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Mycologia, 98(6), 2006, pp. 829–837. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 Issued 19 April 2007

Research Coordination Networks: a phylogeny for Fungi (Deep )

Meredith Blackwell1 publications that require a phylogenetic classification Department of Biological Sciences, Louisiana State of fungi. University, Baton Rouge, Louisiana 70803 Key words: mycological community, mycota, David S. Hibbett systematics Department of Biology, Clark University, Worcester, Fungi have a profound impact on global ecosys- Massachusetts 01610 tems. They modify our habitats and are essential for many functions. Fungi form soil, recycle John W. Taylor nutrients, decay wood, enhance growth and cull Department of Plant and Microbial Biology, University from their environment. They feed us, poison of California, Berkeley, California 94720 us, parasitize us and cure us. They destroy our crops, Joseph W. Spatafora homes and libraries, but they also produce valuable Department of Botany and Plant Pathology, Oregon biochemicals, such as ethanol and antibiotics. For State University, Corvallis, Oregon 97331 both practical and intellectual reasons it is important to provide a phylogeny of Fungi on which a classifica- tion can be firmly based. The Deep Hypha Research Abstract: Research in fungal phylogenetics and Coordination Network, supported by the United systematics progressed rapidly in the past decade States National Science Foundation (NSF), promoted due to advances in DNA sequencing technologies and and facilitated the cooperation necessary for the analytical methods. A newfound wealth of sequence mycological community to construct a comprehensive data acquired through community-wide initiatives has phylogeny of the Fungi. Although Deep Hypha did advanced the process of acquiring a stable phyloge- not support data collection, it provided an essential netic classification of many fungal taxa. Financial forum for fungal systematists to plan, coordinate and support from the National Science Foundation Re- report their activities. One initiative that grew out of search Coordination Networks: a phylogeny for Deep Hypha was the NSF-supported Assembling the kingdom Fungi (Deep Hypha) for 5 y enabled more Fungal of Life project (AFTOL), which provided than 100 fungal systematists to assess the taxon money to develop multilocus molecular and morpho- sampling, molecular markers and analytical methods logical datasets for the entire kingdom. As the articles necessary to facilitate such a project. Later a second in this Deep Hypha issue of Mycologia attest, AFTOL NSF program provided financial support for the and other recent independent projects, helped di- Assembling the Fungal Tree of Life (AFTOL) project rectly or indirectly by Deep Hypha, have dramatically to accomplish much of the research. Deep Hypha enhanced our understanding of fungal phylogeny. In may be viewed as an involved parent of AFTOL with this mission, Deep Hypha has been a success. As a continuing role as coordinator of likeminded a gauge of progress in the field one may consider the workers. Many questions posed at the beginning of growth of fungal systematics through the latter half of the Deep Hypha project have been addressed, at least the 20th century, as reflected in the successive in part, although some details remain to be clarified. volumes of Introductory by C.J. Alexopoulos Many of the main branches of the fungal tree are and colleagues (Alexopoulos 1952, 1962; Alexopoulos stable and well supported, often as a result of and Mims 1979; Alexopoulos, Mims, Blackwell 1996). multigene analyses that involved collaboration of many laboratories. More work is necessary, however, The growth of fungal phylogenetics seen through to resolve certain branching events near the base of Alexopoulos’s Introductory Mycology.—The intent the tree, as well as to reconstruct relationships in of Alexopoulos’s Introductory Mycology has always some terminal groups. The phylogenetic classification been to be organized phylogenetically, as far as in this issue of Mycologia is a product of the AFTOL possible. The first edition (Alexopoulos 1952) began project and many other independent research in- with , including actinomycetes, and a modern itiatives, and it is an initial synthesis of a working concept of prokaryotic cells and their structure was classification designed to be used for all major lacking. The second edition (Alexopoulos 1962) omitted bacteria but included for the first time Labyrinthulales, Hyphochytridiomycetes [sic] and Accepted for publication 12 November 2006. Trichomycetes. These groups are still included in 1 Corresponding author. E-mail: [email protected] the latest edition of the text but mostly removed from

