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A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi

James K Hane12, Thierry Rouxel3, Barbara J Howlett4, Gert HJ Kema5, Stephen B Goodwin6 and Richard P Oliver7*

Author Affiliations

1 CSIRO Plant Industry, Centre for Environment and Life Sciences, Private Bag 5, Perth, 6193, Australia

2 Faculty of Health Sciences, Murdoch University, Perth, 6150, Australia

3 INRA-Bioger, Avenue Lucien Brétignières, BP 01, Thiverval-Grignon, 78850, France

4 School of Botany, The University of Melbourne, Melbourne, 3010, Australia

5 Wageningen UR, Plant Research International, Department of Biointeractions and Plant Health, PO Box 69, Wageningen, 6700 AB, The Netherlands

6 USDA-ARS, Crop Production and Pest Control Research Unit, Purdue University, 915 West State Street, West Lafayette, IN 47907-2054, USA

7 Australian Centre for Necrotrophic Fungal Pathogens, Curtin University, Perth, 6845, Australia

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Genome Biology 2011, 12:R45  doi:10.1186/gb-2011-12-5-r45

Published: 24 May 2011

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.