TaSPX3 Enhances Wheat Resistance to Leaf Rust by Antagonising TaDi19‐Mediated Repression of Pathogenesis‐Related Genes

Abstract

Wheat leaf rust, caused by Puccinia triticina (Pt), threatens global wheat production, with yield losses further exacerbated by the pathogen's evolving virulence. Although Syg1/Pho81/Xpr1 (SPX) domain‐containing proteins are known regulators of phosphate homeostasis, their involvement in plant–pathogen interactions remains largely unexplored. We demonstrated that TaSPX3, a wheat SPX family gene, is rapidly induced during early Pt infection and flg22 treatment. Genetic evidence indicates that TaSPX3 is a positive regulator of rust resistance, with knockdown lines showing increased susceptibility and overexpression lines exhibiting enhanced resistance. Using yeast two‐hybrid screening, we identified TaDi19‐1D, a zinc finger transcription factor, as a direct TaSPX3 interactor. TaDi19‐1D functions as a negative immune regulator by suppressing the expression of pathogenesis‐related (PR) genes (TaPR1, TaPR2, TaPR5) through direct promoter binding. TaSPX3 counteracts this repression by physically interacting with TaDi19‐1D, thereby derepressing PR gene expression and boosting wheat resistance to Pt. Our findings revealed a novel TaSPX3–TaDi19 regulatory module that fine‐tunes TaPRs expression, providing mechanistic insights into pattern‐triggered immunity (PTI) and potential genetic targets for breeding durable broad‐spectrum disease‐resistant wheat varieties.