829 830 MYCOLOGIA a monophyletic concept of fungi with the exception removed with fungi and sharing common of some Trichomycetes. As will be seen below some ancestors? members of these of groups have come back into consideration as that are in a position basal to Phylogenetic status of kingdom Fungi at the time of fungi and animals. Alexopoulos was concerned writing the Deep Hypha proposal. A monophyletic particularly about the placement of slime , kingdom Fungi had been defined when Deep Hypha and although they are excluded from fungi their began (Barr 1992, Bruns et al 1992) with our position continues to be somewhat unsettled. The understanding of major subkingdom relationships third edition (Alexopoulos and Mims 1979) had a new summarized as follows: look with the addition of electron micrographs, the N Four phyla generally were accepted in kingdom revolutionary technique of the time. Classification, Fungi: , , Basidiomy- still problematic, included slime groups within cota and (Alexopoulos et al 1996, Barr Fungi but separated them in a different subdivision. 1992, Bowman et al 1992, Bruns et al 1992, and chytrids also were placed in separate Hawksworth et al 1995). subdivisions, and Deuteromycotina was a group equal N The phyla Chytridiomycota and Zygomycota were to but distinct from zygomycetes, ascomycetes and not supported as monophyletic and intergraded at basidiomycetes. several points based on analyses of the SSU rDNA In 1993 Charles Mims and Meredith Blackwell (Nagahama et al 1995, James et al 2000). revised the text to provide a fourth edition (1996). N The Chytridiomycota was the only taxon within For a book with a phylogenetic arrangement the kingdom Fungi to include representatives with timing of the revision was arguably less than a flagellated stage at some point in their life cycle, optimum, because results from DNA-based phyloge- and analyses agreed that some lineage of the netic studies were just appearing. In fact the text was Chytridiomycota occupied the most basal branch sent to the printer with a multitude of additions in the of kingdom Fungi, a finding consistent with ‘‘blue line’’ stage because of the appearance of new a ancestor; however there was papers and graciously contributed unpublished stud- conflict in the literature as to which group of the ies that helped to establish the bare bones of Chytridiomycota was most basal ( James et al 2000). a molecular phylogeny, which endured fairly well N The Chytridiomycota was paraphyletic, largely de- despite heavy reliance on a single gene, SSU rDNA. A fined by the ancestral character state of a smooth phylogeny was presented in a series of unresolved posterior . The Zygomycota was suspected that required the use of informal names for of being polyphyletic with multiple origins within numerous taxonomic groups. The text however did kingdom Fungi. Based on rDNA, at least one origin use for the first time the term ‘‘phylum’’, newly was derived from within the Chytridiomycota, sanctioned by the revised International Code of representing the loss of the flagellum; however Botanical Nomenclature from the Tokyo Botanical this was contradicted by analysis of b-tubulin Congress, and as such served as a transition between sequences (Keeling et al 2000, James et al 2000). the old and the new, with hints of many changes to N At the other extreme, the (until then come. The monophyly of Fungi was established by considered a member of Zygomycota) appeared separating four phyla from a number of excluded more closely related to the Ascomycota/Basidio- groups (water molds, labyrinthulids and several types mycota clade (Simon et al 1993) based on rDNA. of slime molds). Chytrids were placed firmly among N The larger clade comprising the Glomerales, Fungi, and the were unques- Ascomycota and was referred to as tionably excluded. There were surprises: Pneumocystis ‘‘crown’’ fungi; ‘‘crown’’ fungi were supported as was determined to be a , Mixia was recognized a derived, higher monophyletic taxon within the as a basidiomycete and Saccharomyces and Schizosac- Fungi, originated and diversified along with land charomyces were shown to be widely separated. plants (Redecker et al 2000, Simon et al 1993, Evidence was available to recognize the polyphyly of Taylor et al 1995). groups such as gasteromycetes and , and N