A review of the Ustilago-Sporisorium-Macalpinomyces complex
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© 2012 Nationaal Herbarium Nederland & Centraalbureau voor Schimmelcultures You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. Persoonia 29, 2012: 55 – 62 www.ingentaconnect.com/content/nhn/pimj http://dx.doi.org/10.3767/003158512X660283 REVIEW ARTICLE INTRODUCTION Three genera of smut fungi (Ustilaginomycotina), Ustilago, Sporisorium and Macalpinomyces, contain about 540 described species (Vánky 2011b). These three genera belong to the family Ustilaginaceae, which mostly infect grasses (Begerow et al. 2006) and have teliospores that germinate to produce phragmobasidia (Bauer et al. 2001, Begerow et al. 2006). Ustilago and Sporisorium were shown to form a monophyletic group within the Ustilaginaceae after molecular phylogenetic analyses (Begerow et al. 1997, 2006, Stoll et al. 2003, 2005). The systematic position of Macalpinomyces is ambiguous within the Ustilaginales (Begerow et al. 2006). Many taxa within Ustilago, Sporisorium and Macalpinomyces share two or more morphological characters indicative of the different genera. This makes taxonomic placement of species within genera problematic. The original characters used to identify genera were not sufficiently robust to encompass the full morphological diversity of novel species that have since been discovered. Taxa within Ustilago, Sporisorium and Macalpino- myces are part of a systematically unresolved complex (Vánky 2002a, Stoll et al. 2003, 2005, Piepenbring 2004, Vánky et al. 2006, Vánky & Shivas 2008). Three further genera, Anomalo- myces, Melanopsichium and Tubisorus, are considered to be distinct, well-defined members of this complex. Attempts to reconcile the taxonomy of this complex using either morphology (Vánky 1991, Piepenbring et al. 1998) or molecular phylogenetics (Stoll et al. 2003, 2005) have been unsuccessful. This paper reviews chronologically changing generic concepts in the Ustilago-Sporisorium-Macalpinomyces complex and presents an approach for resolving systematic anomalies. TAXONOMIC HISTORY Ustilago Ustilago, derived from the Latin ustilare (to burn), was named by Persoon (1801) for the blackened appearance of the inflores- cence in infected plants, as seen in the type species U. hordei. According to Clinton (1906), Persoon adopted the name Usti- lago from Johann Bauhin’s 1651 edition of ‘Historia plantarum universalis’. Persoon (1801) created Ustilago as a subgenus of Uredo in his ‘Synopsis Methodica Fungorum’. He described Uredo, now classified within the rust subphylum Pucciniomyco- tina (Aime et al. 2006), as lacking a peridium and having spores that were powdery, loose, uniform and mostly globose. Ustilago, now classified in the smut subphylum Ustilaginomycotina, was separated from Uredo by possessing black to brown powdery spores that parasitize mostly plant inflorescences. Ustilago was promoted to the level of genus by Roussel (1806). Ustilago be- came a catch-all genus for a diversity of smut fungi. Many taxa currently regarded as belonging to Ahmadiago, Antherospora, Anthracoidea, Aurantiosporium, Bambusiomyces, Bauerago, Cintractia, Eriocaulago, Exoteliospora, Farysia, Farysporium, Liroa, Macalpinomyces, Melanopsichium, Microbotryum, Par- vulago, Pericladium, Schizonella, Sporisorium, Thecaphora, Tilletia, Tranzscheliella, Ustanciosporium, Vankya, Websdanea and Yelsemia were originally described as members of Ustilago (e.g. Piepenbring et al. 1996, Vánky 1998a, 1999a, b, 2002a, b, 2003b, 2004b, 2011a, b, Bauer et al. 1999, 2007, 2008, Piepen- bring 2000, Vánky et al. 2008). Juliohirschhornia was proposed for its pattern of spore germi- nation, which was considered to be intermediate to the Usti- laginaceae and Tilletiaceae (Hirschhorn 1986). Vánky (2002a) noted that Juliohirschhornia was an invalid genus and further considered its spore germination represented only a variant of the Ustilago-type. Several other genera were regarded by Vánky (2002a) as synonymous with Ustilago, including Crozal- siella, Necrosis, Pericoelium and Ustilagidium. Two attempts have been made to subdivide Ustilago, although the proposed classifications have not been widely accepted. Firstly, Brefeld (1912) proposed the genus Mycosarcoma for Ustilago maydis. Brefeld (1912) based Mycosarcoma on the A review of the Ustilago-Sporisorium-Macalpinomyces complex A.R. McTaggart 1,2,3,5 , R.G. Shivas 1,2 , A.D.W. Geering 1,2,5 , K. Vánky 4 , T. Scharaschkin 1,3 1 Cooperative Research Centre for National Plant Biosecurity, GPO Box 5012, Bruce, ACT 2617, Australia; corresponding author e-mail: [email protected]. 