Plant growth-promoting rhizobacteria, in association with plant roots, can trigger induced systemic resistance (ISR). Considering that low-molecular weight volatile hormone analogues such as methyl jasmonate and methyl salicylate can trigger defense responses in plants, we examined whether volatile organic compounds (VOCs) associated with rhizobacteria can initiate ISR. In Arabidopsis seedlings exposed to bacterial volatile blends from Bacillus subtilis GB03 and Bacillus amyloliquefaciens IN937a, disease severity by the bacterial pathogen Erwinia carotovora subsp. carotovora was significantly reduced compared with seedlings not exposed to bacterial volatiles before pathogen inoculation. Exposure to VOCs from rhizobacteria for as little as 4 d was sufficient to activate ISR in Arabidopsis seedlings. Chemical analysis of the bacterial volatile emissions revealed the release of a series of low-molecular weight hydrocarbons including the growth promoting VOC (2R,3R)-(-)-butanediol. Exogenous application of racemic mixture of (RR) and (SS) isomers of 2,3-butanediol was found to trigger ISR and transgenic lines of B. subtilis that emitted reduced levels of 2,3-butanediol and acetoin conferred reduced Arabidopsis protection to pathogen infection compared with seedlings exposed to VOCs from wild-type bacterial lines. Using transgenic and mutant lines of Arabidopsis, we provide evidence that the signaling pathway activated by volatiles from GB03 is dependent on ethylene, albeit independent of the salicylic acid or jasmonic acid signaling pathways. This study provides new insight into the role of bacteria VOCs as initiators of defense responses in plants.

Summary: Photosynthesis is regulated by environmental factors as well as endogenous sugar signals. Whereas light‐driven sugar biosynthesis is essential for terrestrial organisms, as well as belowground microflora, whether and how soil symbionts regulate photosynthesis has yet to be reported. Here, we show that the plant growth‐promoting soil bacterium Bacillus subtilis GB03 augments photosynthetic capacity by increasing photosynthetic efficiency and chlorophyll content in Arabidopsis. Mechanistic studies reveal an elevation of sugar accumulation as well as the suppression of classic glucose signaling responses, including hypocotyl elongation and seed germination, with exposure to GB03. Compared with wild‐type plants, two Arabidopsis mutants defective in hexokinase‐dependent sugar signaling exhibit increased photosynthetic capacity, which is not further enhanced with GB03 exposure. Overlap in sugar/ABA sensing is observed in GB03‐exposed plants, with a reduction of ABA‐biosynthetic transcripts as well as downstream metabolite levels in leaves. Moreover, exogenous ABA abrogates GB03‐triggered increases in photosynthetic efficiency and chlorophyll content. These results demonstrate that certain rhizobacteria elevate photosynthesis through the modulation of endogenous sugar/ABA signaling, and establish a regulatory role for soil symbionts in plant acquisition of energy.

Flavonoids are stress-inducible metabolites important for plant-microbe interactions. In contrast to their well-known function in initiating rhizobia nodulation in legumes, little is known about whether and how flavonoids may contribute to plant stress resistance through affecting non-nodulating bacteria. Here we show that flavonoids broadly contribute to the diversity of the Arabidopsis root microbiome and preferentially attract Aeromonadaceae, which included a cultivable Aeromonas sp. H1 that displayed flavonoid-induced chemotaxis with transcriptional enhancement of flagellum biogenesis and suppression of fumarate reduction for smooth swims. Strain H1 showed multiple plant-beneficial traits and enhanced plant dehydration resistance, which required flavonoids but not through a sudden “cry-for-help” upon stress. Strain H1 boosted dehydration-induced H₂O₂ accumulation in guard cells and stomatal closure, concomitant with synergistic induction of jasmonic acid-related regulators of plant dehydration resistance. These findings revealed a key role of flavonoids, and the underlying mechanism, in mediating plant-microbiome interactions including the bacteria-enhanced plant dehydration resistance.