Tritrophic interactions involving a biocontrol agent, a pathogen, and a plant have been analyzed predominantly from the perspective of the biocontrol agent. To explore the adaptive strategies of wheat in response to beneficial, pathogenic, and combined microorganisms, we performed the first comprehensive transcriptomic, proteomic, and biochemical analysis in wheat roots after exposure to Bacillus velezensis CC09, Gaeumannomyces graminis var. tritici, and their combined colonization, respectively. The transcriptional or translational programming of wheat roots inoculated with beneficial B. velezensis showed mild alterations compared with that of pathogenic G. graminis var. tritici. However, the combination of B. velezensis and G. graminis var. tritici activated a larger transcriptional or translational program than for each single microorganism, although the gene expression pattern was similar to that of individual infection by G. graminis var. tritici, suggesting a prioritization of defense against G. graminis var. tritici infection. Surprisingly, pathogen-associated molecular pattern-triggered immunity and effector-triggered immunity made wheat pretreated with B. velezensis more sensitive to subsequent G. graminis var. tritici infection. Additionally, B. velezensis triggered a salicylic acid (SA)-dependent mode of induced systemic resistance that resembles pathogen-induced systemic acquired resistance. Wheat plants mainly depend on SA-mediated resistance, and not that mediated by jasmonic acid (JA), against the necrotrophic pathogen G. graminis var. tritici. Moreover, SA-JA interactions resulted in antagonistic effects regardless of the type of microorganisms in wheat. Further enhancement of SA-dependent defense responses such as lignification to the combined infection was shown to reduce the level of induced JA-dependent defense against subsequent infection with G. graminis var. tritici. Altogether, our results demonstrate how the hexaploid monocot wheat responds to beneficial or pathogenic microorganisms and prolongs the onset of take-all disease through modulation of cell reprogramming and signaling events.
Keywords: bacterium–plant symbiosis; biocontrol bacteria; fungus–plant interactions; genomics; induced systemic resistance; metabolomics; molecular signaling; omics; phytopathology; plant defense system; plant disease; plant–microbial interaction; proteomics.