Fungal Systematics: Is a New Age of Enlightenment at Hand?
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PERSPECTIVES Nomenclature for Algae, Fungi, and Plants ESSAY (ICN). To many scientists, these may seem like overdue, common-sense measures, but Fungal systematics: is a new age to some fungal taxonomists, the changes were seismic11. of enlightenment at hand? In the long run, a unitary nomenclature system for pleomorphic fungi, along with the other changes, will promote effective David S. Hibbett and John W. Taylor communication. In the short term, however, Abstract | Fungal taxonomists pursue a seemingly impossible quest: to discover the abandonment of dual nomenclature will require mycologists to work together and give names to all of the world’s mushrooms, moulds and yeasts. Taxonomists to resolve the correct names for large num‑ have a reputation for being traditionalists, but as we outline here, the community bers of fungi, including many economically has recently embraced the modernization of its nomenclatural rules by discarding important pathogens and industrial organ‑ the requirement for Latin descriptions, endorsing electronic publication and isms. Here, we consider the opportunities ending the dual system of nomenclature, which used different names for the sexual and challenges posed by the repeal of dual nomenclature and the parallels and con‑ and asexual phases of pleomorphic species. The next, and more difficult, step will trasts between nomenclatural practices for be to develop community standards for sequence-based classification. fungi and prokaryotes. We also explore the options for fungal taxonomy based on Taxonomists create the language of bio‑ efforts to classify taxa that are discovered environmental sequences and ask whether diversity, enabling communication about through metagenomics5. sequence-based taxonomy can be reconciled different organisms among basic and In the lead‑up to the last IBC in July with the ICN. applied scientists, educators, students and 2011, a vocal and well-organized group of the general public. This essential work is mycologists launched a ‘One fungus, one One name, one fungus particularly challenging in hyperdiverse name’ campaign aimed at ending the system The dual nomenclature system for pleomor‑ and morphologically cryptic groups, such of dual nomenclature. The movement culmi‑ phic fungal species arose in the nineteenth as the kingdom Fungi. Roughly 100,000 nated in the publication of ‘The Amsterdam century, influenced by the use of sexual species of fungi are accepted in the current declaration on fungal nomenclature’ (by morphology in the Linnaean classification taxonomy1, but more than 400,000 fun‑ 88 co-authors from 26 countries)4, which of plants12,13. Despite the fact that is illogi‑ gal species names — including numerous suggested that if dual nomenclature were cal to assign multiple names to one species, synonyms — are recorded in the literature, retained in the botanical code, it might be the dual nomenclature system persisted, and it is likely that millions of new species2 necessary to create a separate MycoCode for in part because the morphology of sexual still await description. Thus, the challenge the kingdom Fungi6. Independently, some reproductive structures was assumed to be for modern fungal taxonomy is to weed out mycologists had already begun to publish superior to that of asexual forms for infer‑ redundant published names while accelerat‑ new fungal names that ignored reproductive ring the evolutionary relationships of fungi14. ing the naming of newly discovered species. morphology, putting sexual and asexual spe‑ However, sexual characteristics lost their To regulate the naming of fungi, mycologists cies in the same genus and thus deliberately pre-eminence for classifying fungi in the adhere to the International Code of Botanical disregarding the code7–9. Facing nomenclatu‑ late 1980s, when PCR made DNA variation Nomenclature3. The code provides stability ral disobedience and the threat of secession, accessible to systematic mycologists. More to a potentially chaotic discipline, but it is the Nomenclature Section of the 2011 IBC than 20 years later, the dual nomenclature updated only once every 7 years and only voted to abolish the dual system of fungal system was finally abolished. at meetings of the Nomenclature Section nomenclature10,11. At the same time, and in As is always the case, the hard work during the International Botanical Congress response to pressure from other activists, begins after the revolution. For mycologists, (IBC), which makes the code slow to adapt the Nomenclature Section also voted to this means choosing names for thousands of to modern practices in systematics. The eliminate Latin descriptions (English will pleomorphic fungal species. Some choices fungal