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

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.

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

“…In Arabidopsis, hybrid necrosis in the F 1 generation has been reported in about 2% of crosses between different accessions (Bomblies et al, 2007). Genetic mapping of stunted growth and necrotic phenotypes for a small subset of these crosses using laboratory strains such as Col and Ler as one of the parents implicated epistasis between a few loci involved in pathogen defense (Bomblies et al, 2007;Alcázar et al, 2009).…”

“…It is commonly implied that hybrid incompatibilities arise because different substitutions are fixed by natural selection in different populations, but chance fixation because of genetic drift (cf., Bomblies et al, 2007), and a selfing mating system could also have a role. Selfing could hasten initial fixation because of increased homozygosity within populations, and decreased gene flow between populations (Gimond et al, 2013).…”

“…Bomblies et al (2007) generated 4800 different F 1 progenies from 280 unique accessions and found a 2% incidence of hybrid necrosis in the rosette stage. Subsequent quantitative trait loci (QTL) mapping using Col as one of the parental lines indicated that the genetic basis of necrosis was due to negative epistatic interactions involving 2-4 loci (Bomblies et al, 2007).…”

“…Bomblies et al (2007) generated 4800 different F 1 progenies from 280 unique accessions and found a 2% incidence of hybrid necrosis in the rosette stage. Subsequent quantitative trait loci (QTL) mapping using Col as one of the parental lines indicated that the genetic basis of necrosis was due to negative epistatic interactions involving 2-4 loci (Bomblies et al, 2007). Similar interactions, mapped to approximately the same regions, were found in a study of the genetic basis of necrosis in two different recombinant inbred line mapping populations with Ler as a parental line (Alcázar et al, 2009).…”

Linkage group correction using epistatic distorted markers in F2 and backcross populations

“…Epistasis, the interaction between loci, has been shown to have a strong association with segregation distortion (Bomblies et al, 2007;Alheit et al, 2011). Epistatic SDL has a significant implication for inbreeding depression (Phillips, 2008), which is mainly manifested as hybrid male or female sterility.…”