2 Department of Agriculture, Fisheries and Forestry, Ecosciences Precinct, GPO Box 267, Brisbane, Queensland 4001, Australia. 3 EEBS, Faculty of Science and Technology, Queensland University of Technology, 2 George Street, Brisbane, Queensland 4001, Australia. 4 Herbarium Ustilaginales Vánky (HUV), Gabriel-Biel-Str. 5, D-72076 Tübin- gen, Germany. 5 Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, Ecosciences Precinct, GPO Box 267, Brisbane, Queensland 4001, Australia. Key words smut fungi systematics Ustilaginaceae Abstract The fungal genera Ustilago, Sporisorium and Macalpinomyces represent an unresolved complex. Taxa within the complex often possess characters that occur in more than one genus, creating uncertainty for species placement. Previous studies have indicated that the genera cannot be separated based on morphology alone. Here we chronologically review the history of the Ustilago-Sporisorium-Macalpinomyces complex, argue for its resolution and suggest methods to accomplish a stable taxonomy. A combined molecular and morphological ap- proach is required to identify synapomorphic characters that underpin a new classification. Ustilago, Sporisorium and Macalpinomyces require explicit re-description and new genera, based on monophyletic groups, are needed to accommodate taxa that no longer fit the emended descriptions. A resolved classification will end the taxonomic confusion that surrounds generic placement of these smut fungi. Article info Received: 18 May 2012; Accepted: 3 October 2012; Published: 27 November 2012.
Transcript of A review of the Ustilago-Sporisorium-Macalpinomyces complex
© 2012 Nationaal Herbarium Nederland & Centraalbureau voor Schimmelcultures
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Persoonia 29, 2012: 55–62www.ingentaconnect.com/content/nhn/pimj http://dx.doi.org/10.3767/003158512X660283REVIEW ARTICLE
INTRODUCTION
Three genera of smut fungi (Ustilaginomycotina),Ustilago, Spo ri sorium and Macalpinomyces, contain about 540 described species (Vánky 2011b).These three genera belong to the family Ustilaginaceae,whichmostlyinfectgrasses(Begerowetal.2006)andhaveteliospores thatgerminate toproducephragmobasidia (Bauer et al. 2001,Begerow et al. 2006).Ustilago and Sporisorium were shown to form a monophyletic group within the Ustilaginaceae after molecular phylogenetic analyses(Begerowetal.1997,2006,Stolletal.2003,2005).The systematic position of Macalpinomyces is ambiguous within the Ustilaginales(Begerowetal.2006).Many taxa within Ustilago, Sporisorium and Macalpinomyces share two or more morphological characters indicative of the differentgenera.Thismakestaxonomicplacementofspecieswithin genera problematic.The original characters used toidentifygenerawerenotsufficientlyrobusttoencompassthefullmorphological diversity of novel species that have since been discovered.TaxawithinUstilago, Sporisorium and Macalpino-myces arepartofasystematicallyunresolvedcomplex(Vánky2002a,Stolletal.2003,2005,Piepenbring2004,Vánkyetal.2006,Vánky&Shivas2008).Threefurthergenera,Anomalo-myces, Melanopsichium and Tubisorus, are considered to be distinct,well-definedmembersofthiscomplex.Attempts to reconcile the taxonomy of this complex using either morphology(Vánky1991,Piepenbringetal.1998)ormolecularphylogenetics(Stolletal.2003,2005)havebeenunsuccessful.This paper reviews chronologically changing generic concepts in the Ustilago-Sporisorium-Macalpinomyces complex and presentsanapproachforresolvingsystematicanomalies.
