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Sequencing the Fungal Tree of Life

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Sequencing the Fungal Tree of Life New 818 Forum Letters Phytologist Letters fungi whose genomes have been sequenced are residents of Sequencing the fungal tree soil and plants (Martinez et al., 2004, 2009; Martin et al., of life 2008, 2010; Ohm et al., 2010; Spanu et al., 2010; Stajich et al., 2010) and these sequences will provide baseline genomic information that enables scientists to explore Terrestrial ecosystems host a complex array of interacting the genomes and functions of thousands of soil fungal communities, with thousands of species of animals, plants, species that cannot be cultured and sequenced directly. fungi and bacteria. In soils, this complex web of life is Unfortunately, reference fungal genomes sequenced to date, responsible for the cycling of carbon (C), for water and and those in progress, show significant bias towards fungi of nutrients, for soil quality and for plant nutrition and health. medical importance (Cuomo & Birren, 2010). The avail- To predict future changes of these threatened ecosystems ability of genome sequences from ecologically and and to fully grasp the biological and chemical workings of taxonomically diverse fungi not only would allow ongoing these complex interactions, one must not only regard organ- research on those species, but enhances the value of other isms as individuals but also as members of a larger sequences through comparative studies of gene evolution, community, considering the interplay and communication genome structure, metabolic and regulatory pathways, and between individuals within these entangled populations, saprotrophism ⁄ symbiosis ⁄ pathogenesis lifestyles. Recently, that is, their extended phenotype (Whitham et al., 2008). the US Department of Energy Joint Genome Institute (JGI) One emerging model for such studies is the interaction launched the Fungal Genomics Program (FGP), aimed at between soil-borne fungi and plant communities. exploration of fungal diversity for energy and environmental Fungi are one of the largest and most diverse kingdoms sciences and applications through the scale-up of sequencing of eukaryotes and function as important biological compo- and analysis (Grigoriev et al., 2011). nents of all terrestrial ecosystems. They are central to the global C cycle, constitute the major group of plant patho- Fungal genomics for energy and environment gens in managed and natural ecosystems, serve as symbionts with heterotrophic and autotrophic organisms alike, and The Genomic Encyclopedia of Fungi of the JGI FGP play an integral and growing role in the development and (http://www.jgi.doe.gov/fungi) targets fungal genomes in production of renewable bio-based fuels and chemicals. The three areas: plant health, biorefinery and fungal diversity. success and importance of fungi to life on Earth are directly Plant health depends on interactions of the plant with both attributable to the remarkable diversity of enzymes and fungal mutualists and parasites. While on the surface, the metabolites that they produce, which afford them a broad effects of both on a host are orthogonal; they may share range of nutritional modes and grant them access to an common characteristics to escape the plant defense system amazing breadth of C sources and ecological niches. and acquire host nutrients (e.g. the role of effector-like Understanding how saprotrophic, symbiotic and patho- secreted proteins in Laccaria bicolor and in Melampsora genic fungi achieve their lifestyle is crucial for understanding larici-populina), live within the host (e.g. the semibiotroph their ecological functions and their subsequent impact on Mycosphaerella graminicola) and balance between saprobic the fate of plant communities. The inconspicuous nature of and parasitic (or mutualistic) lifestyles (e.g. Heterobasidion soil fungi, the inaccessibility of their habitats and our inabil- annosum). Comparative genomics should lead us to under- ity to culture many of them have made them difficult to stand these mechanisms critical for sustainable growth of study. Advances in large-scale DNA barcoding surveys have forest trees and bioenergy feedstocks, such as poplars, pines circumvented some of these limitations and allowed us to and eucalypts. Biorefinery includes industrial hosts such as determine the composition and the dynamics of several fun- Trichoderma reesei and Aspergillus niger. Novel ‘modules’ or gal soil communities, including mycorrhizal fungi (Bue´e ‘parts’ – metabolic processes, enzymes and regulatory et al., 2009; O¨ pik et al., 2009; Jumpponen et al., 2010). elements with desired properties from other fungi – will be Several hundred species are active in soils, and ongoing me- plugged into these established hosts to accelerate the tagenomics and