Translationally controlled tumor protein interacts with TaCIPK23 to positively regulate wheat resistance to Puccinia triticina

SUMMARY Hypersensitive response‐programmed cell death (HR‐PCD) regulated by Ca2+ signal is considered the major regulator of resistance against Puccinia triticina (Pt.) infection in wheat. In this study, the bread wheat variety Thatcher and its near‐isogenic line with the leaf rust resistance locus Lr26 were infected with the Pt. race 260 to obtain the compatible and incompatible combinations, respectively. The expression of translationally controlled tumor protein (TaTCTP) was upregulated upon infection with Pt., through a Ca2+‐dependent mechanism in the incompatible combination. The knockdown of TaTCTP markedly increased the area of dying cell and the number of Pt. haustorial mother cells (HMCs) at the infection sites, whereas plants overexpressing the gene exhibited enhanced resistance. The interaction between TaTCTP and calcineurin B‐like protein‐interacting protein kinase 23 (TaCIPK23) was also investigated, and the interaction was found occurred in the endoplasmic reticulum. TaCIPK23 phosphorylated TaTCTP in vitro. The expression of a phospho‐mimic TaTCTP mutant in Nicotiana benthamiana promoted HR‐like cell death. Silencing TaCIPK23 or TaCIPK23/TaTCTP co‐silencing resulted in the same results as silencing TaTCTP. This suggested that TaTCTP is a novel phosphorylation target of TaCIPK23, and both participate in the resistance of wheat to Pt. in the same pathway. Significance Statement Wheat leaf rust caused by Puccinia triticina infection causes losses to agriculture worldwide. Calcium signaling and its mediated hypersensitive response are critical for leaf rust resistance in wheat. By demonstrating the phosphorylation of TaTCTP by TaCIPK23 and their contribution to the leaf rust resistance phenotype in wheat, this study reveals the mechanism by which calcium mediates biotic stress resistance and provides valuable insights for future crop improvement strategies.