Mushrooms: Morphological Complexity in the Fungi
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COMMENTARY Mushrooms: Morphological complexity in the fungi John W. Taylor1 and Christopher E. Ellison Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720 he PNAS paper by Stajich et al. Arabidopsis (1) describes a superbly assem- rice bled and annotated genome of Puccinia graminis T Independent Uslago maydis one of the most morphologically complex fungi, the “inky cap” mushroom origins of complex Basidiomycota Cryptococcus neoformans Coprinopsis cinerea, and illustrates the ac- mulcellularity Phanerochaete chrysosporium complishments that can be made when Coprinopsis cinerea working with a genetic model organism Laccaria lacata and the challenges that lie ahead if we Schizosaccharomyces pombe Ascomycota Saccharomyces cerevisiae are to truly understand how genomes re- Candida glabrata late to the evolution of organism com- Yarrowia lipolyca plexity (Fig. 1). Tuber melanosporum Plants and animals may be the first to Fusarium graminearum come to mind when thoughts turn to the Magnaporthe grisea evolution of complexity, but within the Neurospora crassa fungi, there is an amazing amount of Coccidioides immis morphological diversity, from unicellular Aspergillus nidulans yeasts to large “fruiting bodies” capable of Rhizopus arrhizus producing trillions of spores (2). That di- sponge versity, and the relatively small genomes of fish this group, have helped create the most chicken comprehensive set of whole-genome se- human quences for any major Eukaryotic lineage fruit fly mosquito in both the number and phylogenetic nematode breadth of taxon sampling. Furthermore, collar flagellate the high incidence of convergent evolution of similar forms creates an ideal system for using phylogenomic comparative me- 1250 1000 750 500 250 0 thods to study the evolution of develop- Millions of years ment within the fungi. However, given Fig. 1. Bayesian relaxed clock tree based on amino acid sequence for 50 loci and linked to the fossil record the wealth of fungal genomes, fungal evo- at four divergences (20). Current hypotheses on the origin of complex, multicellular organisms are marked devo is in its infancy, because most of the in orange. Comparison of Copriniopsis with Basidiomycota macrofungi Laccaria or Phanerochaete, or with fungi with well-assembled and annotated Ascomycota macrofungus Tuber, could reveal commonalities associated with complex multicellularity. If genomes are unicellular (3). Enter C. cin- microfungi that are complex and multicellular share these commonalities, useful comparisons could in- erea, which develops into a macroscopic clude Ascomycota on the clade that contains Neurospora and Aspergillus [Reproduced with permission from ref. 20 (Copyright 2010, Elsevier)]. mushroom and is well-characterized genetically. Stajich et al. (1) assembled the 36-Mb teny between C. cinerea and another worms (4) and other fungi, such as yeast genome sequence of C. cinerea into 13 mushroom-producing fungus, Laccaria (5), Candida (6), and fission yeast (7). chromosomes, 9 of which include both The picture that has emerged is of a highly fi lacata,withwhichC. cinerea shared an telomeres, and identi ed centromeres by ancestor some 200 Ma, is recognizable dynamic genome where chromosomal re- their high concentration of retrotrans- over 40% of the genome. The estimate of gions frequently duplicate, and those rare posons. Annotation was improved by ac- the rate of genome rearrangement be- duplications that facilitate adaptation cess to expressed sequence tags (EST) and tween these fungi is 3-fold higher than are retained (8), with a bias toward sub- serial analysis of gene expression (SAGE) that seen in Saccharomyces,andishigh, telomeric regions. It is a generality that can data. Comparison of the physical chro- in general, for Eukaryotes. Stajich et al. be extended to the bacteria, where ge- mosome to a genetic map that covered nomes can be sorted into stable regions, 86% of the genome allowed the authors to (1) also discovered several blocks of syn- teny that are much larger than expected with genes coding for core activities, and observe that recombination varies along dynamic regions, where selfish elements if rearrangements occur randomly, sug- the chromosomes and that the highest and genes responsible for local adaptation gesting that gene order in these regions is rates are achieved within their distal 15%. are more likely to be found (9, 10). In regions of low recombination, retro- being conserved by purifying selection. In A product of the dynamic genome, transposons, which outnumber DNA these large blocks, genes are unusually which has been implicated as a means transposons 10:1, are missing. Genes closely packed; genes with core, eukary- of rapid