Crop domestication and pathogen virulence: Interactions of tomato and Botrytis genetic diversity

Abstract

Human selection during crop domestication alters numerous traits, including disease resistance. Studies of qualitative resistance to specialist pathogens typically find decreased resistance in domesticated crops in comparison to their wild relatives. However, less is known about how crop domestication affects quantitative interactions with generalist pathogens. To study how crop domestication impacts plant resistance to generalist pathogens, and correspondingly how this interacts with the pathogens genetics, we infected a collection of wild and domesticated tomato accessions with a genetically diverse population of the generalist pathogen Botrytis cinerea. We quantified variation in lesion size of 97 B. cinerea genotypes (isolates) on 6 domesticated Solanum lycopersicum and 6 wild S. pimpinellifolium genotypes. This showed that lesion size was significantly controlled by plant domestication, plant genetic variation, and the pathogens genotype. Overall, resistance was slightly elevated in the wild germplasm in comparison to domesticated tomato accessions. Genome-wide association (GWA) mapping in B. cinerea identified a highly polygenic collection of genes. This suggests that breeding against this pathogen would need to utilize a diversity of isolates to capture all possible mechanisms. Critically, we identified a discrete subset of B. cinerea genes where the allelic variation was linked to altered virulence against the wild versus domesticated tomato accessions. This indicates that this generalist pathogen already has the necessary allelic variation in place to handle the introgression of wild resistance mechanisms into the domesticated crop. Future studies are needed to assess how these observations extend to other domesticated crops and other generalist pathogens.