Natural variation in a FtMYB32-FtCES18 module drives Rhizoctonia solani resistance by reprogramming jasmonate and flavonoid metabolism in Tartary buckwheat

Abstract

Tartary buckwheat (Fagopyrum tataricum) is renowned for its adaptability to complex growing conditions and stress tolerance. However, soil-borne necrotrophic pathogens such as Rhizoctonia solani frequently cause devastating diseases that severely compromise its yield and quality. In this study, through a genome-wide association study (GWAS), we identified a carboxylesterase gene, FtCES18, and demonstrated that it acts as a core positive regulator of disease resistance in Tartary buckwheat. Overexpression of FtCES18 significantly enhanced plant resistance, whereas virus-induced gene silencing (VIGS) led to a highly susceptible phenotype. Further analyses revealed that FtCES18 efficiently catalyzes the hydrolysis of methyl jasmonate (MeJA) into free jasmonic acid (JA), which initiates downstream JA-Ile signaling and rapidly promotes endogenous jasmonate accumulation upon pathogen infection. This JA signaling cascade reprograms host flavonoid metabolism, promoting the substantial accumulation of downstream defensive flavonoids (such as rutin and quercetin). Furthermore, we found that the transcription factor FtMYB32 directly binds to the MBS cis-element in the FtCES18 promoter to activate its expression. Notably, evolutionary analysis revealed a domestication-associated C-terminal truncation in the cultivated FtMYB32 that impairs its transactivation capacity, explaining the compromised basal resistance in cultivated accessions compared to their wild ancestors. Crucially, a natural single-nucleotide polymorphism (SNP) in the FtMYB32 promoter defines a superior haplotype (hapC) conferring enhanced basal transcriptional activity. This natural variation in promoter activity controls the expression abundance of the FtMYB32-FtCES18 module via a “dosage fine-tuning” effect, which is subsequently amplified by the downstream metabolic cascade, ultimately contributing to the natural variation in disease resistance among different Tartary buckwheat accessions. This study provides valuable genetic resources and a theoretical basis for breeding novel Tartary buckwheat varieties with high disease resistance.