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

Authors: YUZON, JENNIFER - Max Planck Institute For Evolutionary Biology; Wyatt, Nathan; VASIGHZADEH, ASIEH - Department Of Plant Protection; CLARE, SHAUN - Department Of Plant Protection; Navratil, Emma; Friesen, Timothy; STUKENBROCK, EVA - Max Planck Institute For Evolutionary Biology

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/19/2023
Publication Date: 3/15/2023
Citation: Yuzon, J.D., Wyatt, N.A., Vasighzadeh, A., Clare, S., Navratil, E.M., Friesen, T.L., Stukenbrock, E.H. 2023. Hybrid inferiority and genetic incompatibilities drive divergence of fungal pathogens infecting the same host. Genetics. https://doi.org/10.1093/genetics/iyad037.
DOI: https://doi.org/10.1093/genetics/iyad037

Interpretive Summary: Net form net blotch and spot form net blotch are major diseases of barley caused by Pyrenophora teres f. teres (Ptt) and P. teres f. maculata (Ptm), respectively. Ptt and Ptm are considered the same species and can be crossed in the lab, however, sexual crossing in the field is rarely reported. In this study, we investigated the potential barriers to this incompatibility in the field. We showed that hybrid progeny from a Ptt x Ptm cross were less virulent than the parental Ptt and Ptm isolates on a susceptible barley line. This work indicates that out crossing in the field decreases the fitness of the pathogen and for the first time provides a explanation for why these two forms of the same species do not out cross in nature. This work adds to our knowledge of pathogen genetics and shows that it is unlikely that these pathogens will interbreed to form a more virulent species, knowledge that is important to breeders trying to maintain resistance to these two important diseases.

Technical 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. 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 colonize 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). Intriguingly, these regions are contain genes predicted or known to play a role in virulence, potentially suggesting that divergent niche adaptation – albeit in the same host plant - is a driver of speciation in P. teres.