric assay that first combined 10 µl of our

phenolic extracts with 140 µl of a solution of pH 10 carbonate solution and 0.6% formic acid

solution mixed with a ratio of 9/5 (v/v) respectively in a 96 well plate. Then 50 µl of this solution

was combined with 50 µL 1 N Folin-Ciocalteau and 100 µL 20% sodium carbonate solution. After

60 min of intermittent shaking at 25ºC, absorbance was measured at 730 nm with the microplate

spectrophotometer. Oxidative capacity was measured by first standardizing phenolic

concentration of samples to an absorbance of 1 and oxidizing them by combining 10 µL of

normalized extract with 90 µL of pH 10 carbonate solution. We stopped the oxidization after 90

minutes by adding 50 µL 0.6% formic acid solution. Then, we measured total phenolics on the

oxidized solution as described above. The difference in total phenolics before and after oxidization

was used as a measure of oxidative capacity (Salminen & Karonen, 2011).

S2

Page 3: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

S3

Page 4: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Methods S2 Summary of focal R script for statistical analysesThe statistical significance of model terms were tested by creating nested models and comparing

them using likelihood ratio tests with the function anova (model1, model2). We here illustrate the

full models:

1) Herbivore performance: Analyses performed at the level of the plant.

Survival:

glmer( cbind(Live caterpillars, Dead caterpillars) ~ 1 + DOMESTICATION + (1|

PAIR:SPECIES)+ (DOMESTICATION|PAIR), data=data, na.action=na.omit,

family=binomial)

Caterpillar growth or aphid number:

lmer( log(aphids +1) ~ 1 + DOMESTICATION + (1|PAIR:SPECIES)+ (DOMESTICATION|

PAIR), data=data, na.action=na.omit, REML=F)

2) Effect of date of domestication or cultivation and the tissue under selection: Given that a

single value was required for each crop-wild pair we calculated a proportional change in herbivore

performance.

Difference in performance = (Crop mean value – Wild mean value) / mean (Wild mean value,

Crop mean value)

Date of cultivation or domestication:

lmer( Difference in performance ~ Date + (1|FAMILY), data=data, na.action=na.omit,

REML=F)

Tissue under selection:

lmer( Difference in performance ~ Tissue + (1|FAMILY), data=data, na.action=na.omit,

REML=F)

3) Plant traits under domestication: Traits were log-transformed and standardized before

analysis.

lmer( trait ~ 1 + DOMESTICATION + (DOMESTICATION|PAIR), data=SPP,

na.action=na.omit, REML = F)

S4

Page 5: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

4) Multiple regression analyses of plant traits driving resistance:

Traits were log-transformed and standardized before analysis.

Survival:

dredge( glmer(cbind(Live caterpillars, Dead caterpillars) ~ DOMESTICATION*RGR +

DOMESTICATION*Toughness + DOMESTICATION*Trichomes +

DOMESTICATION*SLA + DOMESTICATION* LDMC + DOMESTICATION*Total

Phenolics + DOMESTICATION*Phloem Sugar+ DOMESTICATION*P.Carb +

DOMESTICATION*P.Nit+ (1|FAMILY/PAIR), data=s.ldata, family=binomial),

beta = F, evaluate = T, rank = AIC, trace = T)

Caterpillar growth and aphids number:

dredge( lmer( log(Aphids +1) ~ DOMESTICATION*RGR + DOMESTICATION*Toughness +

DOMESTICATION*Trichomes + DOMESTICATION*SLA + DOMESTICATION* LDMC +

DOMESTICATION*Total Phenolics + DOMESTICATION*Phloem Sugar+

DOMESTICATION*P.Carb + DOMESTICATION*P.Nit+ (1|FAMILY/PAIR), data=a.ldata,

REML= F), beta = F, evaluate = T, rank = AIC, trace = T)

S5

Page 6: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Methods S3 Phylogenetic inference and explicit analyses of resistance

traitsWe inferred the phylogeny of the wild relatives using the Phylomatic v.3 online tool

(http://phylodiversity.net/phylomatic/) based on the R20120829 megatree (Webb & Donoghue,

2005). The tree was dated using fossil dates from Wikstrom et al. (2001) and the “bladj” function

in Phylocom (http://phylodiversity.net/phylocom/ ; Webb et al., 2008). We increased the

resolution of the Poaceae and Solonaceae families using family specific phylogenies (Bouchenak-

Khelladi et al., 2010; Särkinen et al., 2013). Finally, we added the crop species next to their

corresponding wild relative species. Node depths were based on the estimated dates of

domestication (Table S1).

We conducted three different PGLS analyses (Grafen, 1989). These PGLS analyses

account for correlations between species trait values due to shared phylogenetic history given a

specific evolutionary model of trait evolution. The first PGLS assumed a star phylogeny where

there is no phylogenetic structure and all species were equally related. The second utilized our

phylogenetic tree (Fig. 1) and correlations were based on a Brownian Motion model of trait

evolution extracted using the corBrownian function in the “ape” package of R (Paradis, 2005). The

third PGLS utilized the same tree but modeled evolution as an ‘Ornstein-Uhlenbeck’ model of

stabilizing selection, performed using the corMartins function in ape. The PGLS analyses were

conducted using the “nlme” (Pinheiro et al., 2011) package in R (R Core Team, 2013). We could

not conduct a PGLS on survival data using a binomial error distribution and instead we used

arcsine square root transformed of mean percent survivorship. We compared the fit of these PGLS

models to that of the LME models for each herbivore performance trait using AIC values. All

models were fit using REML.