The Basidiomycota and Ascomycota each were perhaps most important of all there was no phyloge- monophyletic and together formed the most netically defensible use of the Deuteromycetes derived fungal clade (Bowman et al 1992, Bruns (Taylor 1995, Taylor et al 1999). There were however et al 1992) that comprised more than 95% of all many intriguing unresolved questions: Is it possible known fungi. Higher-level relationships within that Basidiobolus is not a zygomycete? Are smuts and both the Ascomycota and Basidiomycota were rusts not monophyletic? Do animals represent the tenuous. sister group of fungi, or is the relationship more N The Ascomycota generally was recognized to in- BLACKWELL ET AL:APHYLOGENY FOR FUNGI 831

clude the classes Euascomycetes (mostly filamen- for deep nodes that have proved problematical tous, -producing and mitosporic or co- (e.g. monophyly of plus Ustilagi- nidial forms), (the true ), nomycotina, and monophyly of plus and Archiascomycetes (a paraphyletic assemblage Trichomycetes s.s.). of basal taxa) (Nishida and Sugiyama 1994, Taylor N James et al: The Chytridiomycota is not mono- et al 1993). phyletic. Fourteen clades, including a core group N The Basidiomycota generally was recognized to of the traditional chytrids, are defined; these include three classes: Urediniomycetes (rusts and clades have a paraphyletic relationship to other relatives), (smuts) and Hyme- flagellated fungi, notably Blastocladiales, many of nomycetes ( and relatives) (Swann and which have distinctive life cycles with sporic Taylor, 1995, Wells 1994). meiosis. Olpidium also falls outside the other N To that date, the lion’s share of phylogenetic chytrids. studies had been performed on nucleotide data N White et al: The Zygomycota as previously recog- determined from nuclear rDNA (Alexopoulos et al nized is not a monophyletic group. Two trichomy- 1996). cete groups no longer are considered to be fungi and the remaining traditional members have Deep Hypha accomplishments.—Mycologists were a paraphyletic relationship. Basidiobolus, tentative- primed for the first NSF Assembling the Tree of Life ly suggested to be a chytrid by SSU rDNA data, competition (2002) thanks to the community-wide appears as a sister of the with discussions on taxon sampling and methodology that increased taxon sampling and use of a multigene had been supported by Deep Hypha. Working with N dataset. the AFTOL consortium (and with much overlap in Redecker and Raab: is accepted as membership) many Deep Hypha participants focused a sister group of Basidiomycota + Ascomycota on the same major loci, including the well character- within kingdom Fungi on the basis of rDNA ized nuclear rRNA genes, and the protein-coding loci analysis (Schu¨ßler et al 2001). Some recent tef1 and rpb1 and rpb2, which had been promoted as analyses including protein coding genes support molecular phylogenetic markers in Fungi by Hall and monophyly of the phylum but also cast doubt on colleagues (Liu et al 1999). The coordinated sam- the sister group relationship of these fungi with pling enabled construction of kingdomwide multi- Dikaryomycota. With a two-gene dataset the Glo- gene datasets (Lutzoni et al 2004, James et al 2006). meromycota is upheld as a monophyletic taxon Several Deep Hypha symposia and workshops were with six major clades. N 5 held in conjunction with other meetings during the Aime et al: ( Urediniomycetes) 5 AFTOL funding period. The symposia and workshops comprises the rusts, Pucciniales ( Urediniales) promoted multigene, collaborative research in fungal and related -producing taxa (e.g. Septo- phylogenetics, the use of state-of-the-art phylogenetic basidiales, Sporidiales, etc.). The is algorithms and fungal biology in broader scientific defined with eight major clades ranked as classes and educational communities. This Deep Hypha issue (, , Classi- of Mycologia presents phylogenetic analyses of most culomycetes, , Cystobasi- diomycetes, , major fungal clades, including many studies that were and ) and eighteen orders. aided by Deep Hypha and that use data obtained in N 5 the AFTOL project. The articles included in this issue Begerow et al: ( Ustilaginomy- provide summaries of the status of the phylogenetic cetes) comprises the smuts, Ustilaginales and related reconstruction for most of the major fungal lineages, taxa. Based on morphological, ultrastructural and molecular phylogenetic data, Ustilaginomycotina is although some clades (e.g. , Laboulbenio- defined with three classes, , Usti- mycetes) have been omitted. Some highlights