Repeated loss of the ability of a disease resistance gene to function at high temperatures suggests that thermoresist

Specificity in plant-pathogen gene-for-gene interactions is determined by the recognition of pathogen proteins by the products of plant resistance (R) genes. R gene resistance is predicted to be costly to the host, but evidence for this prediction is limited. R gene resistance is most often thermosensitive, being only expressed at temperatures below 30ºC. The evolutionary dynamics of R genes has been mostly analysed in plant-bacteria and plant-fungi interactions, with few studies of plant-virus systems.

We analysed the evolution of the L resistance locus to tobamoviruses in the wild pepper Capsicum annuum var. glabriusculum (chiltepin), a crop relative undergoing incipient domestication. We estimated the frequency of the L locus in 41 chiltepin populations under different levels of human management over its distribution range in Mexico. The frequency of resistance was lower in cultivated than in wild chiltepin populations. L-locus genetic diversity showed a strong spatial structure, with a pattern that suggests environment-specific selection, possibly associated to infection by the highly virulent tobamoviruses found in the surveyed regions. There was a large allelic diversity at L, and alleles differed in recognition specificity and in the expression of resistance at different temperatures.

Broad-spectrum recognition of more than one pathotype and expression of resistance above 32ºC were found to be ancestral traits that were repeatedly lost along L-locus evolution. Overall, our study indicates that loss of resistance co-occurs with incipient domestication and broad-spectrum resistance expressed at high temperatures has fitness costs.

These findings contribute to understand the role of fitness trade-offs in plant-virus co-evolution.

Image: Network representing the genetic and phenotypic diversity of L alleles (left) and expressions of resistance/susceptibility (right).

Original Paper: Poulicard, N., Pagán, I., González-Jara, P., Mora, M.Á., Hily, J.-M., Fraile, A., Piñero, D., García-Arenal, F. 2023. Repeated loss of the ability of a wild pepper disease resistance gene to function at high temperatures suggests that thermoresistance is a costly trait. New Phytologist. DOI: 10.1111/nph.19371