S6

Page 7: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Fig. S1 Domestication increased relative growth rate but it did not consistently influence other

plant traits. Values represent the mean difference between log-transformed trait values for crops

and wild relatives. Error bars represent 95% confidence intervals. Positive values imply that

domestication increases trait values. Statistical results of LME analyses (Table S3) are illustrated

above the bars; (*) represents P < 0.05 and (.) represents P < 0.10. “RGR” represents relative

growth rate, “SLA” is specific leaf area, and “LDMC” is leaf dry matter content. Morphological

traits are green whereas chemical traits are in orange. Numbers below bars represent the number of

independent domestication events tested.

S7

Page 8: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Table S1 Summary of crop species and their closely related wild relatives. For each crop - wild relative pair we provided the common

name of the crop and its hypothesized relationship with the wild relative. Although crops are selected for multiple tissues throughout

their cultivation history we identified the main tissue subject to direct artificial selection (Target). Years since first cultivation (Cult.)

and domestication (Dom.) are estimated from the literature (see Reference column). Seed sources included: GRIN (USDA Germplasm

Resource Information Network, www.ars-grin.gov), prseeds (Prairie Garden Seeds, Saskatchewan, Canada, http://prseeds.ca/), OSC

(OSC Seeds, Ontario, Canada, www.oscseeds.com), PRGC (Plant Gene Resources of Canada, Agriculture and Agri-Food Canada,

http://pgrc3.agr.gc.ca/index_e.html), Hendrick (Hendrick Seeds, Ontario, Canada, www.hendrickseeds.com), Richters (Richters Herbs,

Ontario, Canada, www.richters.com), Dianeseeds (Dianeseeds, Utah, U.S.A., www.dianeseeds.com), and TGRC (C.M. Rick Tomato

Genetics Resource Center, California, U.S.A., http://tgrc.ucdavis.edu)

S8

Page 9: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Table S1

Pair Crop and Relation to

Wild Relative

Species Target Target (simple)

*

Cult. (ybp)

Dom. (ybp)

Seed Source Origin Accession or Variety

References

1 Amaranth Amaranthus cruentus

seed; leaf

repro; veg

7000 6000 GRIN Guatemala PI 658727 (Chan & Sun, 1997;

Meyer et al., 2012)

Progenitor Amaranthus hybridus

GRIN Ohio, U.S.A.

PI 603886

2 Quinoa Chenopodium quinoa

seed repro 7000 5000 prseeds Chile Dave #407 (Rana et al., 2010; Meyer et al., 2012)Closely related

wild congenerChenopodium

albumGRIN India PI 658737;

PI 6587383 Beet Beta vulgaris

vulgarisleaf; root

veg 12000 2400 prseeds Canada Detroit Dark Red

(1892)

(Panella & Lewellen,

2007; Meyer et al., 2012)Progenitor Beta vulgaris

maritimaGRIN France PI 540598;

PI 5406014 Onion Allium cepa

ceparoot veg 7000 5200 OSC NA White

Sweet Spanish

(Gurushidze et al., 2007; Meyer et al.,

2012)Progenitor Allium vavilovii GRIN Former Soviet Union

PI 281727

5 Carrot Daucus carota sativa

root veg 4450 1050 OSC Canada Imperator (Bradeen et al., 2002;

Meyer et al., 2012)

Wild conspecific progenitor

Daucus carota carota

GRIN Switzerland Catalogne race delta PI

4788786 Chicory Cichorium

intybusroot; leaf

veg 2000 450 GRIN France PI 651937 (Van Cutsem et al., 2003; Meyer et al.,

2012)Wild

conspecific progenitor

Cichorium intybus

Peter Kotanen, Univ. of Toronto

Ontario, Canada

Wild collected

S9

Page 10: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Pair Crop and Relation to

Wild Relative

Species Target Target (simple)

*

Cult. (ybp)

Dom. (ybp)

Seed Source Origin Accession or Variety

References

7 Lettuce Lactuca sativa leaf veg 7500 4500 OSC Canada Iceburg (de Vries, 1997; Meyer et al., 2012)

Progenitor Lactuca serriola GRIN Israel PI 667819

8 Safflower Carthamus tinctorius inermis

seed repro 4500 3960 Inder Sheoran, Univ. of Toronto

NA WT-5 2006 (Sehgal et al., 2008;

Meyer et al., 2012)Progenitor Carthamus

palaestinusGRIN Israel PI 235663

9 Canola Brassica napus seed repro 7000 3000 OSC Canada NA (Meyer et al., 2012)Wild congener Brassica

tournefortiiGRIN Pakistan PI 426414

10 Radish Raphanus sativus

root veg 5000 4000 OSC Canada Sparkler White Tip

(Yamane et al., 2009;

Meyer et al., 2012)

Progenitor Raphanus raphanistrum

L. Campbell, Ryerson U

USA NA

11 Sweet Potato Ipomoea batatas root veg 10000 4500 GRIN Peru PI 531122 'Jewel'

(Srisuwan et al., 2006;

