Autoimmune Response as a Mechanism for a Dobzhansky-Muller-Type Incompatibility Syndrome in Plants

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Abstract
Epistatic interactions between genes are a major factor in evolution. Hybrid necrosis is an example of a deleterious phenotype caused by epistatic interactions that is observed in many intra- and interspecific plant hybrids. A large number of hybrid necrosis cases share phenotypic similarities, suggesting a common underlying mechanism across a wide range of plant species. Here, we report that approximately 2% of intraspecific crosses in Arabidopsis thaliana yield F1 progeny that express necrosis when grown under conditions typical of their natural habitats. We show that several independent cases result from epistatic interactions that trigger autoimmune-like responses. In at least one case, an allele of an NB-LRR disease resistance gene homolog is both necessary and sufficient for the induction of hybrid necrosis, when combined with a specific allele at a second locus. The A. thaliana cases provide insights into the molecular causes of hybrid necrosis, and serve as a model for further investigation of intra- and interspecific incompatibilities caused by a simple epistatic interaction. Moreover, our finding that plant immune-system genes are involved in hybrid necrosis suggests that selective pressures related to host–pathogen conflict might cause the evolution of gene flow barriers in plants. Hybridization brings together genetic material from different genomes. Sometimes, the novel combinations of genes are deleterious in the offspring, even though the genes were innocuous, or even beneficial, in their parents. Such “genetic incompatibilities” have been observed in crosses within and between species in plants, animals, and fungi, and could contribute to the maintenance of population or species boundaries. We have investigated a highly deleterious genetic incompatibility called hybrid necrosis that is observed in many plant taxa. Using different wild strains of Arabidopsis thaliana as a model, we show that hybrid necrosis is often associated with inappropriate activation of the plant immune system—effectively plant autoimmunity. We identified a gene in one strain that triggers necrosis when combined with a second locus from another strain. The product of this gene is an NB-LRR protein, the most common type of plant disease resistance protein. This finding raises the possibility that selective pressure exerted by pathogens can promote rapid evolution of gene variants that might provide benefits to the parent lineage but can cause serious problems for hybrid progeny.