A truncated CC-NB-ARC gene TaRPP13L1-3D positively regulates powdery mildew resistance in wheat via the RanGAP-WPP complex-mediated nucleocytoplasmic shuttle

Main Conclusion A wheat RPP13-like isoform interacting with WPP1 contributes to quantitative and/or basal resistance to powdery mildew (Blumeria graminis f. sp. tritici) by restricting the development of Bgt conidia. Plant disease resistance (R) genes confer an ability to resist infection by pathogens expressing specific avirulence genes. Recognition of Peronospora parasitica 13-like (RPP13-like) genes belong to the nucleotide-binding site and leucine-rich repeat (NBS-LRR) superfamily and play important roles in resistance to various plant diseases. Previously, we detected a TaRPP13-like gene located on chromosome 3D (TaRPP13L1-3D) in the TaSpl1 resided region, which is strongly induced by the cell death phenotype (Zhang et al. 2021). Here, we investigated the expression and functional role of TaRPP13L1-3D in wheat responding to fungal stress. TaRPP13L1-3D encoded a typical NB-ARC structure characterized by Rx-N and P-loop NTPase domains. TaRPP13L1-3D transcripts were strongly upregulated in wheat by powdery mildew (Blumeria graminis f. sp. tritici; Bgt) and stripe rust (Puccinia striiformis f. sp. tritici; Pst) infection although opposing expression patterns were observed in response to wheat-Bgt in incompatible and compatible backgrounds. Overexpression of TaRPP13L1-3D enhanced disease resistance to Bgt, accompanied by upregulation of the defense-related marker genes encoding phytoalexin-deficient4 (PAD4), thaumatin-like protein (TLP) and chitinase 8-like protein (Chi8L), while silencing of TaRPP13L1-3D disrupted the resistance to Bgt infection. Subcellular localization studies showed that TaRPP13L1-3D is located in both the plasma membrane and nucleus, while yeast-two-hybrid (Y2H) assays indicated that TaRPP13L1-3D interacts with WPP domain-containing protein 1 (TaWPP1). This indicates that TaRPP13L1-3D shuttles between the nucleus and cytoplasm membrane via a mechanism that is mediated by the RanGAP-WPP complex in nuclear pores. This insight into TaRPP13L1-3D will be useful in dissecting the mechanism of fungal resistance in wheat, and understanding the interaction between R gene expression and pathogen defense.

Automated summary

In wheat, TaRPP13L1-3D contributes to quantitative and/or basal resistance to powdery mildew by interacting with WPP1 and restricting the development of Bgt conidia. TaRPP13L1-3D is strongly upregulated in response to powdery mildew and stripe rust infections, and its overexpression enhances resistance to powdery mildew, while silencing it disrupts resistance.