Ren Chun-Xiu, Chen Song-Yu, He Yu-Han, Xu You-Ping, Yang Juan, Cai Xin-Zhong
Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou 310058, China.
Centre of Analysis and Measurement, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou 310058, China.
Plant Commun. 2024 Dec 9;5(12):101072. doi: 10.1016/j.xplc.2024.101072. Epub 2024 Aug 27.
Plants perceive pathogen-associated molecular patterns (PAMPs) using plasma-membrane-localized pattern recognition receptors (PRRs) to activate broad-spectrum pattern-triggered immunity. However, the regulatory mechanisms that ensure robust broad-spectrum plant immunity remain largely unknown. Here, we reveal that the transcription factor WRKY8 has a dual role in the transcriptional regulation of PRR genes: repressing expression of the nlp20/nlp24 receptor gene RLP23 while promoting that of the chitin receptor gene CERK1. SsNLP1 and SsNLP2, two nlp24-type PAMPs from the destructive fungal pathogen Sclerotinia sclerotiorum, activate two calcium-elicited kinases, CPK4 and CPK11, which phosphorylate WRKY8 and thus release its inhibition on RLP23 to promote accumulation of RLP23 transcripts. Meanwhile, SsNLPs activate the RLCK-type kinase PBL19, which phosphorylates WRKY8 and thus enhances accumulation of CERK1 transcripts. Intriguingly, RLP23 is repressed at later stage by PBL19-mediated phosphorylation of WRKY8, thus avoiding excessive immunity and enabling normal growth. Our findings unveil a plant strategy of "killing two birds with one stone" to elicit robust broad-spectrum immunity. This strategy is based on PAMP-triggered fine-tuning of a dual-role transcription factor to simultaneously amplify two PRRs that recognize PAMPs conserved across a wide range of pathogens. Moreover, our results reveal a novel plant strategy for balancing the trade-off between growth and immunity by fine-tuning the expression of multiple PRR genes.
植物利用位于质膜上的模式识别受体(PRRs)感知病原体相关分子模式(PAMPs),以激活广谱的模式触发免疫。然而,确保强大的广谱植物免疫的调控机制在很大程度上仍然未知。在这里,我们揭示转录因子WRKY8在PRR基因的转录调控中具有双重作用:抑制nlp20/nlp24受体基因RLP23的表达,同时促进几丁质受体基因CERK1的表达。来自毁灭性真菌病原体核盘菌的两种nlp24型PAMPs,即SsNLP1和SsNLP2,激活两种钙诱导激酶CPK4和CPK11,它们使WRKY8磷酸化,从而解除其对RLP23的抑制,促进RLP23转录本的积累。同时,SsNLPs激活RLCK型激酶PBL19,其使WRKY8磷酸化,从而增强CERK1转录本的积累。有趣的是,在后期,PBL19介导的WRKY8磷酸化会抑制RLP23,从而避免过度免疫并实现正常生长。我们的研究结果揭示了一种植物 “一石二鸟” 的策略来引发强大的广谱免疫。该策略基于PAMP触发的对具有双重作用的转录因子的微调,以同时放大两个识别广泛病原体中保守PAMPs的PRRs。此外,我们的结果揭示了一种通过微调多个PRR基因的表达来平衡生长与免疫之间权衡的新型植物策略。