Comparative Genome Structure, Secondary Metabolite, and Effector Coding Capacity across Cochliobolus Pathogens

The genomes of five Cochliobolus heterostrophus strains, two Cochliobolus sativus strains, three additional Cochliobolus species (Cochliobolus victoriae, Cochliobolus carbonum, Cochliobolus miyabeanus), and closely related Setosphaeria turcica were sequenced at the Joint Genome Institute (JGI). The datasets were used to identify SNPs between strains and species, unique genomic regions, core secondary metabolism genes, and small secreted protein (SSP) candidate effector encoding genes with a view towards pinpointing structural elements and gene content associated with specificity of these closely related fungi to different cereal hosts. Whole-genome alignment shows that three to five percent of each genome differs between strains of the same species, while a quarter of each genome differs between species. On average, SNP counts among field isolates of the same C. heterostrophus species are more than 25× higher than those between inbred lines and 50× lower than SNPs between Cochliobolus species. The suites of nonribosomal peptide synthetase (NRPS), polyketide synthase (PKS), and SSP–encoding genes are astoundingly diverse among species but remarkably conserved among isolates of the same species, whether inbred or field strains, except for defining examples that map to unique genomic regions. Functional analysis of several strain-unique PKSs and NRPSs reveal a strong correlation with a role in virulence. The filamentous ascomycete genus Cochliobolus includes highly aggressive necrotrophic and hemibiotrophic pathogens with particular specificity to their host plants, often associated with production of host selective toxins (HST) that allow necrotrophs to trigger host cell death. Hemibiotrophs must keep their hosts alive during initial infection stages and rely on subverting host defenses by secreting small protein effectors. Many Cochliobolus species have emerged rapidly as devastating pathogens due to HSTs. The genomes of Cochliobolus and related pathogens that differ in host preference, host specificity, and virulence strategies have been sequenced. Our comparative results, at the whole-genome level, and with a spotlight on core genes for secondary metabolism and small secreted proteins, touch on how pathogens develop and hone these tools, according to host or lifestyle. We suggest that, while necrotrophs and hemibiotrophs employ fundamentally contrasting mechanisms of promoting disease, the tools they utilize (HSTs and protein effectors) overlap. The suites of secondary metabolite and SSP genes that each possesses reflect astounding diversity among species, hinting that gene products, particularly those associated with unique genomic regions, are candidates for pathogenic lifestyle differences. Manipulations of strain-unique secondary metabolite genes associated with host-specific virulence provide tangible examples.