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© 2011 International Mycological Association

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INTRODUCTION

It has been a bit over two decades since the polymerase chain reaction(PCR)changedevolutionarybiologyingeneralandfungal systematics in particular.EvenbeforePCRbecamegenerally available, mycologists realized that the evolutionary record contained in the nucleic acid sequence of every fungus could be used to merge two systems of nomenclature that hadbeenemployedinmostfungi,i.e.oneforthe“Eumycota”basedonsexualmorphologyandthe“Deuteromycota”basedonallothermorphologies(Berbee&Taylor1992,Brunset al.1991,Guadetet al.1989,Reynolds&Taylor1992).Why,then,has it taken more than two decades for nomenclature to catch up with biology, and why is the possibility of nomenclatorial rapprochementnowbeingtakenseriously?Thesequestions,and three others posed to the participants in this symposium willbethesubjectofthiscontribution:DoesDNAsequencingmakedualnomenclaturesuperfluous?CantheInternationalCodeofBotanicalNomenclature(ICBN)(McNeillet al.2006)bemodified to enable this process, orwould aMycoCodebe more effective? How can the mycological community get ridofthelegacyofdualnomenclatureandArticle59withoutnomenclatural chaos?

Two examples illustrate the practical problems raisedby dual nomenclature. First, this year, while serving as amember of a governmental committee researching the use of mycoherbicides to eradicate drug crops, it fell to me to explain the nomenclature of two poppy pathogens that are sister species, one named as a teleomorph Crivellia

papaveracea and the other as an anamorph, Brachycladium papaveris(Inderbitzinet al.2006)(Fig.1).Thefifteenothermembers of the committee, eleven academics and four very knowledgeable staff, stared at me in disbelief when I said that sisterspeciescouldhavedifferentgenericnames.Second,together with Tom Bruns, I have been directing researchabout fungi that naturally decay plants proposed as sources oflignocellulosefortheproductionofbiofuels.Inthecourseof this work, we have sequenced ITS using DNA isolatedfrom the decaying grasses and compared the sequences to thosedepositedinGenBank.Often,asinglesequencewillbeattached to two names; you guessed it, it’s the same fungus with some GenBank sequences having been depositedunder the teleomorph name and others under the anamorph name.Perpetuationofdualnomenclaturewhenwehavethemeanstoabandonitishinderingmycology,bothscientificallyandsocially.

Dual nomenclature has persisted for the past 20 yearsbecause few mycologists are deeply interested in both molecular phylogenetics and nomenclature. One Fungus=OneNamehasgainedmomentum,asevidencedby thisconference, because mycologists who are studying the

doi:10.5598/imafungus.2011.02.02.01 IMA FUNgUs · vOlUMe 2 · NO 2: 113–120

One Fungus = One Name: DNA and fungal nomenclature twenty years after PCR

JohnW.Taylor

UniversityofCaliforniaBerkeley,111KoshlandHall,Berkeley,CA94720-3102,USA;e-mail:jtaylor@berkeley.edu

Abstract: Somefungiwithpleomorphiclife-cyclesstillbeartwonamesdespitemorethan20yearsofmolecularphylogeneticsthathaveshownhowtomergethetwosystemsofclassification,theasexual“Deuteromycota”andthesexual“Eumycota”.Mycologistshavebeguntofloutnomenclatorialregulationsandusejustonenamefor one fungus. The International Code of Botanical Nomenclature (ICBN) must change to accommodatecurrentpracticeorbecomeirrelevant.ThefundamentaldifferenceinthesizeoffungiandplantshadaroleintheoriginofdualnomenclatureandcontinuestohinderthedevelopmentofanICBNthatfullyaccommodatesmicroscopicfungi.Anomenclatorialcrisisalsoloomsduetoenvironmentalsequencing,whichsuggeststhatmostfungiwillhavetobenamedwithoutaphysicalspecimen.MycologymayneedtobreakfromtheICBNandcreateaMycoCodetoaccountforfungiknownonlyfromenvironmentalnucleicacidsequence(i.e.ENASfungi).

Article info:Submitted:8June2011;Accepted:15June2011;Published:12July2011.

Key words: AmsterdamDeclarationENASMycoCodenomenclaturepleomorphic fungi

Dedication:DedicatedtoDonReynolds,mycologicalicono-clast,whosesabbaticalvisittoBerkeleyfromtheLosAngelesCountyMuseumofNaturalHistorymorethan20yearsagostimulatedthoughtaboutOneFungus=OneName.

