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The Wheat Wall-Associated Receptor-Like Kinase TaWAK-6D Mediates Broad Resistance to Two Fungal Pathogens Fusarium pseudograminearum and Rhizoctonia cerealis

ABSTRACT: The soil-borne fungi Fusarium pseudograminearum and Rhizoctonia cerealis are the major pathogens for the economically important diseases Fusarium crown rot (FCR) and sharp eyespot of common wheat (Triticum aestivum), respectively. However, there has been no report on the broad resistance of wheat genes against both F. pseudograminearum and R. cerealis. In the current study, we identified TaWAK-6D, a wall-associated kinase (WAK) which is an encoding gene located on chromosome 6D, and demonstrated its broad resistance role in the wheat responses to both F. pseudograminearum and R. cerealis infection. TaWAK-6D transcript induction by F. pseudograminearum and R. cerealis was related to the resistance degree of wheat and the gene expression was significantly induced by exogenous pectin treatment. Silencing of TaWAK-6D compromised wheat resistance to F. pseudograminearum and R. cerealis, and repressed the expression of a serial of wheat defense-related genes. Ectopic expression of TaWAK-6D in Nicotiana benthamiana positively modulated the expression of several defense-related genes. TaWAK-6D protein was determined to localize to the plasma membrane in wheat and N. benthamiana. Collectively, the TaWAK-6D at the plasma membrane mediated the broad resistance responses to both F. pseudograminearum and R. cerealis in wheat at the seedling stage. This study, therefore, concludes that TaWAK-6D is a promising gene for improving wheat broad resistance to FCR and sharp eyespot.

SUBMITTER: Qi H

PROVIDER: S-EPMC8579037 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Wheat sharp eyespot caused by Rhizoctonia cerealis is primarily a severe threat to worldwide wheat production. Currently, there are no resistant wheat cultivars, and the use of fungicides is the primary method for controlling this disease. Elucidating the mechanisms of R. cerealis pathogenicity can accelerate the pace of the control of this disease. Long intergenic noncoding RNAs (lincRNAs) that function in plant-pathogen interactions might provide a new perspective. We systematically analyzed lincRNAs and identified a total of 1,319 lincRNAs in R. cerealis. We found that lincRNAs are involved in various biological processes, as shown by differential expression analysis and weighted correlation network analysis (WGCNA). Next, one of nine hub lincRNAs in the blue module that was related to infection and growth processes, MSTRG.4380.1, was verified to reduce R. cerealis virulence on wheat by a host-induced gene silencing (HIGS) assay. Following that, RNA sequencing (RNA-Seq) analysis revealed that the significantly downregulated genes in the MSTRG.4380.1 knockdown lines were associated mainly with infection-related processes, including hydrolase, transmembrane transporter, and energy metabolism activities. Additionally, 23 novel microRNAs (miRNAs) were discovered during small RNA (sRNA) sequencing (sRNA-Seq) analysis of MSTRG.4380.1 knockdown, and target prediction of miRNAs suggested that MSTRG.4380.1 does not act as a competitive endogenous RNA (ceRNA). This study performed the first genome-wide identification of R. cerealis lincRNAs and miRNAs. It confirmed the involvement of a lincRNA in the infection process, providing new insights into the mechanism of R. cerealis infection and offering a new approach for protecting wheat from R. cerealis. IMPORTANCE Rhizoctonia cerealis, the primary causal agent of wheat sharp eyespot, has caused significant losses in worldwide wheat production. Since no resistant wheat cultivars exist, chemical control is the primary method. However, this approach is environmentally unfriendly and costly. RNA interference (RNAi)-mediated pathogenicity gene silencing has been proven to reduce the growth of Rhizoctonia and provides a new perspective for disease control. Recent studies have shown that lincRNAs are involved in various biological processes across species, such as biotic and abiotic stresses. Therefore, verifying the function of lincRNAs in R. cerealis is beneficial for understanding the infection mechanism. In this study, we reveal that lincRNAs could contribute to the virulence of R. cerealis, which provides new insights into controlling this pathogen.

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The Wheat Wall-Associated Receptor-Like Kinase TaWAK-6D Mediates Broad Resistance to Two Fungal Pathogens Fusarium pseudograminearum and Rhizoctonia cerealis

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