MdMYB54 reduces disease severity caused by Fusarium solani in apple by modulating cell wall cellulose and pectate lyase-dependent defense

The plant cell wall is the first barrier against pathogen invasion. Fusarium solani is the primary pathogen responsible for apple replant disease. In this study, we identified an MYB protein, MdMYB54, which interacts with the positive regulator of F. solani resistance, MdERF114, and confers apple-increased tolerance against F. solani. The cellulose synthetase (CESA) gene MdCesA6 and pectin lyase-like (PLL) genes MdPLL8 and MdPLL12 were screened as three potential downstream target genes of MdMYB54 using DAP-seq. The results of electrophoretic mobility shift and yeast one-hybrid assays showed that MdMYB54 directly binds to the promoters of MdCesA6, MdPLL8, and MdPLL12 in vivo and in vitro. Dual-luciferase and β-glucuronidase assays showed that MdMYB54 activates the expression of these genes. The cellulose content and pectin lyase activity of MdMYB54-overexpressed roots were significantly higher than those of wild-type plants under F. solani treatment but were the opposite in MdMYB54-RNAi roots. The deposition of cellulose enhanced the physical barrier of the plant cell wall, whereas the activation of pectin lyase promoted the formation of oligogalacturonides and the production of reactive oxygen species. Overexpression of MdCesA6, MdPLL8, and MdPLL12 in the root system enhanced the tolerance of apple to F. solani. The direct interaction of MdERF114 with MdMYB54 enhanced MdMYB54-mediated cell wall defense response. These results suggest that modifying these candidate genes may provide a strategy for improving the resistance of apple to F. solani.