follow. laginomycetes and , which collec- N Taylor and Berbee: Estimating the evolutionary age tively comprise 11 orders. of Fungi and the origin of its phyla and subphyla N Hibbett: Agaricomycotina (5Hymenomycetes), remains an elusive goal, but new fossil findings and one of the three main subphyla of Basidiomycota, improved analytical methods support an origin of includes , and Agar- all extant phyla by the (Taylor et al icomycetes. Phragmobasidia are present in all 1995). three classes with holobasidia restricted to the N Celio et al: Subcellular characters, especially . The Agaricomycetes includes associated with septal ultrastructure, while few in eight major subclades that are recognized as number, are providing important synapomorphies subclasses and orders and is characterized by high 832 MYCOLOGIA

levels of homoplasy associated with all major teoid and plicaturopsidoid. Ectomycorrhizae ap- basidioma morphologies (e.g. mushrooms, crusts, pear to have evolved at least 11 times in the etc.) , nine of them in the agaricoid/tricho- N Larsson et al: The (hymenochae- lomatoid clade. A family-based phylogenetic classi- toid clade) is dominated by wood-decaying fication is outlined for the six major clades in previously classified in the artificial families Corti- which 30 families, four autonomous tribes and two ciaceae, Polyporaceae and Stereaceae. The major- informally named clades are recognized. ity of these species cause white rots. No unequiv- N Sugiyama et al: The earliest diverging lineages of ocal morphological synapomorphies are known for the Ascomycota include Neolectomycetes, Pneu- the hymenochaetoid clade. However, almost all mocystidiomycetes, and species examined ultrastructurally have dolipore . These taxa were classified for- septa with continuous . merly in the (5Archiascomy- N Moncalvo et al: The (cantharelloid cetes), and while increased taxon and character clade) includes the genera , Crater- sampling have resulted in increased support, the ellus, Hydnum, Clavulina, Membranomyces, Multi- monophyly of the subphylum is debatable and its clavula, Sistotrema, Botryobasidium,thefamily use remains controversial. Ceratobasidiaceae and possibly Tulasnella. Numer- N Suh et al: Subphylum consists of ous taxa within the clade are characterized by fast a single , Saccharomycetales. Although many molecular evolution, especially rDNA sequences, close relatives of are known which continue to complicate phylogenetic in- from whole genome sequences, few protein-coding ference of this group. gene sequences are available for other species, N Hosaka et al: Phallomycetidae is proposed for the especially basal members of the group. At least 12 gomphoid-phalloid clade, which includes four well clades based on rDNA analyses are strongly supported major subclades. Three of the four supported. subclades (Geastrales, Hysterangiales and Phal- N Spatafora et al: includes the lales) are represented entirely by gastroid taxa. majority of filamentous, sporocarp-producing and While the gastroid morphology is derived from mitosporic or conidial species of Ascomycota. The epigeous, nongastroid taxa (e.g. Ramaria)inthe apothecial classes and Orbiliomy- Gomphales, the topology of the Phallales indicates cetes are supported as being the two most basal that the -like form is an ancestral morphol- taxa of the subphylum. The remaining taxa form ogy of the stinkhorn fruiting bodies. a well supported clade that includes the Arthonio- N Miller et al: The Russulales contains a remarkable mycetes plus , , variety of sporophore forms, including resupinate, plus and Leotio- discoid, effused-reflexed, clavarioid, pileate or mycetes plus . gasteroid. Based on molecular and morphological N Hansen and Pfister: Pezizomycetes comprise all data, 12 families and approximately 80 genera have Ascomycota that form operculate asci with the been identified, although placement of many taxa majority of species forming apothecial ascomata. has not yet been determined. Presence of gloeo- The class includes three well supported subclades, plerous hyphae containing fluid that stains black in all of which are classified currently in the Pezizales. sulfoaldehyde compounds is a synapomorphy for N Schoch et al: Dothideomycetes includes the ma- the Russulales, but amyloid reactions in or jority of bitunicate ascostromatic species, excluding hyphal walls is an inconsistent trait for the order. Chaetothyriales and related taxa. Support for the N Binder and Hibbett: Boletales includes six major monophyly of the class and its sister group