Abstract
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.
Highlights
“Take-all” is one of the most severe soil-borne diseases of wheat plants worldwide, caused by the necrotrophic fungus Gaeumannomyces graminis var. tritici (Bithell et al, 2016)
After removing the low-quality reads and adaptors, a total of 67,293,916, 553,791,342, and 553,453,160 clean reads were generated from the mRNA of Gaeumannomyces graminis var. tritici (Ggt) on potato dextrose agar (PDA) and Ggt in wheat roots with and without B. velezensis CC09 (Bv), which accounted for 91.6%, 83.2%, and 84.9% of raw reads, respectively (Supplementary Table S2)
When compared with Ggt grown on PDA, 4,134 differentially expressed genes (DEGs) (2,142 upregulated, 1,992 downregulated) and 2,011 DEGs (957 upregulated, 1,054 downregulated) were identified in Ggt in wheat roots in the absence and presence of Bv, respectively (Supplementary Figure S2A)
Summary
“Take-all” is one of the most severe soil-borne diseases of wheat plants worldwide, caused by the necrotrophic fungus Gaeumannomyces graminis var. tritici (Bithell et al, 2016). Many genes that contribute to Ggt pathogenicity have been identified, such as cellulase, endo-β-1,4-xylanase, pectinase, xylanase, β-1,3exoglucanase, glucosidase, aspartic protease, and β-1,3-glucanase of cell wall degrading enzymes (CWDEs) (Yang et al, 2015) Based on their comparative transcriptome analysis of Ggt in axenic culture and Ggt-infected wheat, Yang et al (2015) recently pointed out that many genes related to signaling, penetration, fungal nutrition, and host colonization are highly expressed during Ggt pathogenesis in wheat roots. We found that Bv could colonize and migrate in plants, leading to a 66.67% disease-control efficacy of take-all and 21.64% of spot blotch, with a single treatment inoculated on roots (Kang et al, 2018) These attributes make Bv a promising biocontrol agent for the long-term and effective protection of wheat from soil-borne and leaf diseases. Through a comparative analysis of Ggt transcriptomes under three different conditions (e.g., grown on PDA, within wheat roots in the presence or absence of Bv), we sought to reveal the possible pathogenicity gene(s) of Ggt and its regulation by Bv in planta during the early infection of wheat roots
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