Abstract

Understanding early causes and consequences of genetic divergence is important for elucidating how intrinsic gene flow barriers might arise among populations during speciation. Arabidopsis thaliana is a primarily self-fertilizing plant species made up of many essentially independently diverging lineages with little gene flow among them, making it an ideal model system for investigating early stages of genetic divergence. We examined progeny of 1487 intercrosses among 311 wild accessions. Most were compatible, as expected for within-species crosses, but 21 first-generation hybrids showed strongly deleterious phenotypes including dwarfism, severe tissue necrosis and sterility. In independent cases we found that this is due to hyperactivation of the plant immune system (effectively, plant autoimmunity). Consistent with this, at least two cases are caused by combinations of different known or suspected pathogen resistance ( R ) genes. Plant immune systems, like animal immune systems, are necessarily diverse to counter the barrage of variable pathogens that attempt to exploit them. However, for all their benefits, plant pathogen resistance genes are inherently dangerous entities that regulate a terminal programmed cell death response. Genetic divergence among immune system genes can thus have dire consequences for hybrid progeny in crosses among plant lineages where protein partners have not co-evolved to function together. Our results, together with results from other groups, suggest that pathogen pressure may indirectly promote genetic incompatibility by promoting divergence of R genes. Furthermore, the prevalence of such “hybrid necrosis” phenotypes suggests that 1) A. thaliana is a useful model for understanding a common phenomenon in plants, and 2) that necrosis may be an important factor in the adaptive evolution of the plant immune system.