The ptsG Gene Encoding the Major Glucose Transporter of Bacillus cereus C1L Participates in Root Colonization and Beneficial Metabolite Production to Induce Plant Systemic Disease Resistance

Abstract

Rhizosphere interactions between microorganisms and plants have great influence on plant health. Bacillus cereus C1L, an induced systemic resistance (ISR)-eliciting rhizobacterium from Lilium formosanum, can protect monocot and dicot plants from disease challenges. To identify the ISR-involved bacterial genes, the systemic protection effect of transposon-tagged mutants of B. cereus C1L against southern corn leaf blight (SCLB) was surveyed, and a mutant of the ptsG gene encoding glucose-specific permease of the phosphotransferase system was severely impaired in the abilities of disease suppression and root colonization. The ptsG mutant lost the preferential utilization of glucose and showed reduction of glucose-assisted growth in minimal medium. A promoter-based reporter assay revealed that ptsG expression could be activated by certain sugar constituents of maize root exudates, among which B. cereus C1L exhibited the highest chemotactic response toward glucose, whereas neither of them could attract the ptsG mutant. Additionally, ptsG deficiency almost completely abolished glucose uptake of B. cereus C1L. Metabolite analysis indicated that the lack of ptsG undermined glucose-induced accumulation of acetoin and 2,3-butanediol in B. cereus C1L, both eliciting maize ISR against SCLB. Pretreatments with B. cereus C1L, ptsG mutant, acetoin, and 2,3-butanediol enhanced defense-related reactive oxygen species accumulation and callose deposition at different levels that were positively correlated to their ISR-eliciting activities. Thus, glucose uptake–mediating ptsG participates in ISR elicitation by endowing B. cereus C1L with the full capacities for root colonization and beneficial glucose metabolite production, providing a clue regarding how ISR-mediating rhizobacteria create a mutually beneficial relationship with various plant species.