This study aimed to explore potential biocontrol mechanisms involved in the interference of antagonistic bacteria with fungal pathogenicity in planta . To do this, we conducted a comparative transcriptomic analysis of the “take-all” pathogenic fungus Gaeumannomyces graminis var. tritici ( Ggt ) by examining Ggt -infected wheat roots in the presence or absence of the biocontrol agent Bacillus velezensis CC09 ( Bv ) compared with Ggt grown on potato dextrose agar (PDA) plates. A total of 4,134 differentially expressed genes (DEGs) were identified in Ggt -infected wheat roots, while 2,011 DEGs were detected in Bv + Ggt -infected roots, relative to the Ggt grown on PDA plates. Moreover, 31 DEGs were identified between wheat roots, respectively infected with Ggt and Bv + Ggt , consisting of 29 downregulated genes coding for potential Ggt pathogenicity factors – e.g., para-nitrobenzyl esterase, cutinase 1 and catalase-3, and two upregulated genes coding for tyrosinase and a hypothetical protein in the Bv + Ggt -infected roots when compared with the Ggt -infected roots. In particular, the expression of one gene, encoding the ABA3 involved in the production of Ggt ’s hormone abscisic acid, was 4.11-fold lower in Ggt -infected roots with Bv than without Bv . This is the first experimental study to analyze the activity of Ggt transcriptomes in wheat roots exposed or not to a biocontrol bacterium. Our results therefore suggest the presence of Bv directly and/or indirectly impairs the pathogenicity of Ggt in wheat roots through complex regulatory mechanisms, such as hyphopodia formation, cell wall hydrolase, and expression of a papain inhibitor, among others, all which merit further investigation.
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.
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