TAXONOMIC HISTORY
UstilagoUstilago, derived from the Latin ustilare(toburn), was named byPersoon(1801)fortheblackenedappearanceoftheinflores-cence in infected plants, as seen in the type species U. hordei.AccordingtoClinton(1906),PersoonadoptedthenameUsti-lagofromJohannBauhin’s1651editionof‘Historiaplantarumuniversalis’.Persoon(1801)createdUstilago as a subgenus of Uredo inhis‘SynopsisMethodicaFungorum’.HedescribedUredo,nowclassifiedwithintherustsubphylumPucciniomyco-tina (Aimeetal.2006), as lacking a peridium and having spores thatwerepowdery,loose,uniformandmostlyglobose.Ustilago, nowclassifiedinthesmutsubphylumUstilaginomycotina, was separated from Uredo by possessing black to brown powdery sporesthatparasitizemostlyplantinflorescences.Ustilago was promotedtothelevelofgenusbyRoussel(1806).Ustilago be-cameacatch-allgenusforadiversityofsmutfungi.Manytaxacurrently regarded as belonging to Ahmadiago, Antherospora, Anthracoidea, Aurantiosporium, Bambusiomyces, Bauerago, Cintractia, Eriocaulago, Exoteliospora, Farysia, Farysporium, Liroa, Macalpinomyces, Melanopsichium, Microbotryum, Par-vulago, Pericladium, Schizonella, Sporisorium, Thecaphora, Tilletia, Tranzscheliella, Ustanciosporium, Vankya, Websdanea and Yelsemia were originally described as members of Ustilago (e.g.Piepenbringetal.1996,Vánky1998a,1999a,b,2002a,b, 2003b,2004b,2011a,b,Baueretal.1999,2007,2008,Piepen-bring2000,Vánkyetal.2008).Juliohirschhornia was proposed for its pattern of spore germi-nation, which was considered to be intermediate to the Usti-laginaceae and Tilletiaceae(Hirschhorn1986).Vánky(2002a)noted that Juliohirschhornia was an invalid genus and further considered its spore germination represented only a variant of the Ustilago-type.SeveralothergenerawereregardedbyVánky(2002a)assynonymouswithUstilago, including Crozal-siella, Necrosis, Pericoelium and Ustilagidium.Two attempts have been made to subdivide Ustilago, although theproposedclassificationshavenotbeenwidelyaccepted.Firstly,Brefeld(1912)proposedthegenusMycosarcoma for Ustilago maydis. Brefeld(1912)basedMycosarcoma on the
A review of the Ustilago-Sporisorium-Macalpinomyces complexA.R.McTaggart1,2,3,5,R.G.Shivas1,2,A.D.W.Geering1,2,5,K.Vánky4,T.Scharaschkin1,3
1 CooperativeResearchCentre forNationalPlantBiosecurity,GPOBox5012,Bruce,ACT2617,Australia;
correspondingauthore-mail:[email protected] DepartmentofAgriculture,FisheriesandForestry,EcosciencesPrecinct,GPOBox267,Brisbane,Queensland4001,Australia.
3 EEBS, Faculty of Science andTechnology,QueenslandUniversity ofTechnology,2GeorgeStreet,Brisbane,Queensland4001,Australia.
4 HerbariumUstilaginalesVánky(HUV),Gabriel-Biel-Str.5,D-72076Tübin-gen,Germany.
5 QueenslandAllianceforAgricultureandFoodInnovation,TheUniversityofQueensland,EcosciencesPrecinct,GPOBox267,Brisbane,Queensland4001,Australia.
Key words
smut fungisystematicsUstilaginaceae
Abstract The fungal genera Ustilago, Sporisorium and Macalpinomycesrepresentanunresolvedcomplex.Taxawithin the complex often possess characters that occur in more than one genus, creating uncertainty for species placement.Previousstudieshave indicated that thegeneracannotbeseparatedbasedonmorphologyalone. Here we chronologically review the history of the Ustilago-Sporisorium-Macalpinomyces complex, argue for its resolutionandsuggestmethodstoaccomplishastabletaxonomy.Acombinedmolecularandmorphologicalap-proachisrequiredtoidentifysynapomorphiccharactersthatunderpinanewclassification.Ustilago, Sporisorium and Macalpinomyces require explicit re-description and new genera, based on monophyletic groups, are needed toaccommodatetaxathatnolongerfittheemendeddescriptions.Aresolvedclassificationwillendthetaxonomicconfusionthatsurroundsgenericplacementofthesesmutfungi.
Article info Received:18May2012;Accepted:3October2012;Published:27November2012.
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structure of the peridium, incubation time in the host, localized infectionanddevelopmentofaerialconidia.Genericplacementof U. maydis withinthecomplexiscontentious(Piepenbringetal.2002,Stolletal.2005)anduntil the complex is resolved, this taxon is best left within Ustilago because of its importance asamodelplantpathogen.Another attempt to subdivide Ustilago was made in 1949 by the mycologist Tchen Ngo Liou, who considered that the basidia of U. esculenta differed from the type species of Ustilago(citedinPiepenbringetal.2002).LiouerectedthegenusYenia, with Y. esculenta as the type, and transferred seven additional Us-tilago speciesintothenewgenus(Liou1949).Vánky(2002a)considered that the eight taxa Liou selected were very different in biology, soral structure, spore morphology and germination patterns,anddidnotconstituteanaturalgroup.Piepenbring et al. (2002)intheirsingle-locusphylogeneticanalysisfoundthatU. esculenta was sister to 21 species of Ustilago and Sporiso-rium, accepting that U. esculenta belonged in a separate genus to Ustilago.Stolletal. (2005)didnotsupporttheseparationofU. esculenta from Ustilago on the basis of a molecular phylo-geneticanalysis,which included thisand97otherUstilago, Sporisorium and Macalpinomyces species. Beck(1894)introducedthegenusMelanopsichium for a taxon firstdescribedasUstilago austro-americanum on Polygonum.The genus was characterised by compact, hard, irregularly lobedgallsintheinflorescence,stemsandleaves(Halisky&Barbe1962,Vánky2002a).Weissetal.(2004),Begerowetal. (2004)andStolletal. (2005)concludedthatMelanopsichium representedanexampleofahostjumpfromPoaceae to Poly-gonaceae, as M. pennsylvanicum belonged to the Ustilago clade.Begerowetal. (2006)consequentlyrejectedthefamilyMelanopsichiaceae proposedbyVánky(2001a).
