Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai 200234, China.
College of Agriculture, Yangtze University, Jingzhou 434025, China.
Plant Cell. 2022 Aug 25;34(9):3443-3459. doi: 10.1093/plcell/koac176.
Phytophthora effector PSR1 suppresses small RNA (sRNA)-mediated immunity in plants, but the underlying mechanism remains unknown. Here, we show that Phytophthora suppressor of RNA silencing 1 (PSR1) contributes to the pathogenicity of Phytophthora sojae and specifically binds to three conserved C-terminal domains of the eukaryotic PSR1-Interacting Protein 1 (PINP1). PINP1 encodes PRP16, a core pre-mRNA splicing factor that unwinds RNA duplexes and binds to primary microRNA transcripts and general RNAs. Intriguingly, PSR1 decreased both RNA helicase and RNA-binding activity of PINP1, thereby dampening sRNA biogenesis and RNA metabolism. The PSR1-PINP1 interaction caused global changes in alternative splicing (AS). A total of 5,135 genes simultaneously exhibited mis-splicing in both PSR1-overexpressing and PINP1-silenced plants. AS upregulated many mRNA transcripts that had their introns retained. The high occurrence of intron retention in AS-induced transcripts significantly promoted Phytophthora pathogen infection in Nicotiana benthamiana, and this might be caused by the production of truncated proteins. Taken together, our findings reveal a key role for PINP1 in regulating sRNA biogenesis and plant immunity.
疫霉效应物 PSR1 抑制植物中的小 RNA(sRNA)介导的免疫,但潜在机制尚不清楚。在这里,我们表明疫霉 RNA 沉默抑制物 1(PSR1)有助于大豆疫霉的致病性,并且特异性结合真核 PSR1 相互作用蛋白 1(PINP1)的三个保守 C 端结构域。PINP1 编码 PRP16,它是一种核心前体 mRNA 剪接因子,可解链 RNA 双链,并与初级 microRNA 转录本和一般 RNA 结合。有趣的是,PSR1 降低了 PINP1 的 RNA 解旋酶和 RNA 结合活性,从而抑制了 sRNA 的生物发生和 RNA 代谢。PSR1-PINP1 相互作用导致可变剪接(AS)的全局变化。共有 5135 个基因在 PSR1 过表达和 PINP1 沉默植物中同时表现出错误剪接。AS 上调了许多保留内含子的 mRNA 转录本。AS 诱导的转录物中内含子保留的高发生率显著促进了烟草中的疫霉病原体感染,这可能是由于产生了截断蛋白。总之,我们的研究结果揭示了 PINP1 在调节 sRNA 生物发生和植物免疫中的关键作用。