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The Fungal Tree of Life Genome-Scale Comparative

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The Fungal Tree of Life Genome-Scale Comparative Guy Leonard & Thomas A. Richards Genome-scale comparative analysis of: Guy Leonard & Thomas A. Richards @guyleonard Synapomorphies To investigate the fidelity of gene fusion characters, we developed an approach for identifying A shared, derived character is used as a cladistic device, differentially distributed gene fusions among whole-genome datasets: fdfBLAST. grouping individual taxa or groups of taxa together into specific clades. Applying this tool to the Fungi, we identified 63 gene fusions present in two or more genomes. Using a combination of phylogenetic and comparative genomic analyses, A B A we then investigated the evolution of these genes across 115 The Fungal Tree of Life C fungal genomes, testing 36 C 12 Phanerochaete chrysosporium each gene fusion for 56 Phanerochaete carnosa A Accounting for these considerable sources of homoplasy, we identified 12 Phlebiopsis gigantea evidence of 16 31 12 36 Bjerkandera adusta B fusion characters that provide support for multiple nodes in the phylogeny 12 36 Phlebia brevispora 16 Fomitopsis pinicola A homoplasy, 32B 14 Postia placenta of the Fungi, including relationships within the deeply derived flagellum-forming 49 Agaricomycotina 12 Ceriporiopsis subvermispora B including gene 16 Wolfiporia cocos Agaricomycetes fungi (i.e. the chytrids) 32A 13 Ganoderma sp. B C Dichomitus squalens C 16 Basidiomycota fission, convergence, 32A 49 Trametes versicolor 13 16 49 8 12 16 12 Stereum hirsutum It has been argued that gene fission events occur at a low frequency because 36 Heterobasidion annosum Gene fusions can be used as synapomorphies if they are and horizontal 32B 36 56 38 45 Pleurotus ostreatus 12 15 16 32B 36 56 Laccaria bicolor shown to be stable and monophyletic; thus the root of a tree the process requires multiple simultaneous evolutionary occurances at 31 56 gene transfer. 12 16 31 32B 56 Schizophyllum commune can be excluded from a clade defined by a gene fusion, 36 Gloeophyllum trabeum selectively viable positions within an ORF (1): i) gain of a stop codon, ii) gain 12 16 32B Punctularia strigosozonata allowing phylogenetic relationships to be polarized on a tree. 49 16 32B 45 Fomitiporia mediterranea of a promoter region, and iii) appropriation of a start codon 49 16 12 Serpula lacrymans 13 Coniophora puteana 31 56 Coprinus cinereus * 31 45 38 (Mechanism 1). 36 Agaricus bisporus 15 31 45 Auricularia delicata Gene Fusions 15 Dacryopinax sp. AA novelnovel modemode ofof visualvisual Gene fusions are a hyrbid of two or more Tremella mesenterica 51 57 Cryptococcus neoformans Tremellomycetes previously separate open reading frames (ORFs). Gene fusions, therefore, have been suggested to 15 17 Wallemia sebi perceptionperception inin thethe fungi…fungi… Rhodotorula graminis 1 15 Sporobolomyces roseus Pucciniomycotina Single Gene represent useful tools for polarizing evolutionary 17 Puccinia graminis One gene fusion, consistent with the 9 11 Melampsora laricis-populina Promoter Region Malassezia globosa relationships (1-3). This approach follows the logic that 11 13 5 27 28 29 Ustilago maydis * Ustilaginomycotina monophyly of the Blastocladiomycota Coding Region 14 15 Pyrenophora teres 60 taxa possesing a gene fusion are monophyletic to the 42 55 Pyrenophora tritici-repentis 55 includes a novel hybrid-protein that we 42 55 Alternaria brassicicola Dothideomycetes exclusion of taxa that possess unfused orthologs. 