Langdon&Fullerton(1975)studiedthesoralontogenyofsixUstilago species.Their revisedconceptofUstilago included taxa that colonised host plants with hyphae that destroyed parenchymatous tissue to then become spores, without forming fungalperidia,columellae,sterilecellsorsporeballs.The gross morphology of Ustilago isvariable(Fig.1).Piepen-bring(2004)recorded14differentsoralmorphologiesforUsti-lago in her treatise of the sori found in the Ustilaginomycotina.Some taxa, such as U. sparsa and U. trichophora, occurred as localised galls on the host plant, inducing hypertrophied ovaries ratherthandestroyingtheentireinflorescence.Ustilago altilis and U. esculenta infected the culms of the host, and some species occurred in the leaves, for example U. calamagrostidis and U. striiformis.Vánky(2002a)consideredUstilago as oc-curring solely on hosts in the Poaceae,accepting174species(Vánky2011b).
Sporisorium Ehrenberg described Sporisorium in a letter to Link, based on a collection he had made of S. sorghi on the cultivated grass Sor-ghum in the Poaceae(Link1825).Sporisorium was described as unique because it possessed columellae of equal length as the glumes, formed agglutinated spores and mutilated floral parts.Sporisorium also had sterile partitioning cells in groups or chainsandaperidium(Link1825,Langdon&Fullerton1978).Four years after the description of Sporisorium,Rudolphi(1829)described the confusingly named Sorosporium from Saponaria officinalis in the Caryophyllaceae.Manyauthorssubsequentlychose Sorosporium for smut taxa with peridia and spore balls includingthosethatinfectedgrasses(Poaceae).Sporisorium was overlooked for about 150 years until Langdon & Fullerton (1978)re-establishedthename.Manyofthespeciesdescribed
Fig. 1DiversityofsoralmorphologyinUstilago.a.Ustilago spinificis on Spinifex longifolius;b.Ustilago xerochloae on Xerochloa barbata;c.Ustilago drak-ensbergiana on Digitaria tricholaenoides; d.Ustilago tritici on Triticum aestivum;e.Ustilago bouriquetii on Stenotaphrum dimidatum;f.Ustilago altilis on Triodia sp.;g.Ustilago phragmitis on Phragmites karka;h.Ustilago cynodontis on Cynodon dactylon.
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in Sorosporium and UstilagohavesincebeenreclassifiedinSporisorium.More precisely,Sporisorium contains at least 60taxaoriginallyclassifiedasUstilago,andabout170taxadescribed as Sorosporium(Robertetal.2005).Sorokin described Endothlaspis in1890fortwosmuts,onSor-ghum and Melica, of which the respective types have been lost (citedinLangdon&Fullerton1978,Vánky2002a).Langdon&Fullerton(1978)believedthedescriptionandillustrationsofEndothlaspis werevagueandpoorlyexecuted.Vánky(2002a)considered that Endothlaspis was a synonym of Sporisorium andthatthetypespecieswasbasedonahostmisidentification.Lavrov(1936)andCiferri(1938)dividedSorosporium into two subgenera depending on whether they infected hosts in Poa-ceae or Caryophyllaceae(citedinVánky2002a).Langdon&Fullerton(1975) noted that Sorosporium species on Poaceae
differed in soral ontogeny and structure to species on Caryo-phyllaceae, essentially in that Sorosporium on Caryophyllaceae lackedawell-definedsorus.Langdon&Fullerton(1975)sug-gested that smuts on Poaceae should be grouped in a separate genus,butdidnotmakeanytaxonomicrevisionsatthatstage.Vánky(1998b)consideredSorosporium to be a synonym of Thecaphora after an examination of the types of both genera revealedno essentialmorphological differences.This deci-sion was subsequently supported by molecular phylogenetic analyses(Vánkyetal.2008).SphacelothecawasestablishedbydeBary(1884)forSph. hy-dropiperis on Polygonum.Sphacelothecawasdefinedashavinga membrane or peridium enclosing the spores and a columella (citedinLangdon&Fullerton1978).Clinton(1902)transferred10 taxa from Ustilago to Sphacelotheca, including Sporisorium
Fig. 2DiversityofsoralmorphologyinSporisorium.a.S. cenchri-elymoidis on Cenchrus elymoidis;b.S. cryptum on Yakirra sp.;c.S. heteropogonicola on Heteropogon contortus;d.S. bothriochloae on Dichanthium sericeum;e.S. tumefaciens on Chrysopogon sp.; f.S. iseilematis-ciliati on Iseilema sp.; g.S. themedae on Themeda triandra;h.S. aristidicola on Aristida sp.;i.S. likhitekerajae on Ischaemum sp.;j.S. doidgeae on Capillipedium parviflorum; k.S. sacchari on Saccharumsp.;l.Ustilago scitaminea on Saccharum officinarum;m.Sporisorium caledonicum on Heteropogon contortus;n.S. ischaemum on Ischaemum indicum;o.S. holwayi on Andropogon bicornis.