adaptation, is change in gene unique to C. cinerea, as well as single-copy otic functions are common; the density of genes, are more abundant, whereas genes transcription factors is elevated; and with paralogs are rare. In chromosomal transposons are absent. In almost all of Author contributions: J.W.T. and C.E.E. wrote the paper. regions where recombination is high, these attributes, C. cinerea is like other The authors declare no conflict of interest. multigene families are younger and tend eukaryotes where well-assembled and See companion article on page 11889. to be tandemly oriented compared with annotated genomes have been analyzed 1To whom correspondence should be addressed. E-mail: areas where recombination is low. Syn- with access to good genetic data, e.g., [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1006430107 PNAS Early Edition | 1of2 Downloaded by guest on October 2, 2021 family size (11), and Stajich et al. (1) have Coprinopsis researchers to test hypotheses complex reproductive structures known as identified three examples: genes with about FunK1 kinases, p450 genes, and truffles, Tuber (Ascomycota) (15), might protein kinase domains, p450 genes, and hydrophobins. Another tack is to generate separate multicellular development from hydrophobins (proteins that facilitate de- more hypotheses, and can there be a bet- nutritional mode, as might comparison of velopment in an environment where sur- ter hypothesis generator than comparative macroscopic Basidiomycota and Ascomy- face tension is the dominant force) (12). In genomics? Which comparisons might be cota, which cause plant disease (e.g., Ar- C. cinerea, there are 380 genes with pro- most informative? If mushroom producers millaria and Sclerotinia). tein kinase domains, including many not Between fungi that produce large re- found in yeast and some previously found Within the fungi, there productive structures (e.g., mushrooms and only in animals. The largest such family truffles) and those that make no repro- contains the FunK1 domain, which is is an amazing amount ductive structures apart from the meiocytes found in complex Basidiomycota and As- themselves (e.g., yeasts) lie most species of comycota and is absent in other fungi. of morphological the higher fungi [e.g., Neurospora (16), Almost one half, 59, of the proteins with Aspergillus (17), Coccidioides (18), Fusa- this domain are packed into one sub- diversity. rium, and the lichenized fungi]. If size does telomeric region of one chromosome. A not matter, and the developmental com- reasonable hypothesis is that FunK1 do- plexity and tissue differentiation seen in mains are important to the development have common genome features, compari- these microscopic fungi reflect that seen in of complex, multicellular fungi and that son of C. cinerea to other macroscopic mushrooms and truffles, comparison of selection has been involved in retaining Basidiomycota, e.g., Phanerochaete (13) genetically tractable species with C. cinerea these genes over numerous, tandem gene or Laccaria (14), would be useful. How- duplications. Other similar and equally ever, each of these fungi has a different and relatives should also pay dividends. A reasonable hypotheses could be framed approach to nutrition (living and repro- pair of membranous organelles worth in- for the P450 and hydrophobin genes. ducing in dung, wood, or the roots of living vestigating might be the Woronin body of However, despite significant advances plants, respectively), and this diversity Ascomycota and the septal pore complex related to the mechanisms of genome could confound comparisons aimed only of Basidiomycota, which function to seal evolution that emerged from this analysis at the development of morphological damaged hyphae and might have been in- of the C. cinerea genome, the goal of complexity. In this regard, comparison strumental in allowing fungi to make com- understanding, with confidence, the ge- of C. cinerea with other dung fungi that plex, multicellular structures (19). Making nomic basis of developmental complexity are complex and multicellular, e.g., the the comparisons suggested herein, most remains elusive. complex dung fungus Ascobolus (Asco- of which can be attempted with existing What, then, will it take to understand mycota) and the simple dung fungus Phy- genome assemblies, might not only unravel the genome evolution that led to mush- comyces (Mucoromycota), might control the basis of fungal complexity, but point the rooms and other complex, fungal fruiting for nutritional adaptation. Similarly, com- way for studies of plants and animals, as bodies? One tack, surely, is to use the parison of Laccaria lacata with another more of the much larger genomes found in molecular biological tools available to mycorrhizal fungus, one that makes the those kingdoms