lineages recognized at the subordinal level, Bole- relationship with is strengthened tineae, Paxillineae, , Suillineae, by the acquisition of protein coding data, and two Tapinellineae and Coniophorineae. Analyses of new subclasses, Pleosporomycetidae and Dothideo- the multigene dataset confirmed sister group mycetidae, are described. relationships among Boletales, Agaricales and N Geiser et al: Eurotiomycetes includes two sub- Atheliales, and ancestral state reconstruction sug- classes, Eurotiomycetidae and Chaetothyriomyceti- gests that the ancestor of the Boletales was a brown- dae, which collectively include prototunicate, rotting, resupinate or polyporoid, saprotrophic bitunicate and lichenized species. The monophyly basidiomycete. of Eurotiomycetes has been debated, but new data N Matheny et al: Multigene analyses support Agar- provide strong support for the class as defined icales comprising six major clades, the agaricoid, herein and for the inclusion of the in tricholomatoid, marasmioid, hygrophoroid, plu- the Eurotiomycetidae. BLACKWELL ET AL:APHYLOGENY FOR FUNGI 833

N Wang et al: contains the majority of in a phylogenetic context. Members of Opistokontia the inoperculate, apothecial fungi with the excep- (Animalia, Fungi and four allies, including tion of , which is shown to represent Choanoflagellata, Ichthyosporea, a separate origin of the earth tongue morphology. and Corallochytrea, Nuclearia and Ministeria) share Leotiomycetes contains the Helotiales, Rhytisma- an insertion of about 12 amino acids (positions 153– tales, , Cyttariales and , 238) in the EF-1a protein sequence (Baldauf and and proves to be one of the most diverse classes of Palmer 1993). Phylogenetic analysis of four combined Ascomycota with respect to ascomatal morpholo- nuclear protein-coding gene sequences includes gies. opistokont protists as well as basal metazoans and N Zhang et al: Sordariomycetes includes all non- fungi (Amaral- Zettler et al 2001, Medina et al 2003, lichenized perithecial species and related cleis- Steenkamp 2006) and provides evidence that Nucle- tothecial and anamorphic taxa. Multigene analyses aria is the sister taxon of Fungi (Steenkamp 2006). support the recognition of three subclasses (Hy- Furthermore the establishment of the monophyly of pocreomycetidae, Sordariomycetidae and Xylario- Choanoflagellata indicates that these organisms could mycetidae), but placement of additional lineages not have been an ancestor shared by animals and within the class is undetermined. fungi, as has been suggested (Cavalier-Smith 1987). N Miadilkowska et al: Lecanoromycetes includes The data also reject other hypotheses, including most of the -forming fungal species (.13 groupings of plants and fungi (Philip et al 2005), 500). Three subclasses are recognized, including and animals and plants (Lo¨ytynoja and Milinkovitch Acarosporomycetidae, Ostropomycetidae and Le- 2001). canoromycetidae, but support for Lecanoromyce- Cienkowski (1865), who studied a number of tidae is tenuous. Monophyly of several orders and problematic organisms, including species of Amoebi- families is not supported, and traditional use of dium and labyrinthulids, also described Nuclearia. morphology in systematics of the class cannot This is a of amoeboid protists with spherical be applied consistently. bodies and radiating, rigid, filose ; many species form walled cysts (Patterson 1984). These The works described above will have a large impact species are known from freshwater where they ingest on future textbooks and continuously updated Web- based educational materials, which will continue to and might be associated with aquatic animals, increase in importance. Toward this end, Deep including fish. Environmental DNA samples indicate Hypha participants are involved in the Tree of Life that members of the genus also might be present in Project ,http://tolweb.org/tree/., where biological marine environments (Bhattacharya and Oliveira information, including phylogenetic trees, soon will 2000). Are we close to inferring the morphology of be available for each of the major fungal taxa ‘‘first fungus’’? If Steenkamp and colleagues (2006) discussed in this issue of Mycologia. are correct, we are getting close. One superficial problem however is the absence of a flagellum in Work remaining.