The role of gene presence–absence variations on genetic incompatibility in Asian rice

Abstract

Summary Genetic incompatibilities are widespread between species. However, it remains unclear whether they all originated after population divergence as suggested by the Bateson–Dobzhansky–Muller model, and if not, what is their prevalence and distribution within populations. The gene presence–absence variations (PAVs) provide an opportunity for investigating gene–gene incompatibility. Here, we searched for the repulsion of coexistence between gene PAVs to identify the negative interaction of gene functions separately in two Oryza sativa subspecies. Many PAVs are involved in subspecies‐specific negative epistasis and segregate at low‐to‐intermediate frequencies in focal subspecies but at low or high frequencies in the other subspecies. Incompatible PAVs are enriched in two functional groups, defense response and protein phosphorylation, which are associated with plant immunity and consistent with autoimmunity being a known mechanism of hybrid incompatibility in plants. Genes in the two enriched functional groups are older and seldom directly interact with each other. Instead, they interact with other younger gene PAVs with diverse functions. Our results illustrate the landscape of genetic incompatibility at gene PAVs in rice, where many incompatible pairs have already segregated as polymorphisms within subspecies, and many are novel negative interactions between older defense‐related genes and younger genes with diverse functions.