New biologically relevant resistance to bacterial wilt in heat-stressed tomato revealed by two-reference Genome Wide Association

Abstract

Ongoing climate change is driving unprecedented environmental fluctuations, with extreme events predicted to increase in frequency, intensity and duration. Among climatic parameters, temperature is expected to fluctuate the most by the end of the century and its elevation has already demonstrated to pose a major challenge to plant health. In this context, understanding how temperature modulates plant-pathogen interactions and their underlying genetic architecture is critical. Bacterial wilt, caused by strains of the Ralstonia solanacearum species complex, is a devastating disease affecting many plant species. Genetic resistance remains the most effective control strategy. In tomato, resistance is quantitative and mostly relies on quantitative trait loci (QTLs) bwr-6 and bwr-12. However, as in other crops, high temperature and humidity can compromise this resistance in commercial tomato cultivars. We investigated temperature-dependent quantitative disease resistance (QDR) using a panel of 189 wild tomato accessions, predominantly Solanum pimpinellifolium, representing genetic diversity from contrasting ecological conditions. Disease progression was monitored from three to ten days post-inoculation at 28 °C and 32 °C, using a time-course phenotyping approach. Genome-wide association (GWA) analyses were performed, based on daily symptom scores and two reference genomes, to account for structural variations and improve QTL detection. This strategy identified 44 candidate genes and revealed a temporally dynamic genetic architecture of the plant response. Strikingly, no candidate genes were shared between temperatures, supporting distinct genetic determinants under different temperature conditions. Many candidate genes were expressed in roots and belong to gene families involved in plant immunity, with two candidates co-localizing with bwr-6 and bwr-12, whose causal genes remain unknown. Altogether, our findings demonstrate that resistance to bacterial wilt in wild tomato is flexible, environment-dependent, and temporally dynamic, highlighting the importance of integrating environmental context and genomic diversity to better understand plant-pathogen interactions.