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Title: Mesosynteny; A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi

item HANE, JAMES - Commonwealth Scientific And Industrial Research Organisation (CSIRO)
item ROUXEL, THEIRRY - Institut National De La Recherche Agronomique (INRA)
item HOWLETT, BARBARA - University Of Melbourne
item KEMA, GERT H. - Plant Research International - Netherlands
item Goodwin, Stephen - Steve
item OLIVER, RICHARD - Indiana University-Purdue University

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/24/2011
Publication Date: 5/24/2011
Citation: Hane, J.K., Rouxel, T., Howlett, B., Kema, G.J., Goodwin, S.B., Oliver, R.P. 2011. Mesosynteny; A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biology. 12:R45.

Interpretive Summary: Availability of genomic sequences has allowed detailed comparisons of the structures of chromosomes between species. In plants and animals, genes on chromosomes from different species usually occur in the same order and orientation, allowing large chromosomal segments to be lined up in different species. This information has been very helpful for finding genes in related species of plants and animals, because a gene of interest in one species is likely to be located in a similar position in other species. Genes that occur in the same order and orientation in different species are considered to be syntenic, and the overall alignment of chromosomes is referred to as synteny. Alignment of only very small groups of genes is referred to as microsynteny. Previous reports in fungi indicated that synteny among chromosomes may be low, presumably due to higher rates of evolution and longer times since species shared a common ancestor. To perform a thorough test for synteny among chromosomes of fungi, genomic sequences from fungi in several different evolutionary groups were obtained and compared. Alignments of gene sequences showed little evidence for the type of synteny observed previously in plants and animals. Instead, there was a strong conservation of gene content but not order or orientation. This pattern, referred to as mesosynteny, appears to be new and unique to certain groups of fungi. This information will be useful to fungal and evolutionary biologists to better understand chromosome evolution. Knowing that certain genes usually occur together may be useful for genomic sequencing to piece together large blocks of DNA, and it indicates that locations of certain genes in one species could occur anywhere on a particular chromosome in another.

Technical Abstract: We report a novel form of evolution in which genes are conserved within homologous chromosomes, but with randomised orders and orientations. We propose to call this mode of evolution 'mesosynteny'. Mesosynteny is an alternative evolutionary pathway to macrosyntenic conservation. Mesosynteny would be expected to occur when intra-chromosomal (especially inversions) recombinational events greatly out-numbered inter-chromosomal rearrangements. Furthermore, microsyntenic regions are rarely observed. Mesosynteny appears to be restricted to filamentous Ascomycete fungi (the sub-phylum Pezizomycotina) and was most striking between Dothideomycete species, a large taxon responsible for major crop diseases. Filamentous fungi are noted for supernumerary chromosomes, propensity for lateral gene transfer and repeat-induced point mutation (RIP). We propose that mesosynteny is a consequence of the genomic idiosyncrasies of this large and significant group of fungi.