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molecular phylogenetics of economically important fungal groups have begun naming newly recognized genus-level clades with just one Ascomycota name, whether or not the fungus exhibits sexual reproduction.The first thoroughexploration of this practice was provided by Crous et al. (2006), whose revision of the Botrysphaeriaceae includes thissentence, “Separate teleomorphandanamorphnamesare not provided for newly introduced genera, even where both morphs are known.” Where a teleomorph name wasavailable, as in the case of Botryosphaeria, the authors used it.Whereonlyanamorphnameswereavailable, theywereused,e.g.Macrophomina or Neoscytalidium.Whereanewclade was segregated from an existing teleomorph genus, and best distinguished by the anamorphic morphology, the newnamereflectedtheanamorph,e.g.Neofusicoccum.

MattersweretakenfurtherinastudyofPenicillium species by Houbraken et al.(2010).Astheyputit,“Usingthisapproachandapplyingtheconceptofonenameforonefungus(Reynolds& Taylor 1992), we have chosen to describe these twospeciesunder[their]anamorphicname.”That is,Houbrakenet al.describednewspeciesthathavebothanamorphicandteleomorphicstatesasspeciesintheanamorph-typifiedgenusPenicillium and ignored the existing teleomorphic generic name, Eupenicillium. These actions are clearly outside theICBNandconstituteasocialrebellion.Thoughsmallerandfarless important than social rebellions concerning, for example, women’s rights, the rights ofAfricanAmericans, or thoseofhomosexuals, this mycological rebellion is similar to the others in that activism has outpaced the law and the law must now changeorbecomeirrelevant.

Dualnomenclaturehasalonghistory.Thechoicemadeby Houbraken et al. ( 2010) to use the anamorph namePenicillium over the teleomorph name Eupenicillium for one of the most economically important fungi echoes the choice mademorethan40yearsearlierbyRaper&Fennel(1965)when they applied the anamorphic name Aspergillus to all members of that genus whether or not the species also producedasexualstructure.Fortyyearsarenotenoughtounderstand the origins of dual nomenclature, to do that we havetogoall thewaybacktoLinnaeusandthebeginningofbotanicalnomenclature.Inthistourbackthroughtime,ourguideswill beWeresub&Pirozynski through theirexcellentarticle on the history of fungi that produce both meiotic

and mitotic spores, that is, pleomorphic fungi (Weresub& Pirozynski 1979) and the opening chapters of Selecta Fungorum Carpologia,themonumentalworkofLouis-RenéTulasne and Charles Tulasne (Fig. 2) (Tulasne & Tulasne1861).

The Tulasne’s point out that Linnaeus based his planttaxonomyonfloralmorphologyandthathecoulddemonstratethateachplanthadbutonetypeofflower.Atatimewhenfungiwere considered to be plants, and fungal spores were equated withseeds,Linnaeusextendedhistaxonomicconcepttofungi.TheTulasnebrothersthenarguethatLinnaeushadsuchaninfluenceoverhismycologicalcontemporaries,Friesforemostamong them, that these mycologists were in denial about pleomorphy, despite their being able to see more than one typeof“seed”throughtheirlenses.

“IntheMucedinei[Fries]seestheconidia...buteverywhereheflatlydeniesthatthereoccur“twokindsofsporidiaonthesameplant”,exactlyasifhehadheard,soundinginhisears,theloudvoiceofLinnaeus,crying“Itwouldbearemarkabledoctrine–thattherecouldexistracesdifferinginfructification,but possessing one and the same nature and power; that one andhesameracecouldhavedifferentfructifications;forthebasisof fructification,which isalso thebasisofallbotanicalscience, would thereby be destroyed, and the natural classes ofplantswouldbebrokenup”(Tulasne&Tulasne1861:481).The brothers go on to chide Linnaeus, adding “But sincethe illustrious author always completely abjured the use of magnifying glasses, and therefore scarcely ever tried to describeaccuratelyeitherconidiaorspores,wefear(mayhepardonthestatement)thathereallyknewveryfewseedsofeitherkind” (Tulasne&Tulasne1861:48-49).The influencethat the size of an organism has on its systematics can be profound(Tayloret al.2006).Thefactthattheoverwhelmingmajority of plants are macroscopic while the overwhelming majority of fungi are microscopic still affects nomenclature and willberevisitedneartheendofthisarticle.

