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Ralstonia solanacearum  gram‐negative phytopathogenic bacterium exerts its virulence through a type III secretion system (T3SS) that translocates type III effectors (T3Es) directly into the host cells. T3E secretion is finely controlled at the posttranslational level by helper proteins, T3SS control proteins, and type III chaperones. The HpaP protein, one of the type III secretion substrate specificity switch (T3S4) proteins, was previously highlighted as a virulence factor on  Arabidopsis thaliana  Col‐0 accession. In this study, we set up a genome‐wide association analysis to explore the natural diversity of response to the  hpaP  mutant of two  A. thaliana  mapping populations: a worldwide collection and a local population. Quantitative genetic variation revealed different genetic architectures in both mapping populations, with a global delayed response to the  hpaP  mutant compared to the GMI1000 wild‐type strain. We have identified several quantitative trait loci (QTLs) associated with the  hpaP  mutant inoculation. The genes underlying these QTLs are involved in different and specific biological processes, some of which were demonstrated important for  R .  solanacearum  virulence. We focused our study on four candidate genes,  RKL1 ,  IRE3 ,  RACK1B , and  PEX3 , identified using the worldwide collection, and validated three of them as susceptibility factors. Our findings demonstrate that the study of the natural diversity of plant response to a  R .  solanacearum  mutant in a key regulator of virulence is an original and powerful strategy to identify genes directly or indirectly targeted by the pathogen.

molecular plant pathology

Study of natural diversity in response to a key pathogenicity regulator of  Ralstonia solanacearum  reveals new susceptibility genes in  Arabidopsis thaliana