Meyer et al., 2012)

Progenitor Ipomoea trifida GRIN Mexico PI 618966

12 Cucumber Cucumis sativus fruit repro 10000 3500 OSC Canada Market-more

(Sebastian et al., 2010;

Meyer et al., 2012)

Progenitor Cucumis sativus hardwickii

GRIN and Z. van Herwijner,

R. Zwaan Breeding B.V.

India PI 504564

13 Chickpea Cicer arietinum seed repro 9100 8000 PGRC Canada CN 114662 'CDC Anna'

(Talebi et al., 2009; Meyer et al., 2012)Progenitor Cicer

reticulatumGRIN Turkey PI 593709;

PI 510656; PI 599072

S10

Page 11: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Pair Crop and Relation to

Wild Relative

Species Target Target (simple)

*

Cult. (ybp)

Dom. (ybp)

Seed Source Origin Accession or Variety

References

14 Common Bean

Phaseolus vulgaris

seed repro 8000 8000 OSC Canada Stringless green

(Hancock, 2004; Meyer et al., 2012)Progenitor Phaeolus

vulgaris aborigineus

GRIN Mexico, Peru

PI 535411; PI 535422; PI 535416

15 Pea Pisum sativum seed repro 9000 5000 OSC Canada Green Arrow

(Nasiri et al., 2009; Meyer et al., 2012)Progenitor Pisum sativum

elatiusGRIN Sudan,

Turkey, Israel, Latvia

W6 15044; W6 15010; W6 15008; PI 505059; PI 639959

16 Soybean Glycine max seed repro 5000 4000 OSC Canada Grand Forks

(Li et al., 2010; Meyer et al., 2012)Progenitor Glycine soja Hendrick Russia Identity:

009317 Flax Linum

usitatissimum usitatissimum

seed repro 11200 7500 Richters USA S2700G (Meyer et al., 2012; Zohary et al., 2012)

Progenitor Linum bienne GRIN Portugal PI 650308

19 Barley Hordeum vulgare vulgare

seed repro 12000 10000 prseeds Canada Bere (Badr et al., 2000; Meyer et al., 2012)

Progenitor Hordeum vulgare

spontaneum

GRIN Israel PI 296873 to PI

29688321 Corn Zea mays mays seed repro 10000 9000 OSC Canada Sunnyvee (Matsuoka et

al., 2002; Meyer et al.,

2012)Progenitor Zea mays

parviglumisGRIN Mexico Ames

21798

22 Einkorn Triticum seed repro 12700 10000 GRIN Turkey PI 428155 (Heun et al.,

S11

Page 12: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Pair Crop and Relation to

Wild Relative

Species Target Target (simple)

*

Cult. (ybp)

Dom. (ybp)

Seed Source Origin Accession or Variety

References

Wheat monococcum monococcum

to PI 428164

1997; Zohary et al., 2012)

Progenitor Triticum monococcum aegilopoides

GRIN Turkey PI 654312 to PI

65432623 Foxtail Millet Setaria italica

italicaseed repro 7500 5900 prseeds Canada NA

(Benabdelmouna et al.,

2001; Meyer et al., 2012)

Progenitor Setaria italica viridis

GRIN Russia Ames 21520

25 Oat Avena sativa seed repro 10000 3000 OSC Canada NA (Meyer et al., 2012; Zohary et al., 2012)Progenitor Avena sterilis PGRC NA CN 3653

'Australian 2651'

28 Pearl Millet Pennisetum glaucum glaucum

seed repro 5000 4000 PGRC NA CN 84424 'IDC 423 '

(Oumar et al., 2008;

Meyer et al., 2012)Progenitor Pennisetum

violaceumPGRC NA CN 87824

'S-88-197'

29 Pepper Capsicum annuum annuum

fruit repro 8000 6000 prseeds Canada Yankee Bell (Aguilar-Melendez et

al., 2009; Meyer et al.,

2012)

Progenitor Capsicum annuum

glabriusculum

GRIN Mexico PI 593491

30 Potato Solanum tuberosum

root veg 10000 8000 PGRC Canada Female Norvalley,

Male Atlantic

(Spooner et al., 2005;

Meyer et al., 2012)

Progenitor Solanum candolleanum

GRIN Bolivia PI 498226; PI 498227

S12

Page 13: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Pair Crop and Relation to

Wild Relative

Species Target Target (simple)

*

Cult. (ybp)

Dom. (ybp)

Seed Source Origin Accession or Variety

References

31 Tobacco Nicotiana tabacum

leaf veg 3000 1000 Inder Sheoran, U Toronto

NA Xanthi (Yukawa et al., 2006;

Tushingham et al., 2013)

Progenitor Nicotiana sylvestris

Dianeseeds NA Only the lonely

32 Tomato Solanum lycopersicum

fruit repro NA 1000 OSC Canada Brandywine (Ranc et al., 2008; Meyer et al., 2012)Progenitor Solanum

pimpinellifoliumTGRC LA2533

34 Okra Abelmoschus esculentus

fruit repro NA 3150 GRIN Cote D'Ivore

PI 489794; PI 489854

(Bisht et al., 1997; Meyer et al., 2012)Progenitor Abelmoschus

tuberculatusGRIN India PI 639677;

