Inhibition of Xanthomonas growth by bioactive volatiles from Pseudomonas sp. triggers remarkable changes in the phytopathogen transcriptome

Abstract

Volatile organic compounds (VOCs) produced by microorganisms may have a noteworthy role in the control of plant pathogens. Xanthomonas are a well-studied group of phytobacteria that cause diverse diseases in economically important crops worldwide. Key species that infect sugarcane are X. albilineans (Xab) and X. axonopodis pv. vasculorum (Xav). Here, we investigated VOC-producing bacteria with antagonistic effects against Xab and Xav. We demonstrated that VOCs produced by Pseudomonas sp. V5-S-D11 was able to abolish the growth of these pathogens. A set of 32 VOCs was identified in the volatilome of V5-S-D11, with 10 showing a concentration-dependent inhibitory effect on both phytobacteria. Among them, dimethyl disulfide (DMDS), a volatile sulfur compound, has the potential to be biotechnologically explored in agriculture since it can improve plant growth and induce systemic resistance against plant pathogens. Interestingly, transcriptomic analysis of Xab treated with DMDS revealed several up-regulated metabolic pathways such as a two-component system, flagellar assembly, chemotaxis, and a bacterial secretion system. Although the ethanol (ETOH) used as DMDS solvent did not inhibit Xab growth, it triggered a similar up-regulation of some genes, indicating that this phytopathogen can deal with ETOH better than DMDS. Overall, this study explores the wide role of VOCs in the interactions with bacteria. Moreover, our results indicate that VOCs from Pseudomonas sp. may represent a novel biotechnological strategy to counteract diseases caused by Xanthomonas species and can be further exploited for sustainable approaches in agriculture.