metatranscriptomics studies will uncover development of new bioprocesses that efficiently convert the functions encoded in their genomes as well as their biomass into biofuels and renewable chemicals. Finally, expressed transcripts (Martin & Martin, 2010). Many of the exploration of fungal ecological and phylogenetic diversity New Phytologist (2011) 190: 818–821 Ó 2011 The Authors www.newphytologist.com New Phytologist Ó 2011 New Phytologist Trust New Phytologist Letters Forum 819 should bring us more useful ‘modules’ or ‘parts’, such as the first year. Five of the first-tier species represent major thermostable enzymes or thermotolerant hosts from clades of Agaricomycotina that include widespread wood- extreme environments, as well as provide clues on fungal decay species for which there are currently no published evolution. Dramatic improvements in genome-sequencing genomes or (to our knowledge) active genome projects technologies enable us to go beyond sequencing a single ref- (i.e. Auriculariales, Dacrymycetales, Hymenochaetales and erence genome, allowing ‘resequencing’ of several accessions Corticiales). The second-tier species further broaden the (e.g. resequencing of a dozen strains of the ectomycorrhizal phylogenetic diversity of wood-decay genomes (including model species L. bicolor). Through comparative analysis of the as-yet unsampled Atheliales, Amylocorticiales, Jaapiales gene expression, genomic variation across the diversity of and Phallomycetidae). Comparative analyses of these anno- fungi and metagenomics of complex systems, such as soil, tated genomes will also integrate gene-expression profiles we will reach a higher level of understanding of fungal life- determined by high-throughput Illumina RNA-Seq and styles, their interactions with plants and their evolution, by protein mass spectrometry from 12 fungal species. The laying a strong foundation upon which to build practical genome sequence is already available for five species applications for energy and environment. (P. chrysosporium, P. placenta, Pleurotus ostreatus, Serpula lacrymans and H. annosum) and, for the other seven Sequencing saprotrophic Agaricomycotina (Gloeophyllum trabeum, Fistulina hepatica, Fomitiporia mediterranea, Dacryopinax spathularia, Fomitopsis pinicola, Diverse fungi obtain nutrition from primary plant tissues, Auricularia auricular-judae and Punctularia strigosozonata), exudates or phloem sap, but only a relatively small number the genome sequence will be produced in the saprotrophic are able to efficiently degrade wood. The majority of Agaricomycotina project, as already described. Comparative the wood-decaying fungi are in the Agaricomycotina whole-transcriptome analyses of different decayer types and (Basidiomycota), which also includes mycorrhizal and path- clades will facilitate the long-range understanding of their ogenic forms. Within the Agaricomycotina, a polyphyletic biological lifestyles and lignocellulolytic strategies. assemblage, known as white-rot fungi, have the unique abil- ity to depolymerize and mineralize the recalcitrant lignin in Sequencing mycorrhizal genomes order to gain access to cell wall carbohydrates as C and energy sources. Another assemblage, the so-called brown- In soils of most forests, hundreds of species of ecto- rot fungi, rapidly depolymerize cellulose but do not exten- mycorrhizal fungi establish mutualistic symbioses with sively degrade the lignin, which remains in situ as a lateral roots of trees (Bue´e et al., 2009; Martin & Nehls, modified polymeric residue that is highly resistant to further 2009). Genomic-based analyses of the ectomycorrhizal sym- microbial decay. Both types of wood-decay fungi are com- biosis in environmental settings are in their infancy (Courty mon inhabitants of forest ecosystems and play an et al., 2008), but research in environmental genomics is rap- important, if not pivotal, role in the C cycle. idly developing and is crucial for understanding the role of The genomes of three wood-decaying Agaricomycotina – the mycorrhizal symbiosis in nutrient cycling and plant Phanerochaete chrysosporium, Postia placenta and Schizophyllum health. One key step for the future of mycorrhizal research is commune – have been published (Martinez et al., 2004, the production of additional sequenced genomes, both for a 2009; Ohm et al., 2010). P. chrysosporium produces a white variety of mycorrhizal fungi and also for their plant hosts. rot whereas P. placenta is a brown-rot species. They are To date, the genomes of two symbionts – the basidiomycete both members of the Polyporales, but were found to L. bicolor (Martin et al., 2008) and the ascomycete Tuber have radically different decay chemistries. For example, melanosporum (Martin et al., 2010) – have been sequenced. Phanerochaete has 15 genes encoding class II fungal peroxid- Based on their
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