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sorghi, which he referred to as Ustilago sorghi.Clintondidnot mention Sporisorium, but he attributed the authorship of U. sorghi to Link, indicating that he was aware of Sporisorium asanearlierdescribedgenus.Asidefromabriefmentionofthe characters of Sphacelotheca, Clinton gave no reason why the 10 taxa would be better suited to Sphacelotheca.Clinton’stransferral of taxa in Sporisorium to Sphacelotheca sensu Clinton was precedent for over 110 subsequent descriptions of species of Sphacelotheca ongrasses(Robertetal.2005).Langdon&Fullerton(1978)ascertainedthatthecolumellaeinSphacelotheca species on Polygonaceae and Poaceae were nothomologous.Sphacelotheca formed a columella from fungal cells adhering to one another on hosts in the Polygonaceae, whereas columellae were derived from host material in the Poaceae.Langdon&Fullerton(1978)alsonoteddifferencesinthe peridium and the development of the spore mass between Sphacelotheca in the Polygonaceae and Poaceae.Spha-celotheca occurred only on hosts in the Polygonaceae and has beenshownbyBaueretal.(1997)tobelongtotheMicrobotry-ales in the Pucciniomycotina.Thissystematicplacementwasconfirmedbymolecularanalyses(Weissetal.2004,Kemleretal.2006).Langdon&Fullerton(1978)resurrectedSporisorium after show-ing that Sphacelotheca and Sorosporium were not suitable generaforsmutfungiongrasses.Theydesignatedanewtypespecimen of Sporisorium sorghi from an Australian collection on Sorghum leiocladum,whichVánky(1990)believedtorepresentS. cruentum.Vánky(1990)proposedanewneotypefromanEgyptiancollectionofS. sorghi.TheneotypeoriginallyproposedbyLangdon&Fullerton(1978)appearedtobelongtoadistinctspecies, S. australasiaticum (Vánky&Shivas2001).
Langdon&Fullerton(1978)outlinedthecharacteristicsofSpori-sorium based on their neotype of Sporisorium sorghi.Charactersofimportanceincludeda‘hyphalperidium,columellacomposedof host tissues and hyphae, and spores intermixed with partition-ing(sterile)cells’.ThesecharactersarevariableamongotherSporisorium species(Fig.2).The morphological variation of peridia, columellae, sterile cells and dimorphic spores in Sporisorium has led to different inter-pretationsbymycologists.Forexample,Langdon&Fullerton(1975)describedthepresenceofacolumellainSporisorium consanguineum, but itwas later reported absent byVánky&Shivas(2008).AcolumellawasnotdescribedbyLangdon(1962) inUstilago porosa, but this species was regarded to haveonebyVánky&Shivas(2001).Thepresenceorabsenceof columellae, peridia, sterile cells and dimorphic spores has formed the taxonomic boundary between Sporisorium and Usti-lago, and interpretations of these structures must be consistent beforethecomplexcanberesolved.AnothercharacterusedtodefineSporisorium was that spores wereoftencompactedinpermanent(orsemi-permanent)sporeballs (Vánky2002a,Vánky&Shivas 2008).Vánky (1998c)considered spore balls to be homoplasious in the Ustilagino-mycotina and they do not occur across all taxa in Sporisorium. Vánky(2011b)recognised326speciesofSporisorium.
MacalpinomycesLangdon&Fullerton (1977)establishedMacalpinomyces to accommodate M. eriachnes, which they considered as distinct from Sporisorium and Ustilago.Macalpinomyces lacked colu-mellae, produced sterile cells and the spores were uniformly ornamentedandpolyangularorsubpolyangular (Langdon&Fullerton1977,Vánky1996).
