Location: Sugarbeet and Potato ResearchTitle: The heterothallic sugarbeet pathogen Cercospora beticola contains exon fragments of both MAT genes that are homogenized by concerted evolution Author
Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/28/2013
Publication Date: 1/6/2014
Citation: Bolton, M.D., Dejonge, R., Inderbitzin, P., Liu, Z., Birla, K., Vandepeer, Y., Subbarao, K.V., Thomma, B.P., Secor, G.A. 2014. The heterothallic sugarbeet pathogen Cercospora beticola contains exon fragments of both MAT genes that are homogenized by concerted evolution. Fungal Genetics and Biology. 62:43-54. Interpretive Summary: Mating type genes control nonself recognition and sexual reproduction in fungi. In so-called heterothallic fungi, each individual is self-sterile and mating can only occur between isolates of the opposite mating type. In contrast, homothallic fungi are self-fertile and therefore can self, or alternatively, mate with any individual in the population. The evolution of these two forms of sexual reproduction has been of interest for several decades. In this paper we show that the heterothallic fungi Cercospora beticola, C. zeae-maydis, and Mycosphaerella fijiensis harbor fragments of both mating type genes in proximity in their haploid genomes. We show that these fragments are able to reconstitute the exon sequence of both bona fide mating type genes, which suggests that they are retrotranspositioned remnants of a homothallic ancestor in which the two genes were fused. After speciation, mating type genes and gene fragments appear to have undergone concerted evolution since fragments were more closely related to paralogous mating type genes within a species than orthologous mating type genes between all three species. Although heterothallism has been suggested to be the ancestral state for the Dothideomycetes, our data suggest the fungi in this study evolved from a homothallic lineage.
Technical Abstract: Dothideomycetes is one of the most ecologically diverse and economically important classes of fungi. Sexual reproduction in this group is governed by mating type (MAT) genes at the MAT1 locus. Self-sterile (heterothallic) species contain one of two genes at MAT1, MAT1-1-1 or MAT1-2-1, and only isolates of opposite mating type are sexually compatible. In contrast, self-fertile (homothallic) species contain both MAT genes at MAT1. Knowledge of the reproductive capacities of plant pathogens are of particular interest because recombining populations tend to be more difficult to manage in agricultural settings. In this study, we sequenced MAT1 in the heterothallic Dothideomycete fungus Cercospora beticola to gain insight into the reproductive capabilities of this important plant pathogen. In addition to complete MAT genes at MAT1, each isolate contained an identical set of MAT1-1-1 and MAT1-2-1 fragments in proximity (< 1 kb) at ostensibly random loci across the genome. MAT fragments lacked introns and could reconstitute MAT1-1-1 and MAT1-2-1 exons, suggesting a retroposition event occurred in a homothallic ancestor in which both MAT genes were fused. The genome sequences of related taxa revealed that MAT gene fragment pattern of C. zeae-maydis was analogous to C. beticola, but differed in Mycosphaerella fijiensis. In contrast, the genome of more distantly related M. graminicola did not contain MAT gene fragments. Although fragments occurred in syntenic regions of the C. beticola and C. zeae-maydis genomes, each MAT fragment was more closely related to the intact MAT gene of the same species. Taken together, these data suggest MAT genes fragmented after divergence of M. graminicola from the remaining taxa, and concerted evolution functioned to homogenize MAT fragments and MAT genes in each species. Although heterothallism has been suggested to be the ancestral state in most Dothideomycetes, our data suggest a homothallic lineage existed in this fungal class.