PI 63967835 Japanese

Barnyard Millet

Echinochloa esculenta

seed repro NA 5000 GRIN China PI 647850 (Hancock, 2004;

Yamaguchi et al., 2005)Progenitor Echinochloa

crus-galliGRIN Afghanista

nPI 211025

36 Indian Barnyard

Millet

Echinochloa frumentacea

seed repro NA 5000 GRIN India PI 183332 (Hancock, 2004;

Yamaguchi et al., 2005)Progenitor Echinochloa

colonaGRIN India PI 647849

NA Information not available

* Simplified groupings for the tissue subject to direct artificial selection “Target (simple)” include: “veg” for vegetative and “repro” for

reproductive tissue.

S13

Page 14: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Table S2 Comparison of the fit of four analytical approaches to test how plant traits impact

herbivore performance. Values represent AIC scores for the full multiple regression models fit

using restricted maximum likelihood. Models include nine plant traits, domestication status, and

the interactions between traits and domestication. Each row compares the fit of a LME, with pair

nested within family as random effects, to those of PGLS models. The first PGLS model was

conducted on a star phylogeny. The other two where conducted on the inferred phylogeny (Fig. 1)

and fit with a Brownian motion model or an Ornstein-Uhlenbeck model of evolution. For

caterpillar survival, we could not conduct PGLS analyses using generalized linear binomial

regression, and instead present results from arcsine square-root transformed mean percent survival.

Lower AIC values suggest better fits of the models to the data.

Herbivore

Response

Mixed

Model

Star

Phylogeny

Species

Phylogeny –

Brownian

Motion

Species

Phylogeny –

Ornstein-

Uhlenbeck

Caterpillar

survival

(GLMER)

123.3 NA NA NA

Caterpillar

survival

(% survival)

85.5 130.3 289.0 128.7

Caterpillar

weight168.6 215.9 383.5 217.7

Number of

aphids218.1 281.4 420.3 266.9

S14

Page 15: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Table S3 Results of LME analyses testing whether domestication consistently drives changes in

morphological and chemical plant traits. Values represent untransformed fixed effects (means and

± 1 standard error in parentheses). Percent change represents the impact of domestication on trait

value (crop – wild) / wild *100%. “Dom” represents the impact of domestication in the analyses

and “Pair” is the random effect of crop-wild groups.

TraitWild

RelativesCrops %

ChangeP-Values

Dom Pair Dom*PairRGR

(log dry g / day)6.86

(6.75 , 6.97)7.1

(6.98 , 7.22) 3.6 0.03 <0.001 0.288

Toughness(g)

99.9(92.4 , 108)

105.1(95.2 , 115.9) 5.1 0.51 <0.001 0.952

Trichomes(per mm2)

1.41(1.12 , 1.73)

1.03(0.67 , 1.45) -27.0 0.17 <0.001 0.701

SLA(mm2 / mg dry)

36.2(34 , 38.5)

37.1(35.3 , 39.1) 2.7 0.67 0.006 0.143

LDMC(mg dry / g wet)

171.5(162.8 , 180.7)

156.8(147.8 , 166.4) -8.6 0.09 <0.001 0.985

Caterpillar tolerance (Proportion of dry

weight lost)

-0.07(-0.10, -0.04)

-0.04(-0.05 , -0.03) -44.5 0.24 0.242 <0.001

Aphid tolerance(Proportion of dry

weight lost)

-0.02(-0.04 , -0.01)

-0.01(-0.02 , 0) -44.7 0.51 0.770 0.056

Total phenolics(mg gallic acid / g dry

tissue)

10.3(9.6 , 10.9)

11.0(9.9 , 12.2) 6.9 0.27 <0.001 0.052

Phenolic oxidation(mg gallic acid / g dry

tissue)

3.02(2.67 , 3.39)

3.16(2.57 , 3.85) 4.9 0.68 <0.001 0.331

% Nitrogen 3.6(3.47 , 3.72)

3.42(3.24 , 3.6) -4.9 0.15 <0.001 0.784

% Carbon 40.4(40.2 , 40.5)

40.3(40 , 40.5) -0.2 0.70 <0.001 0.705

C:N 11.3(11 , 11.7)

11.9(11.3 , 12.5) 5.3 0.12 <0.001 0.623

Phloem sugar(µg/mL)

0.85(0.71 , 1)

1.02(0.84 , 1.22) 19.8 0.26 <0.001 0.636

S15

Page 16: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Table S4 Best fitting multivariate models, Δ AIC <2, explaining variation in three herbivore

performance traits. “AIC weight” represents the relative likelihood of each model compared to all

others (Burnham & Anderson, 2002). “R2m” and “R2

c” represent the marginal and conditional

coefficients of determination, respectively. Plant trait codes include “A” Domestication, “B”

Phloem sugar, “C” % Carbon, “D” % Nitrogen, “E” RGR, “F” Total Phenolics, “G” LDMC, “H”

SLA, “I” Toughness, “J” Trichomes, and the interactions with domestication status including “K”

Dom * Phloem Sugar, “L” Dom * Percent Carbon, “M” Dom * Percent Nitrogen, “N” Dom *

RGR, “O” Dom * Total Phenolics, “P” Dom * SLA, “Q” Dom * Trichomes, and “R” Dom *

LDMC.

