A virulence protein activates SERK4 and degrades RNA polymerase IV protein to suppress rice anti-viral immunity

Rice, a major global food staple, is threatened by viral infection that hinder its growth and yield. We have recently shown that the virulence protein P3 of rice grassy stunt virus promotes pathogenesis by inducing proteasome-controlled degradation of the rice RNA polymerase IV protein NRPD1a controlled by the P3-interacting E3 ubiquitin ligase P3IP1. However, the underlying mechanisms remain elusive. In this study, we show that P3 acts as a virus-encoded transcription activator-like effector to upregulate transcription of Somatic Embryogenesis Receptor Kinase 4 (SERK4) by directly binding to its promoter. SERK4 phosphorylates P3IP1 and enhances Pol IVa (NRPD1a) degradation following P3IP1-controlled ubiquitination, leading to attenuated antiviral defense in rice. Thus, our study finds a critical viral virulence strategy by encoding a transcription factor-like protein that activates a host kinase to promote proteasome- controlled degradation of NRPD1a, thereby disarming RNA-directed DNA methylation (RdDM) antiviral defense.

水稻作为全球主要粮食作物，其生长与产量正受到病毒感染的严重威胁。本团队前期研究表明，水稻草矮病毒（Rice Grassy Stunt Virus）的致病蛋白P3可通过诱导水稻RNA聚合酶IV（RNA polymerase IV）蛋白NRPD1a的蛋白酶体调控降解来促进病害发生，该过程依赖于与P3互作的E3泛素连接酶P3IP1。然而，其背后的具体分子机制仍有待阐明。本研究发现，P3可作为病毒编码的转录激活因子样效应蛋白，通过直接结合体细胞胚胎发生受体激酶4（Somatic Embryogenesis Receptor Kinase 4，SERK4）的启动子上调其转录水平。SERK4可对P3IP1进行磷酸化修饰，并在P3IP1介导的泛素化过程中增强Pol IVa（NRPD1a）的降解，最终削弱水稻的抗病毒防御。综上，本研究揭示了一种关键的病毒致病策略：病毒通过编码类转录因子蛋白，激活宿主激酶以促进NRPD1a的蛋白酶体调控降解，从而解除RNA指导的DNA甲基化（RNA-directed DNA methylation，RdDM）介导的抗病毒防御。