Molecular evolution of two pathogenicity-associated gene families across the Dothideomycetes class of fungi

Abstract

The Dothideomycetes class of fungi comprises over 19,000 described species, which are distributed into 23 orders. Generally, Dothideomycetes species have a cosmopolitan distribution and exhibit high ecological diversity, with distinct trophic modes (saprotrophic, pathogenic, endophytic, and mycorrhizal). Within the Dothideomycetes, one notable feature is the presence of many plant-pathogenic species, such as Corynespora cassiicola (Pleosporales) that causes diseases in economically important crops. Using data genomic data from 79 Dothideomycetes species (15 orders) and 61 C. cassiicola isolates, we investigated the evolutionary history of two pathogenicity-associated gene families: Pectin methylesterase (PME) and Deuterolysin metalloprotease (M35). We conducted phylogenic reconstructions and gene genealogies to uncover evolutionary patterns in both PME and M35. In C. cassiicola (isolate CC_29), we assessed gene expression patterns of members of each family, PME and M35, during the process of soybean infection. For the PME family, we recovered three major clades across the Dothideomycetes. Among these three clades, two (PME1 and PME2) have experienced duplications and sequent gene retention events, whereas the other clade (PME3) likely has evolved through biased gene loss. Each C. cassiicola isolate displayed five PME genes. The five PME haplogroups in C. cassiicola showed varying levels of genetic diversity and may have undergone distinct selective pressures. For the M35 family, the number of genes varied from zero to seven per genome across the Dothideomycetes. Specifically, some species within the order Botryophaeriales exhibited a higher numbergenesM35 genes. The majority of C. cassiicola isolates display three M35 genes per genome. In C. cassiicola, either gene retention episodes or gene loss characterized each of the four sub-clades within the M35 family. All genes of each family, PME and M35, were expressed in C. cassiicola during the interaction with soybean plants, suggesting that they are functional and may contribute to fungal infection. Keywords: Corynespora. Genomics. Gene duplication. Molecular phylogeny. Plant- pathogens