Plant traits included Parameters Δ AICAIC

weightR2

m R2c

Caterpillar survival

A+C+E+F+N+O 9 0 0.04 0.39 0.74

A+D+F+G+J+O+Q 10 0.32 0.03 0.43 0.74

A+D+E+F+G+N+O 10 0.39 0.03 0.42 0.75

A+C+D+E+F+N+O 10 0.44 0.03 0.38 0.73

A+D+E+F+N+O 9 0.53 0.03 0.35 0.75

A+D+F+J+O+Q 9 0.64 0.03 0.36 0.72

A+D+F+G+I+J+O+Q 11 0.74 0.03 0.48 0.77

A+D+F+G+M+O 9 0.87 0.02 0.50 0.73

A+D+F+G+J+M+O+Q 11 0.88 0.02 0.46 0.74

A+D+F+J+M+O+Q 10 0.99 0.02 0.40 0.73

A+C+D+F+M+O 9 1.07 0.02 0.46 0.72

A+C+D+I+J+L+Q 10 1.07 0.02 0.55 0.77

A+D+E+F+J+N+O 10 1.16 0.02 0.38 0.75

A+D+F+G+H+J+O+Q 11 1.19 0.02 0.43 0.72

A+D+F+M+O 8 1.2 0.02 0.43 0.72

A+C+E+F+L+N+O 10 1.29 0.02 0.43 0.75

A+D+E+F+G+J+N+O+Q 12 1.4 0.02 0.45 0.76

A+D+F+I+J+O+Q 10 1.41 0.02 0.41 0.74

S16

Page 17: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Plant traits included Parameters Δ AICAIC

weightR2

m R2c

A+D+E+F+G+M+N+O 11 1.43 0.02 0.45 0.75

A+C+D+E+F+M+N+O 11 1.43 0.02 0.41 0.73

A+D+F+G+I+J+M+O+Q 12 1.45 0.02 0.51 0.76

A+D+E+F+G+H+N+O 11 1.47 0.02 0.42 0.74

A+C+E+F+I+N+O 10 1.47 0.02 0.39 0.73

A+C+D+E+F+G+N+O 11 1.47 0.02 0.42 0.74

A+D+E+F+J+N+O+Q 11 1.52 0.02 0.38 0.75

A+B+D+G+H+J+K+P+Q 12 1.54 0.02 0.52 0.82

A+C+D+J+L+Q 9 1.55 0.02 0.50 0.74

A+D+E+F+G+J+O+Q 11 1.57 0.02 0.44 0.76

A+C+I+J+L+Q 9 1.57 0.02 0.51 0.78

A+D+E+F+M+N+O 10 1.6 0.02 0.39 0.75

A+D+F+G+H+M+O 10 1.62 0.02 0.49 0.72

A+C+D+E+F+L+N+O 11 1.64 0.02 0.43 0.74

A+D+E+F+G+I+N+O 11 1.64 0.02 0.45 0.75

A+C+D+F+J+O+Q 10 1.65 0.02 0.38 0.70

A+C+D+F+J+M+O+Q 11 1.66 0.02 0.41 0.71

A+D+F+I+J+M+O+Q 11 1.67 0.02 0.46 0.75

A+C+D+E+I+J+L+Q 11 1.69 0.02 0.56 0.80

A+D+F+J+M+O 9 1.71 0.02 0.47 0.74

A+C+F+I+J+L+Q 10 1.72 0.02 0.55 0.77

A+C+D+E+F+J+N+O 11 1.74 0.02 0.40 0.74

A+C+E+F+J+N+O 10 1.81 0.02 0.39 0.74

A+D+E+F+G+J+N+O 11 1.85 0.02 0.42 0.74

A+D+F+G+I+M+O 10 1.86 0.02 0.54 0.75

A+C+E+F+H+N+O 10 1.87 0.02 0.41 0.74

A+B+D+F+J+M+O+Q 11 1.89 0.01 0.43 0.73

A+B+C+E+F+N+O 10 1.91 0.01 0.39 0.74

A+D+E+F+J+O+Q 10 1.95 0.01 0.37 0.74

S17

Page 18: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Plant traits included Parameters Δ AICAIC

