Alternative splicing of OsNPR3 promoted by the bacterial TAL effectors-targeted splicing regulator OsRBP11 antagonizes OsNPR1 function and enhances disease susceptibility in rice.

Abstract

Plant proteins that belong to the nonexpressor of pathogenesis-related (NPR) gene family are paralogous receptors of the plant defense hormone salicylic acid and essential regulators of hormone-dependent plant immunity against diseases caused by various pathogens. Previous studies have established NPR1 and NPR3 as a transcriptional activator and a transcriptional repressor, respectively, of defense-gene expression to promote and inhibit broad-spectrum resistance against different strains of pathogens. However, the regulatory mechanism that underlies the opposing roles of NPR1 and NPR3 in defense-gene activation remains unclear. Here, we report that a rice transcript splicing factor, Oryza sativa RNA-binding protein 11 (OsRBP11), promotes alternative splicing of OsNPR3 to modulate the defense function of OsNPR1 in rice plants infected by Xanthomonas oryzae pathovars, which are important bacterial pathogens of rice. We discovered that 11 transcription activator-like effectors identified in representative bacterial strains activate OsRBP11 expression. The OsRBP11 protein, in turn, facilitates alternative splicing of the OsNPR3 mRNA precursor, leading to the production of truncated OsNPR3 protein variants. The OsNPR3 variants exacerbate bacterial diseases by sequestering OsNPR1 from defense-gene activation. By contrast, both artificial and natural variations in OsRBP11 prevent the alternative splicing of OsNPR3, restore the defense function of OsNPR1, and enhance rice resistance to different bacterial strains. These findings not only reveal a novel regulatory pathway exploited by bacterial pathogens to facilitate their pathogenicity and subvert plant defense but also provide a genetic basis for biotechnological strategies aimed at developing broad-spectrum resistance in crops.