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Abstract

Postzygotic reproductive incompatibility, that is, the sterility or inviability of hybrids, dramatically illustrates breakdown of gene coordination within a genome and is likely important in speciation. We show here that post-zygotic incompatibilty exists among wild strains of Arabidopsis thaliana. Among over 300 hybrid combinations we identified five F1 hybrids that show environmentally sensitive morphological defects, ranging in severity from leaf chlorosis and twisting, to dwarfism, loss of apical dominance, severe leaf defects and growth arrest. The genetic interactions conform to predictions of the Dobzhansky-Muller model for post-zygotic incompatibility involving two dominant loci. All five hybrids are specific; crosses with other ecotypes did not produce abnormalities. Furthermore, hybrid combinations among the parents of these hybrids show that different genes or alleles underlie the F1 phenotypes. Using micro-arrays, histological and other molecular approaches, we found that these hybrids mount autoimmune responses in the absence of pathogen challenge. Consistent with this, one of two causal regions fine-mapped in one hybrid contains two polymorphic TIR-NBS-LRR class resistance (R) genes. We are now testing candidate genes using artificial micro-RNAs and are mapping the causal loci for the remaining four hybrids. Intriguingly, our Arabidopsis hybrid incompatibility phenotypes (including temperature sensitivity) are remarkably similar to a common F1 hybrid syndrome, hybrid necrosis or weakness, which occurs in a wide variety of other plant species. Based on our data, we hypothesize that rapidly-evolving R genes evolve aberrant interactions with gene variants present in conspecific individuals, resulting in hybrid incompatibility at detectable frequency in Arabidopsis and other plant species. This parallels findings in animals that implicate rapidly evolving genes in reproductive isolation and has important implications for plant evolution and speciation.