59 Cochliobolus sativus Stop Codon 43 47 55 59 Cochliobolus heterostrophus show functions in the visual perception Start Codon Setosphaeria turcica 48 60 Leptosphaeria maculans and phototaxis of Blastocladiella Gene Fusion Stagonospora nodorum 10 Hysterium pulicare 48 Rhystidhysteron rufulum zoospore. Deletion Event Septoria musiva 3 Septoria populicola Mycosphaerella fijiensis This light perception is accomplished by Dothistroma septosporum Mycosphaerella graminicola the function of a novel gene fusion (BeGC1) of a Baudoinia compniacensis Gene Fissions 40 61 Aspergillus fumigatus Mechanism 1: Fission by Separation Neosartorya fischeri guanylyl cyclase catalytic domain and rhodopsin-like Insertion Event Aspergillus clavatus 40 Aspergillus oryzae 40 domain. Full genome sequencing was used to recover Aspergillus flavus Eurotiomycetes 54 Aspergillus terreus Pezizomycotina 50 54 61 Aspergillus carbonarius the sequence of the gene-fusion and found no other 40 Aspergillus niger Mechanism 2: Fission by Degeneration 44 50 54 Aspergillus aculeatus Loss Event 54 61 Aspergillus nidulans true rhodopsin genes. Microsporum canis 50 54 61 Microsporum gypseum Phototaxis assays were performed in 35 Trichophyton equinum 9 Coccidioides immitis 61 Coccidioides posadasii Mechanism 3: Fission by Duplication & Differential Loss Ascomycota agar plates, the resulting vegetative cells found in 44 54 Uncinocarpus reesii Loss Event Blastomyces dermatitidis the region of the plates exposed, or not, to light 52 61 Histoplasma capsulatum 10 17 44 Paracoccidioides brasiliensis 58 Sporotrichum thermophile were visualised and counted under a microscope. Loss Event 53 41 Thielavia terrestris Light (521nm) Dark Chaetomium globosum 37 3 37 Podospora anserina 600 Neurospora crassa * 37 Neurospora tetrasperma Sordariomycetes 500 39 Cryphonectria parasitica Magnaporthe grisea 400 Rate and Types of Gene Fission Trichoderma reesei 41 Trichoderma virens 46 Trichoderma atoviride 300 29 Nectria haematococca 46 Fusarium oxysporum 200 These data suggest that gene fission plays Fusarium verticillioides 39 Fusarium graminearum 26 an important and hitherto underestimated 3 33 Verticillium dahliae Number of Zoosporangia 100 Verticillium albo-atrum Acremonium alcalophilum 24 0 role in gene evolution. Gene fusions, Botrytis cinerea Leotiomycetes Sclerotinia sclerotiorum Dark Light Light (521nm) Light Saccharomycotina 22 Spathaspora passalidarum (521nm) + HA (630nm) therefore, are highly labile characters, Candida albicans Pichia stipitis 20 and their use for polarizing evolutionary Debaryomyces hansenii Candida tenuis Zoospores were exposed to hydroxylamine in a photobleaching Candida glabrata 18 relationships, without reference to gene 34 4 Saccharomyces cerevisiae * process, as no gene-knockout is available, to test whether the 62 2 4 Ashbya gossypii 16 and species phylogenies is limited. 8 34 Wickerhamomyces anomalus Hansenula polymorpha gene-fusion was involved in photo-taxis. 34 Pichia membranifaciens 14 Yarrowia lipolytica Localization of BeGC1 to the eye-spot by immunofluorescence 34 Candida caseinolytica Rate of Fission 12 8 Lipomyces starkeyi microscopy. From left to the right: zoospore under phase HGT Schizosaccharomyces octosporus 1 8 9 17 62 24 34 Schizosaccharomyces cryophilus Schizosaccharomycetes 10 1 18 19 20 21 22 23 25 26 30 Schizosaccharomyces pombe * contrast (DIC image); BeGC1 (green); lipid droplets (nile-red) Schizosaccharomyces japonicus Mucor circinelloides * 8 9 Rhizopus oryzae * Mucoromycotina of the eyespot. Phycomyces blakesleeanus 6 Allomyces macrogynus atcc 38327 * 6 7 Blastocladiella emersonii Blastocladiomycota Side body complex - "eye spot" Batrachochytrium dendrobatidis * 4 Spizellomyces punctatus daom br117 Chytridiomycota Mechanism 1: Fission by Separation 100 # 2 Fusion 0.1 80+ Bootstrap Value Genus species * = fdfBLAST Sampled Proteomes Mechanism 2: Fission by Degeneration 50+ } # Reversion 0 Mechanism 3: Fission by Duplication 1 - Stechmann A, Cavalier-Smith T (2002) Rooting the eukaryote tree by using a derived gene fusion. Science 297(5578):89–91. 0 0.1 0.2 0.3 0.4 2 - Philippe H, et al. (2000) Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc Biol Sci 267(1449):1213–1221. Rate of Fusion & Differential Loss Flagellum Unknown 3 - Stechmann A, Cavalier-Smith T (2003) The root of the eukaryote tree pinpointed. Current Biology 13(17):R665–R666. 4 - Leonard, G & RichardsT. A. (2012) Genome-scale comparative analysis of gene fusions, gene fissions, and the fungal tree of life. PNAS 109(52). 5 - Avelar, G M, Schumacher, R I, Zaini, P I, Leonard, G, Richards, T A, Gomes, S L (2013) A novel mode of visual perception in the fungi. Manuscript submitted..
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