Single-locus hybrid necrosis caused by common, co-occurring ACD6 alleles

Resistance to pathogens requires fine-tuning of a complex and constantly evolving immune system. A fundamental feature of this defense system is the ability to distinguish self and non-self. In plants, self-recognition involving immune regulators can sometimes present itself in hybrids, either inter- or intra-specific, leading to an autoimmune response; affected plants grow less well and suffer from spontaneous cell death, but are at the same time more resistant to pathogens. Known instances of hybrid necrosis generally involve epistatic interaction between unlinked loci, and are often caused by relatively rare and/or geographically distant alleles. We identified the first case of single-locus hybrid necrosis, in which interactions between two classes of natural alleles of the ACCELERATED CELL DEATH 6 (ACD6) gene lead to the activation of the Arabidopsis thaliana immune system. One of these allelic classes has recently evolved by partial resurrection of a pseudogene, and each class includes multiple functional variants. The two classes are particularly common in the Northeast of Spain, suggesting a role in local adaptation. In this area, these alleles co-exist in natural populations, and hybrid individuals carrying combinations of the two ACD6 allelic classes can be found as well. The extensive functional variation among ACD6 alleles points to a central role of this locus in fine-tuning pathogen defenses in natural populations