A papain-like cysteine protease-released small signal peptide confers wheat resistance to WYMV infection

Soil-borne virus disease caused by wheat yellow mosaic virus (WYMV) poses a serious threat to wheat production in many countries. In this multiomic study, we have identified a novel WYMV resistance gene, TaRD21A, that belongs to the papain-like cysteine protease family. Genetic manipulation of TaRD21A expression confirmed its positive role in the regulation of wheat WYMV resistance. We also found that the TaRD21A-mediated plant antiviral response relies on a small peptide released via TaRD21A activity. To counteract wheat resistance, WYMV-encoded NIa interferes with TaRD21A activity to ensure virus infection. A natural TaRD21A variant in resistant cultivars has a glycine-to-threonine substitution such that the residue threonine can be phosphorylated, weakening the interaction between NIa and TaRD21A. A large-scale survey indicated that the resistant allele of TaRD21A is present in only 13.5% of selected germplasm panels around the world and has great potential to be exploited in breeding for WYMV resistance. Our study. has revealed a novel WYMV resistance gene and provides new insights into the WYMV resistance mechanism.