Fig. 3Diversityofsoralmorphologyin Macalpinomyces.a.M. ewartii on Sorghum timorense;b.M. arundinellae-setosae on Arundinella setosa;c.M. mackin-layi on Eulalia mackinlayi;d.sporesofM. mackinlayi;e.M. siamensis on Coelorachis striata;f.M. eriachnes on Eriachne helmsii;g.sporesofM. eriachnes.—Scalebars:d,g=10µm.
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The nomenclatural history of M. eriachnes epitomises the confu-sion caused by many taxa in the Ustilago-Sporisorium-Macal-pinomycescomplex.TheoriginalcollectionofM. eriachnes in Australia by the botanist Ferdinand von Mueller, was divided andsenttotwomycologists,MordecaiCookeinEnglandandFelixvonThümeninGermany.Twonewfungaltaxawerede-scribed based on this single collection, Sorosporium eriachnes byThümenin1878andUstilago australis byCookein1879(Langdon&Fullerton1977).Langdon&Fullerton(1977)latertransferred this smut to a new genus, Macalpinomyces, nearly acenturyafterthespecimenwasfirstdescribed.Vánky(1996)broadenedtheconceptofMacalpinomyces to include taxa that lacked a columella but possessed sterile cells, which are morphological features shared by both Sporisorium and Ustilago.Thisledtonumeroustaxonomiccombinations,for example, M. bursus, M. neglectus and M. spinulosus.Thebroadened concept of Macalpinomyces allowed for a variety of gross morphologies to be included, ranging from localised or systemic galls in the ovaries, to longitudinally hypertrophied sori up to 16 cm long in M. chrysopogonicola(Fig.3).Molecular phylogenetic analysis has shown that Macalpinomy-ces ispolyphyletic.Thetypespecies,M. eriachnes, is sister to all other taxa in the complex, and forms a monotypic genus within the Ustilaginaceae (Stoll et al. 2005).Begerow et al. (2006),intheirphylogeneticstudyoftheUstilaginomycotina, proposed that M. eriachnes might not belong to the Ustilagi-naceae as it did not occur in the clade containing Sporisorium, Ustilago and Moesziomyces.Species of Macalpinomyces have sterile cells, a peridium derivedfromhostmaterial,and lack truesporeballs(Vánky2011b).Vánky(2011b)accepted46speciesofMacalpinomyces.
Relationships within the Ustilago-Sporisorium-Macalpinomyces complexTaxa within the Ustilago-Sporisorium-Macalpinomyces com-plex often possess morphological characters that occur in morethanonegenus.Overlappingcharacterscreateuncer-tainty for species placement, as illustrated by Macalpinomyces eriachnes, which was independently placed in both Ustilago and Sorosporium.Inacomprehensivetaxonomicstudyoverthecourseofeightyears,Vánky(1996,1997,1998d,2001c,2002b,2003a,b,2004a,b)andVánky&Shivas(2001,2003)combinedover30smutspeciesthatpossessedacombinationof Sporisorium and Ustilago characters into Macalpinomyces.Taxonomic shuffling occurred later with many species described before1978asUstilago and that were subsequently moved to either Macalpinomyces or Sporisorium.Theresultwasthatmany taxa have been moved back and forth among genera without systematic evidence that they constituted natural, monophyleticgroups.New genera have been raised for some smuts that differed subtly from the type descriptions of Ustilago, Sporisorium and Macalpinomyces.Endosporisorium (Vánky1995a),Lundquis-tia (Vánky2001b),Anthracocystis (Brefeld1912),Yenia (Liou1949) andTubisorus (Vánky&Lutz 2011) are examplesofgenera that were proposed to subdivide Ustilago and Spori-sorium.Thedescriptionofnewgeneraorplacementoftaxainpoorlydefinedgenera,hascontributedtosystematicconfusionwithinthecomplex.Vánky(1995a)describedEndosporisorium to accommodate Sorosporium capillipedii (type)andSorosporium loudetiae and lateraddedtwoothersmut taxa(Vánky1995b).Thisgenusdiffers from Ustilago in having sterile cells and ephemeral spore balls, and from Sporisorium in lacking columellae and afungalderivedperidium.ThesoriofEndosporisorium were describedfromthestemsratherthantheinflorescences.After
