Natural allelic variation underlying a major fitness tradeoff in Arabidopsis thaliana

Plants can defend themselves against a wide array of enemies, yet one of the most striking observations is the variability in the effectiveness of such defences, both within and between species. Some of this variation can be explained by conflicting pressures from pathogens with different modes of attack1. A second explanation comes from an evolutionary tug of war, in which pathogens adapt to evade detection, until the plant has evolved new recognition capabilities for pathogen invasion2-5. If selection is, however, sufficiently strong, susceptible hosts should remain rare. That this is not the case is best justified by costs incurred from constitutive defences in a pest free environment6-11. Using a combination of forward genetics and genome-wide association analyses, we demonstrate that allelic diversity at a single locus, ACCELERATED CELL DEATH 6 (ACD6)12,13, underpins dramatic pleiotropic differences in both vegetative growth and resistance to microbial infection and herbivory among natural Arabidopsis thaliana strains. A hyperactive ACD6 allele, compared to the reference allele, strongly enhances resistance to a broad range of pathogens from different phyla, but at the same time slows the production of new leaves and greatly reduces the biomass of mature leaves. This allele segregates at intermediate frequency both throughout the worldwide range of A. thaliana and within local populations, consistent with this allele providing substantial fitness benefits despite its drastic impact on growth.