Hybrid inferiority and genetic incompatibilities drive divergence of fungal pathogens infecting the same host

Abstract

Abstract Agro-ecosystems provide environments that are conducive for rapid evolution and dispersal of plant pathogens. Previous studies have demonstrated that hybridization of crop pathogens can give rise to new lineages with altered virulence profiles. Currently, little is known about either the genetics of fungal pathogen hybridization or the mechanisms that may prevent hybridization between related species. The fungus Pyrenophora teres is a global pathogen of barley. The pathogenic fungus P. teres exists as two distinct lineages P. teres f. teres and P. teres f. maculata (Ptt and Ptm, respectively), which both infect barley but produce very distinct lesions and rarely interbreed. Interestingly, Ptt and Ptm can, by experimental mating, produce viable progenies. Here, we addressed the underlying genetics of reproductive barriers of P. teres. We hypothesize that Ptt and Ptm diverged in the past, possibly by adapting to distinct hosts, and only more recently colonized the same host in agricultural fields. Using experimental mating and in planta phenotyping in barley cultivars susceptible to both P. teres forms, we demonstrate that hybrids produce mixed infection phenotypes but overall show inferior pathogenic fitness relative to the pure parents. Based on analyses of 104 hybrid genomes, we identify signatures of negative epistasis between parental alleles at distinct loci (Dobzhansky–Müller incompatibilities). Most DMI regions are not involved in virulence but certain genes are predicted or known to play a role in virulence. These results potentially suggest that divergent niche adaptation—albeit in the same host plant—contributes to speciation in P. teres.