Vánky(1996)emendedMacalpinomyces to encompass more taxa, he subsequently synonymised Endosporisorium with Ma-calpinomyces, preferring a large, well-delimited genus, rather thanmanymonotypicandcloselyrelatedgenera(Vánky1997).Vánky(2001b)originallyestablished Lundquistia for L. fascicula-ris(syn.L. panici-leucophaei),andlateraddedthreeothertaxa(Vánky2004c),whichweretransferredfromeitherSporisorium or Ustilago.TheemendedLundquistia (Vánky2004c)differedfromUstilago inhavingsporeballsandsterilecells;fromSporisorium inlackingperidiaandcolumellae;andfromMacalpinomyces in havingpermanentorephemeralsporeballs.Molecularphylo-genetic analyses showed that Lundquistia was a synonym of Sporisorium as it occurred in the Sporisorium clade(Cunningtonetal.2005,Stolletal.2005).Cunningtonetal. (2005)includedfour Lundquistia species in their phylogenetic analysis using the ITSregionanddemonstratedthatitwasapolyphyleticgroup.Vánky(2001b)describedLundquistia as lacking true columellae, whereas,Piepenbring(1999)consideredthefascicularvascularbundles mixed with fungal material as columellae in Sporisorium panici-leucophaei(syn.L. panici-leucophaei).Brefeld(1912)describedAnthracocystis for a smut on Panicum miliaceum, which is currently named Sporisorium destruens.Heconsidered it different from Ustilago due to the peculiar formation ofitssoralperidium,whichdevelopedfromthefloralenvelopes.Soral structures such as columellae and spore balls were not includedintheprotologue(Brefeld1912).Vánky(2002a)erro-neously considered Anthracocystis a nomen nudum and thereby anillegitimatenameaccordingtothethen‘InternationalCodeofBotanicalNomenclature’.However,Anthracocystis is a validly published name, as it contained a diagnosis and was described in1912,beforeLatinwasrequiredintaxonomicdescriptions.Vánkyetal. (2006)describedAnomalomyces as a monotypic genus with shared characters of Ustilago, Sporisorium and Macalpinomyces, but with a unique partitioning of the sorus andtwotypesofsterilecells.Theyestablishedanewgenusbased on the peculiar morphology and a phylogenetic analysis that placed Anomalomyces in a polytomy with the Sporisorium groups and the Ustilago groupoccurring onpooid grasses.Anomalomyces differed from Ustilago by possessing a peridi-um,sporeballsandsterilecells,butdidnotfitintoSporisorium as it lackedcolumellae. Itdiffered fromMacalpinomyces by possessinggenuinesporeballs.SomespeciesfitunambiguouslyintoSporisorium and Ustilago.Molecular phylogenetic analysis has shown many morphologi-cally similar smut species to be sister to the types of Sporisorium and Ustilago(Stolletal.2005).Macalpinomyces was resolved asamonotypicgenus(Stolletal.2005).ThedifficultywiththeUstilago-Sporisorium-Macalpinomyces complex has been that many species do not sit strictly within the boundaries of the generaasdefinedbythetypes.Toresolvethisproblem,thegenera Ustilago and Sporisorium must be re-described and new genera, based on monophyletic groups, must be established toaccommodatetaxanotincludedintheemendedgenera.
DETERMINING A NATURAL CLASSIFICATION OF THE USTILAGO-SPORISORIUM-MACALPINOMYCES COMPLEX
Studies based on spore and ultrastructural morphologies were unable to resolve the Ustilago-Sporisorium-Macalpinomyces complex (Vánky1991,Piepenbringetal.1998).Langdon&Fullerton(1975)usedsoralontogenyasameanstoseparateSporisorium (asSorosporium) and Ustilago. Molecular phylo-genetic analyses showed that there were several monophyletic groups within the Ustilago-Sporisorium-Macalpinomyces com-plex, but there was no correlation between these groups and
60 Persoonia–Volume29,2012
theirmorphologicaltraits(Stolletal.2003,2005).Stolletal. (2005)notedstrongevidencethatsmutshadco-evolvedwiththeir grass hosts, and sister taxa usually occurred on closely relatedgrasses.Stoll etal. (2005)consideredthemorphologyofcolumellae,peridia,sterilecells,sporeballsandtheclassificationof thehosts(tribeorsubtribe)intheirmolecularphylogeneticanalysisof the Ustilago-Sporisorium-Macalpinomyces complex.Theymapped these characters onto the hypothesised phylogeny, butnoneappearedconsistentlywithinthemonophyleticgroups.Stolletal. (2005)concludedthatsoralmorphologywasunsuit-ablefordelimitinggeneraandresolvingtheclassificationoftheUstilago-Sporisorium-Macalpinomyces complex.