elements of the code that have been now suffice), to allow the publication of will be difficult. For example, the anamor‑ criticized as archaic include the dual system new names in online-only journals (previ‑ phic genus Penicillium (with teleomorphic of nomenclature4, which creates different ously, print was required) and to require genera Eupenicillium and Talaromyces) names for the anamorphs (asexual forms) registration of new fungal names in a pub‑ contains fungi as important as Penicillium and teleomorphs (sexual forms) of the same lically accessible database such as Index rubens (the original source of penicillin), species (FIG. 1), and the requirement for Fungorum or MycoBank10. Finally, the code Penicillium marneffei (the causative agent physical type specimens, which complicates itself was renamed the International Code of of an AIDS-defining disease in Thailand), NATURE REVIEWS | MICROBIOLOGY VOLUME 11 | FEBRUARY 2013 | 129 © 2013 Macmillan Publishers Limited. All rights reserved PERSPECTIVES time, the goal was to begin working through the myriad options for the classification of pleomorphic fungi in light of the new rules. Similar meetings and workshops on the taxonomy of the genus Fusarium, the order Hypocreales and other groups were held in association with meetings of the Mycological Society of Japan (May 2012), the Mycological Society of America (July 2012) and the Mycological Society of China (August, 2012). Classification of environmental sequences Now that dual nomenclature has been abolished, the next major challenge for fungal taxonomy is to develop strategies Figure 1 | Two names, one fungus. Eurotium herbariorum is a pleomorphic fungus that has a sexual Nature Reviews | Microbiology for classifying environmental sequences phase, reproducing by ascospores (the teleomorphic form; left), as well as a conidium-producing (FIG. 2). Nobody knows how many unnamed asexual phase (the anamorphic form; right) that has been named Aspergillus glaucus. Images courtesy species have already been detected through of Paul F. Cannon, Royal Botanical Gardens, Kew, London, UK, and the Centre for Agricultural metagenomic studies (and this fact alone Bioscience International (CABI). indicates the need for a centralized database of species that are based on environmental sequences), but as early as 2007 the number and Penicillium camemberti and Penicillium nomenclatural changes mentioned above of clusters of closely related rRNA genes roqueforti (used to make Camembert and illustrate what might lie ahead. Another being discovered with Sanger chemistry Brie, and Roquefort cheeses, respectively). example is the work of Gräfenhan et al.9 approached the number of species being However, Penicillium spp., as traditionally on the taxonomy of the anamorphic genus described from specimens5, and the rate delimited, are paraphyletic as well as pleo‑ Fusarium, one of the largest genera of fungi, of molecular species discovery has surely morphic, so these well-known species containing nearly 1,500 species, subspecies, increased with the application of next- cannot all remain in this historic genus15. varieties and formae speciales. Fusarium generation sequencing in metagenomics. Under the revised code, any of the exist‑ spp. include important plant and animal Environmental studies have revealed ing valid names for a species can be selected pathogens and mycotoxin producers and not only individual species, but also as its correct name, with preference given to have been linked to as many as seven tele‑ major clades of fungi, such as the class the oldest name. However, this libertarian omorph genera. On the basis of sequence Archaeorhizomycetes17, containing a view is tempered by two additional revi‑ analyses for RNA polymerase II and ATP diverse group of soil-inhabiting fungi from sions, both involving review by the General citrate lyase genes, Gräfenhan et al.9 identi‑ the phylum Ascomycota. Sequences of Committee (GC) of the ICN, which is fied 15 clades with Fusarium-like asexual Archaeorhizomycetes members have been empowered to vote on proposals to conserve forms and gave six of them names based on reported in more than 50 independent stud‑ or reject names of fungal taxa, as well as to anamorphs, although five of these six have ies, and they can be grouped into more than modify the ICN itself 3. First, in situations in known teleomorphic forms. The reclassifica‑ 100 species-level entities17. Nevertheless, which both the anamorph and teleomorph tion of Fusarium by Gräfenhan et al. is based only one species, Archaeorhizomyces names for the same taxon are widely used on robust phylogenies and would be nomen‑ finlayi, has been formally described, based — for example, Fusarium (anamorph) and claturally valid under the forthcoming ICN. on a culture that was obtained from coni‑ Gibberella