Multiomics analysis reveals the molecular mechanisms underlying virulence in Rhizoctonia and jasmonic acid–mediated resistance in Tartary buckwheat (Fagopyrum tataricum)

Abstract

Rhizoctonia solani is a devastating soil-borne pathogen that seriously threatens the cultivation of economically important crops. Multiple strains with a very broad host range have been identified, but only one (AG1-IA, which causes rice sheath blight disease) has been examined in detail. Here, we analyzed AG4-HGI 3 originally isolated from Tartary buckwheat (Fagopyrum tataricum), but with a host range comparable to AG1-IA. Genome comparison reveals abundant pathogenicity genes in this strain. We used multi-omics approaches to improve the efficiency of screening for disease resistance genes. Transcriptomes of the plant-fungi interaction identified differentially expressed genes associated with virulence in Rhizoctonia and resistance in Tartary buckwheat. Integration with jasmonate-mediated transcriptome and metabolome changes revealed a negative regulator of jasmonate signaling, cytochrome P450 (FtCYP94C1), as increasing disease resistance probably via accumulation of resistance-related flavonoids. The integration of resistance data for 320 Tartary buckwheat accessions identified a gene homologous to aspartic proteinase (FtASP), with peak expression following R. solani inoculation. FtASP exhibits no proteinase activity but functions as an antibacterial peptide that slows fungal growth. This work reveals a potential mechanism behind pathogen virulence and host resistance, which should accelerate the molecular breeding of resistant varieties in economically essential crops.

Multi‐omics identification of a key glycosyl hydrolase gene FtGH1 involved in rutin hydrolysis in Tartary buckwheat (Fagopyrum tataricum)

“…Previous studies have shown that the accumulation of flavonoids in Tartary buckwheat can increase plant resistance to Rhizoctonia solani (He et al ., 2023 ). As the overexpression of FtbHLH165 could increase the content of flavonoids in Tartary buckwheat hairy roots (Figure 5i ), the disease resistance of FtbHLH165 was further investigated.…”

“…Our results revealed that some flavonoids including nicotiflorin, afzelin, and rutin accumulated in FtbHLH165 overexpression lines (Figure 6h ). As these metabolites were previously shown to enhance plant disease resistance (He et al ., 2023 ; Yang et al ., 2016 ), we speculate that FtbHLH165 might enhance plant resistance to R. solani through increasing flavonoid biosynthesis.…”

“…Plants often face a wide variety of adversities such as UV, drought, disease, and other stresses in their natural environment. However, rutin, as a flavonoid produced by secondary metabolism, is of great importance to both the plant itself (He et al ., 2023 ) and to humans (Ola et al ., 2015 ; Xu et al ., 2014 ). As an important factor for balancing rutin metabolism, rutin hydrolase is not agriculturally favoured.…”

“…For R. solani infected A. thaliana , isolated leaves of two‐week‐old Arabidopsis seedlings were inoculated with sub‐cultured mycelial disks and incubated with 28 °C for 24 h according to methods described previously (He et al ., 2023 ). For R. solani infected tobacco leaves, FtbHLH165 was transiently overexpressed in tobacco leaves for 48 h. And the isolated leaves were inoculated with R. solani according to methods described previously (He et al ., 2023 ). The phenotypes were observed after 24 h. Three biological replicates were performed and the experiment was carried out three times.…”

Genomic insight into the origin, domestication, dispersal, diversification and human selection of Tartary buckwheat

“…As the food crop with the closest phylogenetic relationship to these pharmaceutical plants, buckwheat is generally considered to have more abundant bioactive substances than other more widespread main grain crops of the Poaceae [ 5 ]. Besides these health promoting effects, these substances are usually present due to their role in plant defense against biotic and abiotic stress [ 6 , 7 ]. At present, there are two most widely cultivated buckwheat species, including self-pollinated Tartary buckwheat and self-incompatible common buckwheat [ 8 ].…”