weightR2

m R2c

A+D+E+F+G+I+J+O+Q 12 1.97 0.01 0.49 0.79

A+D+E+F+G+M+O 10 1.98 0.01 0.53 0.76

A+D+E+F+M+O 9 1.99 0.01 0.48 0.76

A+C+E+F+G+N+O 10 1.99 0.01 0.39 0.74

Caterpillar growth

A+D+G+J+Q 9 0.00 0.10 0.27 0.54

A+D+F+G+J+Q 10 0.00 0.10 0.31 0.53

A+D+J+Q 8 0.36 0.08 0.22 0.54

A+D+F+J+Q 9 0.85 0.06 0.25 0.55

A+D+F+G+J+M+Q 11 1.38 0.05 0.33 0.53

A+D+G+J 8 1.44 0.05 0.23 0.51

A+D+G+J+M+Q 10 1.54 0.04 0.28 0.54

A+D+J 7 1.65 0.04 0.19 0.50

A+D+F+G+J+O+Q 11 1.75 0.04 0.31 0.54

A+D+F+G+H+J+Q 11 1.82 0.04 0.31 0.54

A+D+E+G+J+Q 10 1.86 0.04 0.27 0.53

A+D+G+H+J+Q 10 1.87 0.04 0.26 0.54

A+D+E+F+G+J+Q 11 1.87 0.04 0.31 0.53

A+B+D+F+G+J+Q 11 1.90 0.04 0.32 0.54

A+D+F+G+I+J+Q 11 1.90 0.04 0.31 0.55

A+C+D+G+J+Q 10 1.91 0.04 0.28 0.54

A+B+D+G+J+Q 10 1.92 0.04 0.27 0.54

A+D+G+J+P+Q 10 1.92 0.04 0.27 0.54

A+D+J+M+Q 9 1.95 0.04 0.22 0.54

A+D+G+I+J+Q 10 2.00 0.04 0.27 0.54

A+C+D+F+G+J+Q 11 2.00 0.04 0.31 0.53

Aphids

F+J 6 0.00 0.03 0.17 0.89

S18

Page 19: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Plant traits included Parameters Δ AICAIC

weightR2

m R2c

A+C+G+H+J+L+P+Q+R 13 0.27 0.03 0.15 0.95

F+H+J 7 0.33 0.03 0.20 0.89

A+C+F+G+H+J+L+P+Q+R 14 0.33 0.03 0.20 0.94

C+F+J 7 0.54 0.02 0.17 0.91

A+C+G+H+J+L+P+R 12 0.57 0.02 0.15 0.94

A+C+E+G+H+J+L+P+Q+R 14 0.60 0.02 0.16 0.94

A+C+E+G+H+J+L+P+R 13 0.69 0.02 0.16 0.94

D+F+H+J 8 0.69 0.02 0.21 0.90

A+C+E+F+G+H+J+L+P+Q+R 15 0.85 0.02 0.21 0.94

A+C+F+G+H+J+L+P+R 13 0.85 0.02 0.20 0.94

A+C+E+G+H+J+L+N+P+R 14 0.95 0.02 0.17 0.95

C+F+H+J 8 0.96 0.02 0.19 0.91

A+C+G+H+J+P+R 11 0.99 0.02 0.14 0.94

F+G+H+J 8 0.99 0.02 0.20 0.90

A+C+E+G+H+J+L+N+P+Q+R 15 1.05 0.02 0.17 0.95

C+J 6 1.10 0.02 0.11 0.91

A+C+E+F+G+H+J+L+P+R 14 1.15 0.02 0.21 0.93

D+F+J 7 1.15 0.02 0.18 0.89

A+C+E+F+G+H+J+L+N+P+Q+R 16 1.29 0.02 0.22 0.95

A+C+G+H+I+J+L+P+Q+R 14 1.30 0.02 0.16 0.95

F+H+I+J 8 1.32 0.02 0.22 0.90

C+F+G+H+J 9 1.35 0.02 0.18 0.91

A+C+D+G+H+J+L+P+Q+R 14 1.36 0.02 0.15 0.95

A+C+G+H+J+R 10 1.36 0.02 0.15 0.93

A+C+E+G+H+J+P+R 12 1.37 0.02 0.15 0.93

A+C+G+H+I+J+P+R 12 1.38 0.02 0.16 0.94

A+C+E+F+G+H+J+L+N+P+R 15 1.38 0.02 0.21 0.95

A+C+F+G+H+J+P+R 12 1.43 0.02 0.19 0.93

A+B+C+G+H+J+K+L+P+Q+R 15 1.43 0.02 0.16 0.95

S19

Page 20: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Plant traits included Parameters Δ AICAIC