Louis René and Charles Tulasne went on to argueagainst mycological denial of pleomorphy when they wrote, “Thefungusuponwhichwearenowtouching[Pleospora] is not only almost the commonest of all belonging to its order, but also affords a wonderful proof of our doctrine concerning the multiple nature of the seeds ofspeciesoffungi“(Tulasne& Tulasne 1861: 248). One cannot help wondering if thebrothers guessed not only that their work was controversial, but that the mycological world was heading toward dual nomenclature, when they wrote, “As today we have seenthe various members of the same species now unwisely torn fromoneanotheragainstthelawsofnature...”(Tulasne&Tulasne1861:189).

Alas,whenthemostusefulcharactersthatcouldbeusedfor classification were meiosporic, and when many fungidid not exhibit them, there were not many options and the onethatprevailedwasdualnomenclature.Fuckel,aretired

Pleospora

Alternaria

Crivellia papaveracea/Brachycladium penicillatum

Crivellia sp (unnamed)/Brachycladium papaveris

Fig. 1.PhylogeneticrelationshipsofthesisterspeciesCrivellia pa-paveracea and Brachycladium papaveris, the former named as tele-omorphicandthelatterasananamorphicfungus.TheCrivellia state of B. papaveris remains unnamed due to a lack of suitable material to serveasanomenclaturaltype(Inderbitzenet al.2006).

1 The English translations are from the 1931 Clarendon Press(Oxford)edition,andwerepreparedbyWBGroveandeditedbyAHRBullerandCLShear.

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pharmacist,gottheballrolling(Fuckel1870)andSaccardodid the heavy lifting with his Sylloge Fungorum beginning in 1882 (Saccardo1882).By1910, the InternationalRulesofBotanicalNomenclature (Briquet1912)containedasectionofArticle49,Art49 bis(theprecursorofthecurrentArticle59),thatforbade“botanical”namesforanybutthesexualstageof pleomorphic fungi and that is where matters rest with the currentICBN.

Saccardo’s use of mature anamorph morphology iswonderfully convenient for classification and identificationbut,obviously, it isnotbasedonevolutionaryrelationships.Thehopethatstudyofmitosporedevelopmentwouldleadtoa separate systematics based on evolutionary relationships beganwithVuillemin(1910a,b)andMason(1933,1937)andledtotheworkofHughes(1953),Tubaki(1958)andBarron(1968).Elegantmicroscopicstudiesofmitosporedevelopmentfollowed(Cole&Samson1979)andthemovementreachedits zenith at the second Kananaskis conference (Kendrick1979).Justasthesestudiesofdevelopmentwerepeaking,two events occurred in the realms of evolution and systematics that promised the irresistible appeal of a new approach and a seemingly endless supply of characters – cladistic analysis (Hennig1966)andaccesstonucleicacidvariation.

The first applications of nucleic acid variation to fungalsystematics involved DNA-DNA hybridization of yeasts(Kurtzman 1980) and then sequencing of nucleic acids.Pioneering work with painfully difficult RNA sequencingmodeled on thework of bacteriologists (Walker&Doolittle1982, 1983)was followed byDNA sequencing (Gottschalk&Blanz1984,Guadetet al.1989,Guehoet al.1989).But

itwasthediscoveryofthepolymerasechainreaction(PCR)(Rabinow 1996, Saiki et al. 1988) that made possible thebroadstudieswenowtakeforgranted.

The first application of PCR amplified DNA sequenceto fungal phylogenetics demonstrated the evolution of hypogeous fungi from mushroom ancestors (Bruns et al. 1989; Fig. 3). This work relied on the development ofprimers designed to amplify regions of both mitochondrial andnuclearrDNAincludingthenuclearsmallsubunit,largesubunit and internal transcribed spacer (ITS), which werepublished the following year and have been cited a bit more oftenthanonce-a-daysincethen(Whiteet al.1990;Fig.4).

Fig. 2.LouisRenèTulasne(l)andCharlesTulasne(r).Photo:courtesyoftheNationalMuseumofNaturalHistory,Paris.

Boletus

Suillus

Rhizopogon

Boletus

Suillus

Rhizopogon

Fig. 3. Phylogenetic analysis ofPCRamplified rDNAshowing theevolution of hypogeous Basidiomycota in the genusRhizopogon, from mushroom ancestors in the genus Suillus(Brunset al.1989).AdaptedfromBrunset al.(1989).

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Withinafewyears,analysisofPCRamplifiedrDNAshowedthat the anamorphic Sporothrix schenckii nested within the teleomorph genus Ophiostoma (Berbee&Taylor1992;Fig.5). This work demonstrated the integration of anamorphicand teleomorphic fungi based on DNA variation, as hadearlier work on Fusarium(Guadetet al.1989).Thesestudiesshowedaseparateclassification for “Deuteromycota” tobesuperfluous.

