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A Novel Mode of Chromosomal Evolution Peculiar to Filamentous Ascomycete Fungi J.K A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi J.K. Hane, Thierry Rouxel, B.J. Howlett, Ghj Kema, S.B. Goodwin, R.P. Oliver To cite this version: J.K. Hane, Thierry Rouxel, B.J. Howlett, Ghj Kema, S.B. Goodwin, et al.. A novel mode of chromo- somal evolution peculiar to filamentous Ascomycete fungi. Genome Biology, BioMed Central, 2011, 12 (5), pp.1-16; R45. 10.1186/gb-2011-12-5-r45. hal-01001183 HAL Id: hal-01001183 https://hal.archives-ouvertes.fr/hal-01001183 Submitted on 29 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Hane et al. Genome Biology 2011, 12:R45 http://genomebiology.com/2011/12/5/R45 RESEARCH Open Access A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi James K Hane1,2, Thierry Rouxel3, Barbara J Howlett4, Gert HJ Kema5, Stephen B Goodwin6 and Richard P Oliver7* Abstract Background: Gene loss, inversions, translocations, and other chromosomal rearrangements vary among species, resulting in different rates of structural genome evolution. Major chromosomal rearrangements are rare in most eukaryotes, giving large regions with the same genes in the same order and orientation across species. These regions of macrosynteny have been very useful for locating homologous genes in different species and to guide the assembly of genome sequences. Previous analyses in the fungi have indicated that macrosynteny is rare; instead, comparisons across species show no synteny or only microsyntenic regions encompassing usually five or fewer genes. To test the hypothesis that chromosomal evolution is different in the fungi compared to other eukaryotes, synteny was compared between species of the major fungal taxa. Results: These analyses identified a novel form of evolution in which genes are conserved within homologous chromosomes, but with randomized orders and orientations. This mode of evolution is designated mesosynteny, to differentiate it from micro- and macrosynteny seen in other organisms. Mesosynteny is an alternative evolutionary pathway very different from macrosyntenic conservation. Surprisingly, mesosynteny was not found in all fungal groups. Instead, mesosynteny appears to be restricted to filamentous Ascomycetes and was most striking between species in the Dothideomycetes. Conclusions: The existence of mesosynteny between relatively distantly related Ascomycetes could be explained by a high frequency of chromosomal inversions, but translocations must be extremely rare. The mechanism for this phenomenon is not known, but presumably involves generation of frequent inversions during meiosis. Background many authors. Originally it was used in cytogenetics to The evolutionary history of organisms, as revealed by describe two or more loci that are located on the same comparisons of genome sequences, is of the greatest chromosome. As DNA sequencing and comparative biological significance and interest. The current explo- genomics became commonplace, the term synteny sion in the number of genome assemblies of species acquired the additional property of co-linearity; i.e. the within the same class, order and genus is allowing the conservation of gene order and orientation. In this whole-genome interrelationships between organisms to study we refer to synteny in the original cytogenetic be examined in ever greater detail. There is a long his- sense and describe co-linearity as a sub-category of tory of comparisons of individual orthologous gene synteny. If orthologs of multiple genes that are co- sequences and these have revolutionized our under- located in the genome of one organism are co-located standing of phylogenetic relationships [1]. A more in another species, the chromosomes on which the complete understanding of both the mechanism and genes reside are said to be syntenic. Synteny can also results of evolution can be obtained by comparing be quantitative; chromosomes that contain all of the entire genomes [2]. These comparisons have refined same genes are 100% syntenic. the concept of synteny. This term is used loosely by The process of speciation occurs when two indepen- dent populations diverge into reproductively isolated * Correspondence: [email protected] species. Initially the daughter species would have had 7Australian Centre for Necrotrophic Fungal Pathogens, Curtin University, chromosomes that shared both gene content (synteny) Perth, 