Acquisition and loss of secondary metabolite clusters shaped the evolutionary path of three recently emerged phytopathogens of wheat

O_LIWhite grain disorder is a recently emerged wheat disease in Australia, caused by three Botryosphaeriaceae spp.; Eutiarosporella darliae, E. pseudodarliae, and E. tritici-australis. The disease cycle of these pathogens and the molecular basis of their interaction with wheat are poorly understood. To address this, we undertook a comparative genomics approach to identify potential pathogenicity factors.\nC_LIO_LISubsequent genome analysis revealed that each of the white grain disorder species harbour modular polyketide synthase genes. To our knowledge, this is the first report of fungi harbouring such genes. Further comparative analysis using the modular polyketide synthase genes discovered their presence in the closely related Macrophomina phaseolina. Phylogenetic analysis implicates horizontal acquisition of these genes from a bacterial or a protist species.\nC_LIO_LIBoth E. darliae and E. pseudodarliae possess a secondary metabolite cluster with multiple polyketide/non-ribosomal peptide synthase genes (Hybrid-1, -2, and -3). In contrast, only remnant and partial genes homologous to this cluster were identified at a syntenic locus in E. tritici-australis suggesting loss of this cluster. Homologues of Hybrid-2 in other fungi have been proposed to facilitate disease induction in woody plants. Subsequent assays confirmed that E. darliae and E. pseudodarliae were both pathogenic on woody plant hosts, but E. tritici-australis was not, implicating woody plants as potential host reservoirs for the fungi. We hypothesise that loss of the cluster in E. tritici-australis represents a committed lifestyle jump to grasses.\nC_LIO_LICombined, our observations relating to the secondary metabolite potential of the WGD Eutiarosporella spp. have contributed novel data to the field by expanding the range of known fungal secondary metabolite genes, and helped develop our understanding of the lifestyle and potential host-range of a recently emerged pathogen of wheat.\nC_LI