—The base of the tree and the Nuclearia, an apparent loss such as the one that has bare branches. Questions about the base of the fungal occurred within the main fungal lineage, or could the tree remain, but fungi usually have been proposed to flagellum be present in an unconnected missing have a close relationship with animals (Baldauf et al morphological state? Both possibilities were sug- 2000, Baldauf 2003, Baldauf and Palmer 1993, Embley gested. and Martin 2006, Keeling 2003, Keeling et al 2000, Fast The branch tips of the current tree are fairly bare and Keeling 2005, Phillipe et al 2004, Ragan et al 1996, and many taxa remain to be discovered and included Steenkamp et al 2006, Wainright et al 1993), although in analyses. If the conservative estimate of 1 500 000 the details of the basal radiation are not clear. When fungal taxa is used, as it continues to be, less than Deep Hypha began the major questions included: Is a 10th of the taxa in the kingdom have been a choanoflagellate ancestor for fungi well supported? discovered (Hawksworth 2004). Many of these taxa Where is the origin of DAP lysine biosynthesis in the will come from field studies. Fungi from rapid fungal ancestry? Can character evolution (flagella, radiations into a multitude of habitats continue to hyphae, etc.) be traced? Can we infer the general be discovered in large numbers in geographically morphology of ‘‘first fungus’’? Are microsporidians distant localities or undercollected hidden habitats fungi or merely closely related organisms? (Arnold et al 2001, Suh et al 2004, Vanderkoornhuyse Five years later these questions are only partially et al 2002). Other taxa from previously described all answered, largely because of long branches and inclusive taxa, especially those with few distinctive incomplete taxon sampling. In addition, studies of morphological traits, will be dissected out as cryptic physiology and biochemistry have not been addressed taxa (Blackwell and Jones 1997, Fisher et al 2002, 834 MYCOLOGIA

FIG 1. Phylogenetic tree diagram of members of kingdom Fungi. This tree is based on the phylogenetic studies of a number of mycologists. The project was originated by AFTOL and represents a first effort to provide an ordinal level phylogenetic classification to be used by all mycological publications. An expanded discussion of the classification is in preparation and will be published elsewhere. The most recent and archived earlier versions can be accessed at ,http:// www.clarku.edu/faculty/dhibbett/AFTOL/AFTOL.htm.. Also see the site for rules used in its construction. BLACKWELL ET AL:APHYLOGENY FOR FUNGI 835

Kurtzman 2003). One other way we are increasing ———, Mims CW. 1979. Introductory Mycology. New York: numbers of taxa is by applying phylogenetic species John Wiley & Sons. concepts. Use of this concept results in a better ———, ———, Blackwell M. 1996. Introductory Mycology. understanding of the biology of organisms, including New York: John Wiley & Sons. 869 p. Amaral-Zettler LA, Nerad TA, O’Kelly CJ, Sogin ML. 2001. dispersal and geographical and host relations (Cassar The nucleariid amoebae: more protists at the - and Blackwell 1996, Moncalvo 2005, Taylor et al fungal boundary. J Euk Microbiol 48:293–297. 2000). Arnold AE, Maynard Z, Gilbert GS. 2001. Fungal endo- phytes in dicotyledonous neotropical trees: patterns of Classification.—The goal of synthesizing a uniform abundance and diversity. Mycol Res 105:1502–1507. classification for kingdom Fungi was initiated at the Baldauf SL. 2003. The deep roots of . Science Deep Hypha Arizona 2004 meeting and was designed 300:1703–1706. as a collaborative effort with a number of mycolo- ———, Palmer JD. 1993. Animal and fungi are each other’s gists. The authors of the Dictionary of the Fungi, closest relatives: congruent evidence from multiple individual authors of pages of the Tree of Life Web proteins. Proc Natl Acad Sci USA 90:11558–11562. Project, the anticipated revision of the Alexopoulos ———, Roger AJ, Wenk-Siefert I, Doolittle WF. 2000. textbook, GenBank and Myconet (www.fieldmuseum. A kingdom-level phylogeny of eukaryotes based on org/myconet/) have agreed to use the classification. combined protein data. Science 290:972–977. Barr DJS. 1992. Evolution and kingdoms of organisms from Many of the naming conventions applied to the the perspective of a mycologist. Mycologia 84:1–11. classification of all fungi were those of Eriksson for Bhattacharya D, Oliveira MC. 2000. The SSU rDNA coding Myconet. The overall goal of the classification was to region of a filose contains a Group I Intron produce a higher level phylogenetic classification of lacking the universally conserved G at the 39-terminus. the Fungi by naming well supported clades. To do so, J Eukaryot Microbiol 47:585–589. available