6845, Australia and order (co-linearity). Over evolutionary time, the Full list of author information is available at the end of the article © 2011 Hane et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Hane et al. Genome Biology 2011, 12:R45 Page 2 of 16 http://genomebiology.com/2011/12/5/R45 degree of synteny and co-linearity would be degraded Filamentous fungi form an ancient, large and diverse through various processes, including chromosomal group of organisms. Until the last decade, the phyloge- duplications, gene losses/gains and chromosomal rear- netics of fungi was problematic but the application of rangements (Additional file 1), until orthologous genes techniques based on gene sequence variation has created in one species occur randomly in the genome of the astabletaxonomy.Theascomycetefilamentousfungi other. are mostly within the sub-phylum Pezizomycotina (Fig- The related concepts of synteny and co-linearity have ure 1) [11]. This sub-phylum contains four major been refined mostly in plants, animals and bacteria. Syn- classes: Dothideomycetes, Eurotiomycetes, Sordariomy- teny has been differentiated qualitatively based on the cetes and Leotiomycetes. The Dothideomycetes contains length and completeness of co-linear regions. Macrosyn- more than 20,000 species amongst which are many of teny describes co-linearity observable at a whole-chro- the most important plant pathogens worldwide, includ- mosome scale, involving hundreds or thousands of ing those in the genera Phaeosphaeria, Leptosphaeria genes of which a backbone are co-linear. Microsynteny and Mycosphaerella. describes co-linearity spanning a small number (for Evolutionary diversity within the filamentous ascomy- example, two to ten) of successive genes. Comparisons cete fungi is much higher than in flowering plants or of vertebrate and flowering plant species within taxo- vertebrate animals [12]. A number of reasons have been nomic families often have shown extensive macrosyn- proposed to account for this. Filamentous fungi reflect teny [3-8]. Macrosynteny has been exploited to assist approximately 400 million years of evolutionary history, genetic mapping and gene cloning; examples include the comparable to that of the vertebrates but approximately use of the Arabidopsis genome to find genes in canola four times longer than that of the flowering plants [13] [9], and rice/Brachypodium synteny to locate genes in (Figure 1; Table 1). The generation times of fungi are wheat and barley [10]. typically measured in hours or days, whereas plants and Order Class Sub-phylum Phylum Phaeosphaeria nodorum Pleosporales Leptosphaeria maculans Dothideomycetes Mycosphaerella graminicola Capnodiales Mycosphaerella fijiensis Aspergillus fumigatus Eurotiales Penicillium marneffei Eurotiomycetes Arthroderma gypseum Onygenales Pezizomycotina Coccidioides immitus Botryotinia fuckeliana Helotiales Leotiomycetes Sclerotinia sclerotiorum Ascomycota Podospora anserina Sordariales Neurospora crassa Magnaporthales Magnaporthe oryzae Sordariomycetes Fusarium oxysporum Hypocreales Nectria haematococca Lachancea kluyveri Lachancea waltii Saccharomyces cerevisiae Saccharomycetales Saccharomycetes Saccharomycotina Candida albicans Candida tropicalis Schizosaccharomyces pombe Schizosaccharomyces cyrophilus Schizosaccharomycetales Schizosaccharomycetes Taphrinomycotina Schizosaccharomyces japonicus Puccinia graminis Puccinales Pucciniomycetes Pucciniomycotina Malassezia globosa Malasezziales Exobasidiomycetes Ustilaginomycotina Basidiomycota Coprinosis cinerea Agaricales Agaricomycetes Agaricomycotina Laccaria bicolor Allomyces macrogynus Blastocladiales Blastocladiomycetes Blastocladiomycota Batrachochytrium dendrobatidis Chytridiales Chytridiomycetes Chytridiomycota Figure 1 Cladogram of species used in whole-genome comparisons in this study. Detailed information on each species is provided in Additional file 3. http://genomebiology.com/2011/12/5/R45 Hane et al . Genome Biology 2011, 12 Table 1 Summary of whole-genome synteny relationships across selected fungal orders :R45 Sub-phylum Pezizomycotina Saccharomycotina Taphrinomycotina Class Dothideomycetes Eurotiomycetes Sordariomycetes Leotiomycetes Saccharomycetes Schizosaccharomycetes Class Order Capnodiales Pleosporales Eurotiales Onygenales Hypocreales Magnaporthales Sordariales Helotiales Saccharomycetales Schizosaccharomycetales Dothideomycetes Capnodiales
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