Thatsameyear,Reynolds&Taylor(1992)addressedthenomenclaturalimplicationsofusingDNAvariationtoassessthephylogenetic relationshipsof fungi,writing, “Theuseofnucleic acid sequence allows systematists to demonstrate the phylogenetic relatedness of fungi possessing and lackingmeioticallyproducedspores....Thisdemonstrationpresents a serious challenge to the separate classificationof these two types of fungi and undermines the elevated position that characters associated with sexual reproduction haveheldintheclassificationofhigherfungi....Webelievethat all fungi should be classified in one system and thatcharacters associated with sexual reproduction should be giventhesameweightasothercharacters....Bythebroadinterpretation [ofArticle59] incurrentuse, thepotential forpleomorphyisassumedofallfungiandtheArticleisappliedtoall fungi. . . .Withanalternativeandstrict interpretationhowever,Article59wouldapplyonly to fungalspecies thathavebeenactuallydemonstratedtobepleomorphic.Underthe latter interpretation, sexual, asexual, and pleomorphic fungiwouldbeclassified togetherand form taxawouldnotbenecessary.”

FollowingtheFungalHolomorphSymposiuminNewport(OR,USA)todiscussnucleicacidvariationandtheintegrationofanamorphicandteleomorphicclassifications(Reynolds&Taylor1993),therehavebeenpresentationsanddiscussionsonthetopicateveryInternationalMycologicalCongressfrom

Fig. 4.AuthorsofthepublicationofPCRprimersfortheamplificationanddirectsequencingoffungalribosomalRNAgenesforphylogenetics.Lefttoright:TomBruns,TomWhite,SteveLee,andJohnTaylor.Photo:takenin2010,20yearsafterthepublicationofWhiteet al.(1990).

Sporothrix schenckii

Ophiostoma stenoceras

Ophiostoma ulmi

Leucostoma persoonii

Neurospora crassa

Fig. 5.PhylogeneticanalysisofPCRamplified rDNAshowing theanamorphic Sporothrix schenckii nestled within the teleomorphic ge-nus Ophiostoma(Berbee&Taylor1992).

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Vancouver(1994;Taylor1995)toEdinburgh(2010;Norvellet al.2010),leadinguptothepresentOneFungus=OneNameconferenceandtheAmsterdamDeclaration(Hawksworthet al.2011).

Nucleicacidvariabilityhasproved tobeuseful inotherareas of fungal systematics and classification related tomitoticfungi.BeginningwiththemitosporichumanpathogenCoccidioides immitis,DNAvariationhasbeenusedtoshowthatanamorphicfungirecombineinnature(Burtet al.1996),thattheyspeciate(Koufopanouet al.1997),andthat,basedonlyonDNAvariation,theycanbedescribedinthesystemfor Ascomycota (Fisheret al. 2002).AsFisheret al.wrotewhen they described a new Coccidioides species as an ascomycete, “Coccidioides posadasii is morphologically indistinguishable from Coccidioides immitis. C. posadasii is diagnosed by the following nucleotide characters (givenas the gene, the nucleotide position in the gene, and, parenthetically,thenucleotidefixedinC. posadasii)showingreciprocal fixation between C. immitis and C. posadasii: Chitin synthase positions 192 (A), 288 (T); Dioxygenasepositions872 (C),1005 (C),1020 (G),1179 (C),1272 (T);etc.”Ofcourse,descriptionisnotthesameasacceptance.In the case of Coccidioides posadasii, acceptance for this “SelectAgent”camefromanunexpectedquarter,theUnitedStatesCongress(FederalRegister2005).

Another point made soon after PCR became availablewas thatDNA,orevenaDNAsequence, couldactas thetype element in a species description (Reynolds & Taylor1991).This observation has gained importance due to theadvent of environmental sequencing, where mycologists use PCRprimersforrDNAtoamplifyvariableregionsfromDNAisolated fromsoil orplants.Environmental sequencinghasbegun to produce large numbers of rDNA sequences that

document the existence of fungi for which there is neither a specimennoraculture.Most importantly,ecologicalstudeshave shown that the number of these DNA-only fungi,or “Environmental Nucleic Acid Sequences” (ENAS) canexceed the number of fungi for which there is a culture or specimen(Jumpponen&Jones2009,2010).Thisimbalanceposesachallengetofungalclassificationandnomenclaturethat may dwarf the challenge of integrating anamorphic and teleomorphicfungi.

