Acquisition and Loss of Secondary Metabolites Shaped the Evolutionary Path of Three Emerging Phytopathogens of Wheat

Whitegraindisorder is a recently emergedwheatdisease inAustralia, causedby Eutiarosporelladarliae, E. pseudodarliae,andE. triticiaustralis. The disease cycle of these pathogens and the molecular basis of their interaction with wheat are poorly understood. To address this knowledge gap, we undertook a comparative genomics analysis focused on the secondarymetabolite gene repertoire among these three species. This analysis revealed a diverse array of secondarymetabolite gene clusters in these pathogens, including modular polyketide synthase genes. These genes have only been previously associatedwith bacteria and this is the first report of such genes in fungi. Subsequent phylogenetic analyses provided strong evidence that themodular PKS geneswere horizontally acquired from a bacterial or a protist species. We also uncovered a secondary metabolite gene cluster with three polyketide/nonribosomal peptide synthase genes (Hybrid-1, -2, and -3) in E. darliae and E. pseudodarliae. In contrast, only remnant and partial genes homologous to this cluster were identified in E. tritici-australis, suggesting loss of this cluster. Homologues of Hybrid-2 in other fungi have been proposed to facilitate disease inwoody plants, suggesting a possible alternative host range for E. darliae and E. pseudodarliae. Subsequent assays confirmed that E. darliae and E. pseudodarliaewere both pathogenic onwoody plants, but E. tritici-australis was not, implicatingwoody plants as potential host reservoirs for the fungi. Combined, these data have advanced our understanding of the lifestyle and potential host-range of these recently emerged wheat pathogens and shed new light on fungal secondary metabolism.