weightR2

m R2c

A+C+E+G+H+J+N+P+R 13 1.43 0.02 0.16 0.95

E+F+J 7 1.53 0.01 0.18 0.89

A+B+C+F+G+H+J+L+P+Q+R 15 1.59 0.01 0.20 0.94

B+F+J 7 1.64 0.01 0.17 0.90

A+C+D+G+H+I+J+L+P+Q+R 15 1.68 0.01 0.16 0.95

A+C+F+G+H+J+R 11 1.70 0.01 0.21 0.93

A+B+C+G+H+J+L+P+Q+R 14 1.70 0.01 0.15 0.95

A+C+G+H+I+J+R 11 1.73 0.01 0.17 0.94

D+E+F+H+J 9 1.73 0.01 0.22 0.89

A+C+D+G+H+J+L+P+R 13 1.74 0.01 0.15 0.95

A+B+C+F+G+H+J+K+L+P+Q+R 16 1.74 0.01 0.20 0.95

E+F+H+J 8 1.77 0.01 0.20 0.89

F+G+H+I+J 9 1.80 0.01 0.22 0.91

A+F+J 7 1.83 0.01 0.18 0.89

C+F+H+I+J 9 1.85 0.01 0.20 0.92

A+B+C+G+H+J+K+P+R 13 1.86 0.01 0.16 0.94

A+C+G+H+I+J+P+Q+R 13 1.89 0.01 0.17 0.94

A+C+D+E+G+H+J+L+N+P+R 15 1.90 0.01 0.17 0.96

A+C+E+G+H+I+J+L+P+Q+R 15 1.91 0.01 0.17 0.95

A+C+F+G+H+I+J+L+P+Q+R 15 1.91 0.01 0.21 0.94

A+C+G+H+I+J+L+P+R 13 1.92 0.01 0.16 0.94

B+F+H+J 8 1.93 0.01 0.19 0.90

A+C+D+E+G+H+J+L+N+P+Q+R 16 1.93 0.01 0.17 0.96

A+C+E+F+G+H+J+P+R 13 1.94 0.01 0.20 0.93

A+C+F+G+H+J+L+O+P+R 14 1.95 0.01 0.22 0.94

A+B+C+G+H+J+K+R 12 1.95 0.01 0.17 0.94

C+H+J 7 1.96 0.01 0.11 0.91

F+I+J 7 1.98 0.01 0.17 0.89

A+C+E+F+G+H+J+N+P+R 14 1.98 0.01 0.21 0.94

S20

Page 21: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Plant traits included Parameters Δ AICAIC

weightR2

m R2c

A+C+D+F+G+H+J+L+P+Q+R 15 1.99 0.01 0.19 0.94

F+G+J 7 2.00 0.01 0.17 0.89

References for Supporting InformationAguilar-Melendez A, Morrell PL, Roose ML, Kim S-C. 2009. Genetic diversity and structure in

semiwild and domesticated chiles (Capsicum annuum; Solanaceae) from Mexico. American

Journal of Botany 96(6): 1190-1202.

Badr A, Muller K, Schafer-Pregl R, El Rabey H, Effgen S, Ibrahim HH, Pozzi C, Rohde W,

Salamini F. 2000. On the origin and domestication history of barley (Hordeum vulgare).

Molecular Biology and Evolution 17(4): 499-510.

Benabdelmouna A, Abirached-Darmency M, Darmency H. 2001. Phylogenetic and genomic

relationships in Setaria italica and its close relatives based on the molecular diversity and

chromosomal organization of 5S and 18S-5.8S-25S rDNA genes. Theoretical and Applied

Genetics 103(5): 668-677.

Bisht IS, Patel DP, Mahajan RK. 1997. Classification of genetic diversity in Abelmoschus

tuberculatus germplasm collection using morphometric data. Annals of Applied Biology 130(2):

325-335.

Bouchenak-Khelladi Y, Verboom GA, Savolainen V, Hodkinson TR. 2010. Biogeography of

the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical

space and geological time. Botanical Journal of the Linnean Society 162(4): 543-557.

Bradeen JM, Bach IC, Briard M, Le Clerc V, Grzebelus D, Senalik DA, Simon PW. 2002.

Molecular diversity analysis of cultivated carrot (Daucus carota L.) and wild Daucus populations

reveals a genetically nonstructured composition. Journal of the American Society for Horticultural

Science 127(3): 383-391.

Burnham KP, Anderson DR. 2002. Model selection and multimodel inference: a practical

information-theoretic approach. New York: Springer-Verlag.

S21

Page 22: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Chan KF, Sun M. 1997. Genetic diversity and relationships detected by isozyme and RAPD

analysis of crop and wild species of Amaranthus. Theoretical and Applied Genetics 95(5-6): 865-

873.

de Vries IM. 1997. Origin and domestication of Lactuca sativa L. Genetic Resources and Crop

Evolution 44(2): 165-174.

Grafen A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society of

London Series B-Biological Sciences 326(1233): 119-157.

Gurushidze M, Mashayekhi S, Blattner FR, Friesen N, Fritsch RM. 2007. Phylogenetic

relationships of wild and cultivated species of Allium section Cepa inferred by nuclear rDNA ITS

sequence analysis. Plant Systematics and Evolution 269(3-4): 259-269.

Hancock JF. 2004. Plant Evolution and the Origin of Crop Species. Oxford: Oxford University

Press.

Heun M, Schaferpregl R, Klawan D, Castagna R, Accerbi M, Borghi B, Salamini F. 1997.

Site of einkorn wheat domestication identified by DNA fingerprinting. Science 278(5341): 1312-

1314.

Li Y-H, Li W, Zhang C, Yang L, Chang R-Z, Gaut BS, Qiu L-J. 2010. Genetic diversity in

domesticated soybean (Glycine max) and its wild progenitor (Glycine soja) for simple sequence

repeat and single-nucleotide polymorphism loci. New Phytologist 188(1): 242-253.

Matsuoka Y, Vigouroux Y, Goodman MM, G.J. S, Buckler E, Doebley J. 2002. A single

domestication for maize shown by multilocus microsatellite genotyping. Proceedings of the

National Academy of Sciences of the United States of America 99(9): 6080-6084.

Meyer RS, DuVal AE, Jensen HR. 2012. Patterns and processes in crop domestication: an

historical review and quantitative analysis of 203 global food crops. New Phytologist 196(1): 29-

48.

Nasiri J, Haghnazari A, Saba J. 2009. Genetic diversity among varieties and wild species

accessions of pea (Pisum sativum L.) based on SSR markers. African Journal of Biotechnology

8(15): 3405-3417.