higher level names sanctioned by the Blackwell M, Jones KG. 1997. Taxonomic diversity and International Code of Botanical Nomenclature are interactions of insect-associated ascomycetes. Biodiver employed for as many well supported clades as Conserv 6:689–699. possible, and these names are used more consistently Bowman BH, Taylor JW, Brownlee AG, Lee J, Lu S-D, White across the major phyla of Fungi (e.g. Ascomycota and TJ. 1992. Molecular evolution of the fungi: relationship of the Basidiomycetes, Ascomycetes and Chytridiomy- Basidiomycota). The tree diagram (FIG. 1) is based on cetes. Mol Biol Evol 9:285–296. this classification and represents a working or draft Bruns TD, Vilgalys R, Barns SM, Gonzalez D, Hibbett DS, consensus classification of the Fungi. A more com- Lane DJ, Simon L, Stickel S, Szaro TM, Weisburg WG, plete classification is in preparation and will be Sogin ML. 1992. Evolutionary relationships within the published as a multi-authored manuscript (http://www. Fungi: analyses of nuclear small subunit rRNA se- clarku.edu/faculty/dhibbett/AFTOL/AFTOL.htm). quences. Mol Phylogen Evol 1:231–241. The classification presented here (FIG.1)canbeusedas Cassar SC, Blackwell M. 1996. Non-monophyly of ambrosia a guide to the groups discussed in this issue with the fungi in Ambrosiella. Mycologia 88:596–601. goal of producing a stable higher-level phylogenetic Cavalier-Smith T. 1987. The origin of fungi and pseudo- classification of Fungi. fungi. In: Rayner ADM, Brasier CM, Moore D., eds. Evolutionary biology of fungi. Cambridge: Cambridge University Press. p 339–353. Cienkowski L. 1865. Beitra¨ge zur Kenntnis der Monaden. ACKNOWLEDGMENTS Ark Microsk Anat I:203–232. Pls. 12–14. We thank all our collaborators who participated in the Deep Embley TM, Martin W. 2006. Eukaryotic evolution, changes Hypha project. We acknowledge financing from the and challenges. Nature 440:623–630. National Science Foundation (Research Coordination Net- Fast NM, Keeling PJ. 2005. The fungal roots of microspo- ridian parasites. In: Vega FE, Blackwell M., eds. Insect- works in Biological Sciences: a phylogeny for Kingdom fungal associations. New York: Oxford Press. p 97–118. Fungi, NSF- 0090301 to M. Blackwell, J.W. Spatafora and Fischer MC, Koenig GL, White TJ, Taylor JW. 2002. J.W. Taylor. We appreciate the commitment of James E. Molecular and phenotypic description of Rodman to promote systematics and encourage mycology posadasii sp. nov., previously recognized as the non- for the past 25 y. We dedicate this paper to him. California population of . Mycolo- gia 94:73–84. LITERATURE CITED Hawksworth DL. 2004. Fungal diversity and its implications for genetic resource collections. Stud Mycol 50:9–18. Alexopoulos CJ. 1952. Introductory Mycology. New York: ———, Kirk PM, Sutton BC, Pegler DM. 1995. Ainsworth & John Wiley & Sons. Bisby’s dictionary of the fungi. 8th ed. Egham: CAB ———. 1962. Introductory Mycology. New York: John Wiley International. 616 p. & Sons. James TY, Porter D, Leander CA, Vilgalys R, Longcore JE. 836 MYCOLOGIA

2000. Molecular phylogenetics of the Chytridiomycota phylogenic groups and fungal species concepts. In: Xu supports the utility of ultrastructural data in chytrid JP, ed. Evolutionary genetics of Fungi. Norfolk: systematics. Can J Bot 78:336–350. Horizon Scientific Press. p 1–33. ———, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox Nagahama T, Sato H, Shimazu M, Sugiyama J. 1995. CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Phylogenetic divergence of the entomophthoralean Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, fungi: evidence from nuclear 18S ribosomal RNA gene Stajich JE, Hosaka K, Sung G-H, Johnson D, O’Rourke sequences. Mycologia 87:203–209. B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Nishida H, Sygiyama J. 1994. Archiascomycetes: detection of Wilson AW, Schu¨ßler A, Longcore JE, O’Donnell K, a major new lineage within the ascomycota. My- Mozley-Standridge S, Porter D, Letcher PM, Powell coscience 35:361–366. MJ, Taylor JW, White MM, Griffith GW, Davies DR, Patterson DJ. 1984. The genus Nuclearia (Sarcodina, Humber RA, Morton JB, Sugiyama J, Rossman AY, Filosea) species composition and diagnoses of the taxa. Rogers JD, Pfister DH, Hewitt D, Hansen K, Ham- Arch Protistenkd 128:127–139. bleton S, Shoemaker RA, Kohlmeyer J, Volkmann- Philip GK, Creevey CF, McInerney JO. 2005. The Opistho- Kohlmeyer B, Spotts RA, Serdani M, Crous PW, konta and the Ecdysozoa may not be clades: stronger Hughes KW, Matsuura K, Langer E, Langer G, support for the grouping