Taxa in the Ustilago-Sporisorium-Macalpinomyces complex should not be unified under Ustilago: a case study with smuts on ThemedaThemeda belongs to the grass tribe Andropogoneae in the subfamily Paniceae. Themeda is parasitizedby 17 speciesin the Ustilago-Sporisorium-Macalpinomyces complex, which includesfourtypesofsoralmorphology(Fig.4).Severaltaxa,for example, Sporisorium themedae (Fig. 2g),S. exsertum and S. benguetense (Fig.4a),infectallthespikeletsinanin-florescence, but leave the inflorescence architecture otherwise intact.Thesespeciesalsopossessstoutorwoodycolumellae.Sporisorium anthistiriae (Fig.4b)andS. holstii infect individual spikeletsinaninflorescence.SpeciessuchasSporisorium en-teromorphum (Fig.4c)andS. langdonii, destroy entire racemes withsorithathaveseveralfiliformcolumellae.Macalpinomyces bursus (Fig.4d)occurslocalisedinhypertrophiedovaries.Vánky(2001a,2002a)andPiepenbring(2004)believedoneoftwo approaches were needed to resolve the Ustilago-Sporiso-rium-Macalpinomyces complex.Thefirstwastosynonymiseall of the genera under the earliest name, Ustilago, and the second was to split the three genera into smaller genera and subgenera.Unification of the smuts onThemeda into one genuswouldprovideanaturalclassification,albeitnotaveryuseful one, and to group them based on what appear to be convergent characters would exacerbate taxonomic problems withinthecomplex.There has been a view that host anatomy dictates the soral morphologyofsmuttaxa(Piepenbring2004,Stolletal.2005).Holton etal. (1968)arguedthatgrossmorphologywasdeter-minedbygenotypicorinherentlypermanentfactors.Thegrossmorphology of an infection will be influenced to some extent byenvironmentalfactors(Fullerton1975),butasinthecaseof the smuts on Themeda, the morphology of the sorus will be
distinctive for different species rather than dependant on the structureofthegrass.A diverse range of soral morphologies occur in the Ustilago-Sporisorium-Macalpinomyces complex on other andropogonoid grasses, for example, in Bothriochloa, Sorghum and Heteropo-gon,whicharehostto15,nineandeightsmuts,respectively.Itwillbepossibletodistinguishgeneraifsoralmorphologyissynapomorphic.Weconsider that thisdiversitynecessitatesthe recognition of new genera or subgenera, rather than the unificationofcurrentgenerainthecomplexintoUstilago.
CONCLUSION
Is there a solution to the Ustilago-Sporisorium-Macalpinomyces complex?Ithasbeenapproximately200yearssincethegeneraUstilago and Sporisorium werefirstdescribed.Thesegeneracontaina diversity of taxa that do not strictly conform to the original genericdescriptions.Inparticular,thegenusMacalpinomyces containsmanyspeciesthathavespecificcharactersfrombothSporisorium and Ustilago.A stable andworkable taxonomyneedstobedevelopedfortheseimportantplantpathogens.Vánky(2002a),Stoll etal. (2005)andVánky etal. (2006) sug-gested that analysing additional molecular loci could resolve the Ustilago-Sporisorium-Macalpinomyces complex.Itisimportantto relate synapomorphic characters to monophyletic groups inordertocreateameaningfultaxonomy(Mooi&Gill2010).Resolution of the complex will depend on a combined analysis ofmorphologicalandmolecularcharacters.Inclusionofmorphologicaldatawillhelptodeterminesynapo-morphiesthatcanbeusedtodefinegroupswithintheUstilago-Sporisorium-Macalpinomyces complex.To accomplish this,a more detailed examination of the soral structures and their developmentiswarranted.Langdon&Fullerton(1975)identifieddifferent soral development patterns in several species of Sporisorium, but lacked the advantage of molecular phylo-geneticanalysisonwhichtobaseanewclassification.Stoll et al. (2005)consideredthepresenceorabsenceofcolumellaeandperidiaintheirstudy,butdidnotidentifysynapomorphies.Itisprematuretodismisscharactersthatwerethoughttobehomoplasious, for example spore balls, as a means to delimit genera in the Ustilaginaceae. It is possible that sporeballshave evolved independently within monophyletic groups in the Ustilago-Sporisorium-Macalpinomyces complex.Becausethereare limited morphological characters that can be examined it is necessary to include all the available characters to determine theirsystematicpotential.
Fig. 4 Four smuts that occur on Themeda.a.Sporisorium benguetense;b.S. anthistiriae;c.S. enteromorphum;d.Macalpinomyces bursus.
cb da
61A.R.McTaggartetal.:Ustilago-Sporisorium-Macalpinomyces complex
GenericconceptsofUstilago, Sporisorium and Macalpinomy-ces havebeenrefinedoverthelast30years,althoughtheystillremainpolyphyleticgenera.Thediversityoftaxawithinthecomplexrequiresfurtherdelimitationratherthanunificationofall smuts under Ustilago.Ustilago, Sporisorium and Macalpino-myces needtoberevisedandanewclassificationestablishedbased on the synapomorphic characters found in monophyletic groups.
Acknowledgements We thankPaulKirk forhelpwith the taxonomyofAnthracocystis.ARMwouldliketoacknowledgethesupportoftheAustralianGovernment’sCooperativeResearchCentreProgram.
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