Oumar I, Mariac C, Pham J-L, Vigouroux Y. 2008. Phylogeny and origin of pearl millet

(Pennisetum glaucum [L.] R. Br) as revealed by microsatellite loci. Theoretical and Applied

Genetics 117(4): 489-497.

Panella L, Lewellen RT. 2007. Broadening the genetic base of sugar beet: introgression from

wild relatives. Euphytica 154(3): 383-400.

S22

Page 23: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Paradis E. 2005. Statistical analysis of diversification with species traits. Evolution 59(1): 1-12.

Pinheiro JC, Bates DM, DebRoy S, Sarkar D, R Development Core Team 2011. nlme: Linear

and nonlinear mixed effects models.

R Core Team 2013. R: a language and environment for statistical computing. Vienna, Austria: R

Foundation for Statistical Computing.

Rana TS, Narzary D, Ohri D. 2010. Genetic diversity and relationships among some wild and

cultivated species of Chenopodium L. (Amaranthaceae) using RAPD and DAMD methods.

Current Science 98(6): 840-846.

Ranc N, Muños S, Santoni S, Causse M. 2008. A clarified position for Solanum lycopersicum

var. cerasiforme in the evolutionary history of tomatoes (solanaceae). BMC Plant Biology 8: 130.

Salminen J-P, Karonen M. 2011. Chemical ecology of tannins and other phenolics: we need a

change in approach. Functional Ecology 25(2): 325-338.

Särkinen T, Bohs L, Olmstead RG, Knapp S. 2013. A phylogenetic framework for evolutionary

study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology 13(1):

214.

Sebastian P, Schaefer H, Telford IRH, Renner SS. 2010. Cucumber (Cucumis sativus) and

melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of

melon is from Australia. Proceedings of the National Academy of Sciences of the United States of

America 107(32): 14269-14273.

Sehgal D, Rajpal VR, Raina SN. 2008. Chloroplast DNA diversity reveals the contribution of

two wild species to the origin and evolution of diploid safflower (Carthamus tinctorius L.).

Genome 51(8): 638-643.

Spooner DM, McLean K, Ramsay G, Waugh R, Bryan GJ. 2005. A single domestication for

potato based on multilocus amplified fragment length polymorphism genotyping. Proceedings of

the National Academy of Sciences of the United States of America 102(41): 14694-14699.

Srisuwan S, Sihachakr D, Siljak-Yakovlev S. 2006. The origin and evolution of sweet potato

(Ipomoea batatas Lam.) and its wild relatives through the cytogenetic approaches. Plant Science

171(3): 424-433.

Talebi R, Jelodar N-AB, Mardi M, Fayaz F, Furman BJ, Bagheri N-A. 2009. Phylogenetic

diversity and relationship among annual Cicer species using random amplified polymorphic DNA

markers. General and Applied Plant Physiology 35(1-2): 03-12.

S23

Page 24: €¦ · Web viewNew Phytologist Supporting Information . The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events . …

Supporting Information | Turcotte et al.

Tushingham S, Ardura D, Eerkens JW, Palazoglu M, Shahbaz S, Fiehn O. 2013. Hunter-

gatherer tobacco smoking: earliest evidence from the Pacific Northwest Coast of North America.

Journal of Archaeological Science 40(2): 1397-1407.

Van Cutsem P, Du Jardin P, Boutte C, Beauwens T, Jacqmin S, Vekemans X. 2003.

Distinction between cultivated and wild chicory gene pools using AFLP markers. Theoretical and

Applied Genetics 107(4): 713-718.

Webb CO, Ackerly DD, Kembel SW. 2008. Phylocom: software for the analysis of phylogenetic

community structure and trait evolution. Bioinformatics 24(18): 2098-2100.

Webb CO, Donoghue MJ. 2005. Phylomatic: tree assembly for applied phylogenetics. Molecular

Ecology Notes 5: 181-183.

Wikstrom N, Savolainen V, Chase MW. 2001. Evolution of the angiosperms: calibrating the

family tree. Proceedings of the Royal Society B 268(1482): 2211-2220.

Wilkinson TL, Douglas AE. 2003. Phloem amino acids and the host plant range of the

polyphagous aphid, Aphis fabae. Entomologia Experimentalis et Applicata 106(2): 103-113.

Yamaguchi H, Utano A, Yasuda K, Yano A, Soejima A. 2005. A molecular phylogeny of wild

and cultivated Echinochloa in East Asia inferred from non-coding region sequences of trnT-L-F.

Weed Biology and Management 5(4): 210-218.

Yamane K, Lue N, Ohnishi O. 2009. Multiple origins and high genetic diversity of cultivated

radish inferred from polymorphism in chloroplast simple sequence repeats. Breeding Science

59(1): 55-65.

Yukawa M, Tsudzuki T, Sugiura M. 2006. The chloroplast genome of Nicotiana sylvestris and

Nicotiana tomentosiformis: complete sequencing confirms that the Nicotiana sylvestris progenitor

is the maternal genome donor of Nicotiana tabacum. Molecular Genetics and Genomics 275(4):

367-373.

Zohary D, Hopf M, Weiss E. 2012. Domestication of Plants in the Old World. Oxford: Oxford

University Press.

S24