of plant and animal than for Untereiner WA, Lu¨cking R, Bu¨del B, Geiser DM, animal and fungi and stronger support for the Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Coelomata than Ecdysozoa. Mol Biol Evol 22:1175– Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora 1184. JW, Vilgalys R. 2006. Reconstructing the early evolution Philippe H, Snell EA, Bapteste E, Lopez P, Holland PWH, of Fungi using a six-gene phylogeny. Nature 443:818– Casane D. 2004. Phylogenomics of eukaryotes: impact 822. of missing data on large alignments. Mol Biol Evol 21: Keeling PJ. 2003. Congruent evidence from a-tubulin and b- 1740–1752. tubulin gene phylogenies for a zygomycete origin of Ragan MA, Goggin CL, Cawthorn RJ, Cerenius L, Jamieson . Fungal Genet Biol 38:298–309. AVC, Plourd SM, Rand TG, Soderhall K, Gutell RR. ———, Luker MA, Palmer JD. 2000. Evidence from beta- 1996. A novel clade of protistan parasites near the tubulin phylogeny that microsporidia evolved from animal-fungal divergence. Proc Natl Acad Sci USA 93: within the fungi. Mol Biol Evol 17:23–31. 11907–11912. Kurtzman CP. 2003. Phylogenetic circumscription of Redecker D, Morton JB, Bruns TD. 2000. Ancestral lineages Saccharomyces, Kluyveromyces and other members of of arbuscular mycorrhizal fungi (Glomales). Mol the Saccharomycetaceae, and the proposal of the new Phylogenet Evol 14:276–284. genera Lachancea, Nakaseomyces, Naumovia, Vander- Schu¨ßler A, Scwarzott D, Walker C. 2001. A new fungal waltozyma and Zygotorulaspora.. FEMS Res 4:233– phylum, the Glomeromycota: phylogeny and evolution. 245. Mycol Res 105:1414–1421. Liu Y, Whelen S, Hall BD. 1999. Phylogenetic relationships Simon L, Bousquet L, Levesque RC, Lalonde M. 1993. among ascomycetes: evidence from an RNA polymerase Origin and diversification of endomycorrhizal fungi II subunit. Mol Biol Evol 16:1799–1808. and coincidence with vascular plants. Nature 363:67– Lo¨ytynoja A, Milinkovitch MC. 2001. Molecular phylogenet- 69. ic analysis of the mitochondrial ADP-ATP carriers: the Steenkamp ET, Wright J, Baldauf SL. 2006. The protistan Plantae/Fungi/Metazoa trichotomy revisited. Proc Natl origins of animals and fungi. Mol Biol Evol 23:93–106. Acad Sci USA 98:10202–10207. Suh S-O, McHugh JV, Blackwell M. 2004. Expansion of the Lutzoni F, Kauff F, Cox CJ, McLaughlin D, Celio G, Candida tanzawaensis yeast clade: 16 novel Candida Dentinger B, Padamsee M, Hibbett D, James TY, species from basidiocarp-feeding beetles. Int J Syst Evol Baloch E, Grube M, Reeb V, Hofstetter V, Schoch C, Microbiol 54:2409–2429. Arnold AE, Miadlikowska J, Spatafora J, Johnson D, Swann EC, Taylor JW. 1995. Phylogenetic perspectives on Hambleton S, Crockett M, Shoemaker R, Hambleton S, basidiomycete systematics: evidence from the 18S rRNA Crockett M, Shoemaker R, Sung GH, Lucking R, gene. Can J Bot 73:S862–S868. Lumbsch T, O’Donnell K, Binder M, Diederich P, Ertz Taylor JW. 1995. Making the Deuteromycota redundant: D, Gueidan C, Hansen K, Harris RC, Hosaka K, Lim a practical integration of mitosporic and meiosporic YW, Matheny B, Nishida H, Pfister D, Rogers J, fungi. Can J Bot 73S:S754–S759. Rossman A, Schmitt I, Sipman H, Stone J, Sugiyama J, ———, Bowman B, Berbee ML, White TJ. 1993. Fungal Yahr R, Vilgalys R. 2004. Assembling the Fungal Tree of model organisms: phylogenetics of Saccharomyces, Life: progress, classification and evolution of subcellu- and Neurospora. System Biol 42:440–457. lar traits. Am J Bot 91:1446–1480. ———, Jacobson DJ, Fisher MC. 1999. The evolution of Medina M, Collins AG, Taylor JW, Valentine JW, Lipps JH, asexual fungi: reproduction, speciation and classifica- Amaral-Zettler L, Sogin ML. 2003. Phylogeny of tion. An Rev Phytopathol 37:197–246. Opisthokonta and the evolution of multicellularity ———, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, and complexity in Fungi and Metazoa. Int J Astrobiol Hibbett DS, Fisher MC. 2000. Phylogenetic species 2:203–211. recognition and concepts in Fungi. Fungal Genet Biol Moncalvo J-M. 2005. Molecular systematics: major fungal 31:21–32. BLACKWELL ET AL:APHYLOGENY FOR FUNGI 837

Taylor TN, Remy W, Hass H, Kerp H. 1995. Fossil arbuscular Wainwright PO, Hinkle G, Sogin ML, Stickel SK. 1993. mycorrhizae from the lower Devonian. Mycologia 87: Monophyletic origins of the Metazoa: an evolu- 560–573. tionary link with the Fungi. Science 260:340– Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, 342. Young JPJW. 2002. Extensive fungal diversity in plant Wells K. 1994. Jelly fungi, then and now! Mycologia 86:18– roots. Science 295:2051. 48.