Bacillus-Secreted Oxalic Acid Induces Tomato Resistance Against Gray Mold Disease Caused by Botrytis cinerea by Activating the JA/ET Pathway

Bacillus spp. are known for their ability to control plant diseases; however, the mechanism of disease control by Bacillus spp. is still unclear. Previously, bacterial organic acids have been im-plicated in the process of disease suppression. We extracted the total organic acid from Bacillus cereus AR156 culture filtrate and identified oxalic acid (OA) as the programmed cell death- inducing factor. OA strongly suppressed the lesion caused by Botrytis cinerea without significant antagonism against the fun-gus. Low concentration of OA produced by Bacillus spp. in-hibited cell death caused by high concentrations of OA in a concentration-and time-dependent manner. Pretreatment with a low concentration of OA led to higher accumulation of ac-tive oxygen-scavenging enzymes in tomato leaves and provoked the expression of defense-related genes. The activation of gene expression relied on the jasmonic acid (JA) signaling pathway but not the salicylic acid (SA) pathway. The disease suppres-sion capacity of OA was confirmed on wild-type tomato and its SA accumulation-deficient line, while the control effect was di-minished in JA synthesis-deficient mutant, suggesting that the OA-triggered resistance relied on JA and ethylene (ET) signal-ing transduction. OA secretion ability was widely distributed among the tested Bacillus strains and the final environmental OA concentration was under strict regulation by a pH-sensitive degradation mechanism. This study provides the first system-atic analysis on the role of low-concentration OA secreted and maintained by Bacillus spp. in suppression of gray mold disease and determines the dependence of OA-mediated resistance on the JA/ET signaling pathway.