Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi

Abstract

The class Dothideomycetes is one of the largest groups of fungi with a high level of ecological diversity including many plant pathogens infecting a broad range of hosts. Here, we compare genome features of 18 members of this class, including 6 necrotrophs, 9 (hemi)biotrophs and 3 saprotrophs, to analyze genome structure, evolution, and the diverse strategies of pathogenesis. The Dothideomycetes most likely evolved from a common ancestor more than 280 million years ago. The 18 genome sequences differ dramatically in size due to variation in repetitive content, but show much less variation in number of (core) genes. Gene order appears to have been rearranged mostly within chromosomal boundaries by multiple inversions, in extant genomes frequently demarcated by adjacent simple repeats. Several Dothideomycetes contain one or more gene-poor, transposable element (TE)-rich putatively dispensable chromosomes of unknown function. The 18 Dothideomycetes offer an extensive catalogue of genes involved in cellulose degradation, proteolysis, secondary metabolism, and cysteine-rich small secreted proteins. Ancestors of the two major orders of plant pathogens in the Dothideomycetes, the Capnodiales and Pleosporales, may have had different modes of pathogenesis, with the former having fewer of these genes than the latter. Many of these genes are enriched in proximity to transposable elements, suggesting faster evolution because of the effects of repeat induced point (RIP) mutations. A syntenic block of genes, including oxidoreductases, is conserved in most Dothideomycetes and upregulated during infection in L. maculans, suggesting a possible function in response to oxidative stress. Dothideomycetes is the largest and most ecologically diverse class of fungi that includes many plant pathogens with high economic impact. Currently 18 genome sequences of Dothideomycetes are available, 14 of which are newly described in this paper and in several companion papers, allowing unprecedented resolution in comparative analyses. These 18 organisms have diverse lifestyles and strategies of plant pathogenesis. Three feed on dead organic matter only, six are necrotrophs (killing the host plant cells), one is a biotroph (forming an association with and thus feeding on the living cells of the host plant cells) and 8 are hemibiotrophs (having an initial biotrophic stage, and killing the host plant at a later stage). These various lifestyles are also reflected in the gene sets present in each group. For example, sets of genes involved in carbohydrate degradation and secondary metabolism are expanded in necrotrophs. Many genes involved in pathogenesis are located near repetitive sequences, which are believed to speed up their evolution. Blocks of genes with conserved gene order were identified. In addition to this we deduce that the mechanism for mesosynteny, a type of genome evolution particular to Dothideomycetes, is by intra-chromosomal inversions.