Reprogramming of phytopathogen transcriptome by a non-bactericidal pesticide residue alleviates its virulence in rice

Bacteria equipped with virulence systems based on highly bioactive small molecules can circumvent their host???s defense mechanisms. Pathogens employing this strategy are currently threatening global rice production. In the present study, variations in the virulence of the highly destructive Burkholderia plantarii were observed in different rice-producing regions. The environment-linked variation was not attributable to any known host-related or external factors. Co-occurrence analyses indicated a connection between reduced virulence and 5-Amino-1,3,4-thiadiazole-2-thiol (ATT), a non-bactericidal organic compound. ATT, which accumulates in rice plants during metabolization of specific agrochemicals, was found to reduce virulence factor secretion by B. plantarii up to 88.8% and inhibit pathogen virulence by hijacking an upstream signaling cascade. Detailed assessment of the newly discovered virulence inhibitor resulted in mechanistic insights into positive effects of ATT accumulation in plant tissues. Mechanisms of virulence alleviation were deciphered by integrating high-throughput data, gene knockout mutants, and molecular interaction assays. TroK, a histidine protein kinase in a two-component system that regulates virulence factor secretion, is likely the molecular target antagonized by ATT. Our findings provide novel insights into virulence modulation in an important plant-pathogen system that relies on the host???s metabolic activity and subsequent signaling interference.

Automated summary

Bacteria equipped with virulence systems based on highly bioactive small molecules can evade host defense mechanisms. In this study, variations in the virulence of Burkholderia plantarii, a highly destructive pathogen threatening rice production, were observed in different rice-producing regions. The variation in virulence was not due to known host-related or external factors, but rather linked to the accumulation of the non-bactericidal organic compound 5-Amino-1,3,4-thiadiazole-2-thiol (ATT). ATT reduced virulence factor secretion and inhibited pathogen virulence by interfering with an upstream signaling cascade. Mechanistic insights revealed that the histidine protein kinase TroK is likely the molecular target antagonized by ATT. This study provides novel insights into virulence modulation in a plant-pathogen system that relies on host metabolic activity and subsequent signaling interference.