Li Chong, Gong Ben-Qiang, Luo Shuyi, Wang Tong, Long Ruhui, Jiang Xianya, Deng Yi Zhen, Li Jian-Feng
Guangdong Provincial Key Laboratory of Plant Stress Biology, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China.
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, Guangxi University, Nanning 530004, China.
Plant Physiol. 2024 Dec 2;196(4):2956-2972. doi: 10.1093/plphys/kiae499.
Plants must tactically balance immunity and growth when combating lethal pathogens like fungi. CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1), a conserved cell-surface co-receptor for the fungal elicitor chitin, enables plants to induce chitin-triggered immunity to counteract fungal invasion. Previously, we reported that bacterial infection can prime CERK1 through juxtamembrane (JM) phosphorylation to enhance fungal resistance, which only occurs in Arabidopsis (Arabidopsis thaliana) and its close relatives in Brassicaceae. Here, we aim to transfer the priming mechanism of Arabidopsis CERK1 (AtCERK1) to crop CERK1 via JM substitution. We revealed in protoplasts that the entire AtCERK1 JM variable region (AtJM) is essential for imparting the bacterial elicitor flg22-induced primed state to the Nicotiana benthamiana CERK1 (NbCERK1). The NbCERK1 chimera containing AtJM (NbCERK1AtJM) and similarly constructed rice (Oryza sativa) OsCERK1AtJM could undergo flg22-induced JM phosphorylation and confer enhanced antifungal immunity upon bacterial coinfection. Moreover, the NbCERK1AtJM+3D derivative with AtJM phosphomimetic mutations to mimic a constant primed state and similarly constructed OsCERK1AtJM+3D were sufficient to mediate strengthened chitin responses and fungal resistance in transgenic plants independent of bacterial infection. Importantly, no growth and reproduction defects were observed in these plants. Taken together, this study demonstrates that manipulating the primed state of a cell-surface immune receptor offers an effective approach to improve disease resistance in crops without compromising growth and yield and showcases how fundamental insights in plant biology can be translated into crop breeding applications.
在对抗诸如真菌等致命病原体时，植物必须在免疫和生长之间进行策略性平衡。几丁质激发子受体激酶1（CERK1）是真菌激发子几丁质的一种保守的细胞表面共受体，它使植物能够诱导几丁质触发的免疫反应以对抗真菌入侵。此前，我们报道细菌感染可通过近膜（JM）磷酸化使CERK1致敏，从而增强真菌抗性，这种现象仅在拟南芥及其十字花科的近缘种中出现。在此，我们旨在通过JM替换将拟南芥CERK1（AtCERK1）的致敏机制转移至作物的CERK1。我们在原生质体中发现，整个AtCERK1 JM可变区（AtJM）对于赋予烟草CERK1（NbCERK1）细菌激发子flg22诱导的致敏状态至关重要。含有AtJM的NbCERK1嵌合体（NbCERK1AtJM）以及类似构建的水稻（Oryza sativa）OsCERK1AtJM在细菌共感染时可发生flg22诱导的JM磷酸化，并赋予增强的抗真菌免疫力。此外，具有AtJM磷酸模拟突变以模拟恒定致敏状态的NbCERK1AtJM+3D衍生物以及类似构建的OsCERK1AtJM+3D足以在不依赖细菌感染的转基因植物中介导增强的几丁质反应和真菌抗性。重要的是，在这些植物中未观察到生长和繁殖缺陷。综上所述，本研究表明操纵细胞表面免疫受体的致敏状态提供了一种有效的方法来提高作物的抗病性，而不会损害生长和产量，并展示了植物生物学的基本见解如何转化为作物育种应用。