David Hibbett, in his plenary presentation at IMC9(Hibbettet al.2011),notedthatthenumberoffungalOTUsaddedeachyeartoGenBankthatarebasedonlyonrDNAsequences(ENASfungi)isnowexceedingthenumberfromfungi with cultures or specimens (Fig. 6). Ecologists facethe prospect that most of the fungal species dwelling in their favourite environment can neither be cultivated nor collected; asaresulttheyaregoingtohavetorelyonENAStoassessthetruefungaldiversity.Eachoftheseecologicalstudiesmayaddhundredsor thousandsofENAStoGenBank.Already,searches of GenBank using a new ENAS mostly recoverpreviously deposited ENASs, which are identified not bynamesbutbynumbers.Imaginetwoecologicalstudies,onewhereeachnewENASintablesorfiguresisassociatedwithanumbered,existingENASandtheotherwheretheexistingENASshavebeennamed–thereaderwouldcomeawaywithignoranceontheonehandandunderstandingontheother.FungalclassificationandnomenclaturemustrespondtothischallengebydevelopingameansofassociatingENASswithnamesandtheresponsemustbetimely.

AsdiscussedbyHibbettetal. (2011),fungiknownonlyasENAScanbenamedbycomparisontonamedfungialreadyinGenBank.ItseemsimportantthatthisnamebeidentifiedasattachedtoanENASratherthanacultureorspecimen,

Environmental Nucleic Acid Sequence (ENAS)Specimen BasedBoth ENAS and Specimen Based

Fig. 6.GraphoftheOperationalTaxonomicUnits(OTUs)addedtoGenBankfrom1991to2009showingtheincreasingproportionofOTUsbasedonlyonenvironmentalnucleicacidsequence(ENAS).AdaptedfromHibbettet al.(2011).

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perhapsbyappendingENASasasuffix.SeveralessentialissueswillhavetoaddressedbeforeENASnamingcanbegin,among them the problems of sequencing errors, variation in rDNAsequencewithinanindividual,andaccommodationofall thesenewENASfungi inMycoBank(Hawksworthet al. 2010).Perhapsmostunsettlingly,thenamingwillhavetobeautomated in some way because no one can possibly name the thousands of new sequences that will arise in each new environmentalstudy.

At this point, a reader might fairly ask, if separate“Deuteromycota” and “Eumycota” nomenclatural systemsstill remain separate 20 years after their merger becameintellectually obvious, how could anyone possibly entertain thoughts about the acceptance of the automated description of fungi based only on DNA sequence? I see two stepsto acceptance of ENAS fungi. The first step would be apublished demonstration of the naming of ENAS fungi,echoing the aforementioned social activism already in play forOneFungus=OneName(Crouset al.2006,Houbrakenet al.2010).Thesecondstep,acceptanceofnamedENASfungi by the ICBN, is the tougher problem and is unlikelyto occur quickly enough to satisfy the pressing needs of fungalecologists.Here,socialactivismaloneisnotgoingtobesufficient largelydue to theproblemoforganismalsize,mentionedabove,whichisasoldasLinnaeus.Mycologistscannot expect botanists to fully appreciate the problems created by working with microscopic organisms that can neitherberoutinelycollectednorcultured.Mycology,tofreeitself from the legacy of botanical nomenclature, needs a nomenclatorialrevolution.

It is time for mycologists, who best understand the nomenclatorial needs peculiar to fungi, to design a nomenclatorialcodeforfungi.Thetimingcouldnotbebetterbecauseover thepast twodecadesoneofourown,DavidHawksworth, has been helping to guide the development of the BioCode (Greuter et al. 2011, Hawksworth 2011).Modificationof thedraftBioCode toenableOneFungus=OneNameandtoaccommodateENASfungicouldproduceaMycoCodethatwouldbefullycompatiblewiththeBioCode.In considering microscopic organisms, a newly created MycoCode could also inspire those working on Bacteria, Archaea and other microscopic Eukarya. We mycologistshave the need and, in the nomenclatorial committees of the International MycologicalAssociation2 and the MycologicalSectionoftheInternationalUnionofMicrobiologicalSocieties,themeanstoaccomplishthistask.Allthatmycologistsnowlackisanexcusetodonothing.

ACKNOWleDgeMeNTs

Thanks are due toPedroCrous andRobertSamsonof theCBS,Utrecht, who conceived of and hosted the One Fungus = OneNameConference, on 19–20April 2011 inAmsterdam. JWT alsoacknowledgessupportfromNSFDEB-0516511

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