A thaumatin-like effector protein suppresses the rust resistance of wheat and promotes the pathogenicity of Puccinia triticina by targeting TaRCA.

Thaumatin-like proteins (TLPs) in plants play a crucial role in combating stress, and they have been proven to possess antifungal properties. However, the role of TLPs in pathogens has not been reported. We identified a effector protein, Pt9029, which contained a Thaumatin domain in Puccinia triticina (Pt), possessing a chloroplast transit peptide and localized in the chloroplasts. Silencing Pt9029 in the Pt physiological race THTT resulted in a notable reduction in virulence and stunted growth and development of Pt hypha in near-isogenic wheat line TcLr2b. Overexpression of Pt9029 in wheat exerted a suppressive effect on HO production, consequently impeding the wheat's disease resistance mechanisms. The TLP domain of Pt9029 targets the Rubisco activase (TaRCA) in chloroplasts. This interaction effectively inhibited the function of TaRCA, subsequently leading to a decrease in Rubisco enzyme activity. Therefore, this indicates that TLPs in Pt can inhibit host defense mechanisms during the pathogenic process of Pt. Moreover, TaRCA silencing resulted in reduced resistance of TcLr2b against Pt race THTT. This clearly demonstrated that TaRCA positively regulates wheat resistance to leaf rust. These findings reveal a novel strategy exploited by Pt to manipulate wheat rust resistance and promote pathogenicity.