A Puccinia striiformis f. sp. tritici effector inhibits high-temperature seedling-plant resistance in wheat

Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1)-induced protein kinase (RIPK) in Arabidopsis belongs to the receptor-like cytoplasmic kinase (RLCK) family and plays a vital role in immunity. However, the role of RLCKs in the high-temperature seedling-plant (HTSP) resistance of wheat (Triticum aestivum) to Puccinia striiformis f. sp. tritici (Pst), the stripe rust pathogen, remains unclear. Here, we identified a homologous gene of RIPK in wheat, namely TaRIPK. Expression of TaRIPK was induced by Pst inoculation and high temperatures. Silencing of TaRIPK reduced the expression level of TaRPM1, resulting in weaker HTSP resistance. Moreover, TaRIPK interacts with and phosphorylates papain-like cysteine protease 1 (TaPLCP1). Meanwhile, we found that the Pst-secreted protein PSTG_01766 targets TaPLCP1. Transient expression of PSTG_01766 inhibited basal immunity in tobacco (Nicotiana benthamiana) and wheat. The role of PSTG_01766 as an effector involved in HTSP resistance was further supported by host-induced gene silencing and bacterial type three secretion system-mediated delivery into wheat. PSTG_01766 inhibited the TaRIPK-induced phosphorylation of TaPLCP1. Furthermore, PSTG_01766 has the potential to influence the subcellular localization of TaPLCP1. Overall, we suggest that the TaRIPK-TaPLCP1-TaRPM1 module fits the guard model for disease resistance, participating in HTSP resistance. PSTG_01766 decreases HTSP resistance via targeting TaPLCP1. Guarded by wheat and attacked by Pst, TaPLCP1 may serve as a central hub of the defense response. Our findings improve the understanding of the molecular mechanism of wheat HTSP resistance, which may be an important strategy for controlling stripe rust in the face of global warming.

Automated summary

The TaRIPK-TaPLCP1-TaRPM1 module plays a key role in the high-temperature seedling-plant resistance of wheat. The Pst-secreted protein PSTG_01766 targets TaPLCP1, inhibits TaRIPK-induced phosphorylation of TaPLCP1, and decreases high-temperature seedling-plant resistance.