Description
Reproductive barriers perform a vital role during speciation. Hybrid weakness, the poor development of hybrids compared to their parents, hinders gene exchange between different species at the postzygotic stage. The molecular and evolutionary mechanisms of hybrid weakness are poorly understood. Here, we report that two incompatible dominant loci (Hwi1 and Hwi2) involving three genes determine the high temperature-dependent expression of hybrid weakness in interspecific hybrids of rice. Hwi1 comprises two indispensable wild rice (Oryza rufipogon)-specific leucine-rich repeat receptor-like kinase (LRR-RLK) genes, 25L1 and 25L2, for inducing hybrid weakness, and the genes possibly undergo balancing selection. Hwi2, a rare allele that is predominantly distributed in indica rice (Oryza sativa), encodes a secreted putative subtilisin-like protease. Functional analysis indicated that pyramiding of Hwi1 and Hwi2 activates the autoimmune response in the basal nodes of hybrids, interrupting root formation and then impairing shoot growth, likely due to immune signal is transmitted from the basal nodes to the above-ground parts. Considering the nature of RLK activity of Hwi1 and the protease activity of Hwi2, we propose that a certain endogenous signaling molecule produced by Hwi2 is perceived by Hwi1 to activate autoimmunity through ligand-receptor signal transduction. These findings bring new insights into our understanding of reproductive isolation and may benefit rice breeding to maximally utilize invaluable genes from wild rice.