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.
Highlights
Epistasis—the nonadditive interaction between genes—is a critical determinant for the performance of hybrid genotypes
Our results demonstrate that aberrant activation of the plant immune system, due to epistatic interactions between alleles that are harmless in their native genetic context, can have highly deleterious consequences for F1 hybrid progeny, even among strains within a species
F1 incompatibilities that are phenotypically similar to the cases of A. thaliana hybrid necrosis we describe have been observed in progeny of many intra- and interspecific crosses [2,4,23,30,31,32,33], suggesting that a common molecular mechanism may underlie hybrid necrosis across diverse species
Summary
Epistasis—the nonadditive interaction between genes—is a critical determinant for the performance of hybrid genotypes. It encompasses a spectrum of important genetic phenomena, from positive heterosis (hybrid vigor) to negative heterosis (hybrid sterility or lethality). Cytoplasmic male sterility and hybrid necrosis have received relatively little attention outside the plant genetics literature, even though one of the earliest described cases of hybrid necrosis is between two Crepis species and conforms to the tenets for Dobzhansky-Muller type incompatibilities, which establish or maintain gene flow barriers between species [3,4]. Despite advances in our knowledge of the genetics of hybrid incompatibility, the prevalence and mechanisms of early-arising gene flow barriers between members of the same species are not yet well understood
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