Department of Life Sciences, Korea University, Seoul, 02841, Korea.
Research, Institute of Basic Sciences, Seoul National University, Seoul, 08826, Korea.
J Integr Plant Biol. 2024 Oct;66(10):2273-2287. doi: 10.1111/jipb.13747. Epub 2024 Jul 23.
Systemin, the first peptide hormone identified in plants, was initially isolated from tomato (Solanum lycopersicum) leaves. Systemin mediates local and systemic wound-induced defense responses in plants, conferring resistance to necrotrophic fungi and herbivorous insects. Systemin is recognized by the leucine-rich-repeat receptor-like kinase (LRR-RLK) receptor SYSTEMIN RECEPTOR1 (SYR1), but how the systemin recognition signal is transduced to intracellular signaling pathways to trigger defense responses is poorly understood. Here, we demonstrate that SERK family LRR-RLKs function as co-receptors for SYR1 to mediate systemin signal transduction in tomato. By using chemical genetic approaches coupled with engineered receptors, we revealed that the association of the cytoplasmic kinase domains of SYR1 with SERKs leads to their mutual trans-phosphorylation and the activation of SYR1, which in turn induces a wide range of defense responses. Systemin stimulates the association between SYR1 and all tomato SERKs (SlSERK1, SlSERK3A, and SlSERK3B). The resulting SYR1-SlSERK heteromeric complexes trigger the phosphorylation of TOMATO PROTEIN KINASE 1B (TPK1b), a receptor-like cytoplasmic kinase that positively regulates systemin responses. Additionally, upon association with SYR1, SlSERKs are cleaved by the Pseudomonas syringae effector HopB1, further supporting the finding that SlSERKs are activated by systemin-bound SYR1. Finally, genetic analysis using Slserk mutants showed that SlSERKs are essential for systemin-mediated defense responses. Collectively, these findings demonstrate that the systemin-mediated association of SYR1 and SlSERKs activates defense responses against herbivorous insects.
植物中第一个被鉴定的肽激素系统素最初是从番茄（Solanum lycopersicum）叶片中分离得到的。系统素介导植物的局部和系统诱导的伤口防御反应，赋予植物对坏死真菌和草食性昆虫的抗性。系统素被富含亮氨酸重复的受体样激酶（LRR-RLK）受体 SYSTEMIN RECEPTOR1（SYR1）识别，但系统素识别信号如何被转导到细胞内信号通路以触发防御反应还知之甚少。在这里，我们证明 SERK 家族 LRR-RLKs 作为 SYR1 的共受体，在番茄中介导系统素信号转导。通过使用化学遗传学方法和工程化受体，我们揭示了 SYR1 的细胞质激酶结构域与 SERKs 的结合导致它们相互转磷酸化和 SYR1 的激活，这反过来又诱导了广泛的防御反应。系统素刺激 SYR1 与所有番茄 SERKs（SlSERK1、SlSERK3A 和 SlSERK3B）之间的结合。由此产生的 SYR1-SlSERK 异源二聚体复合物触发番茄蛋白激酶 1B（TPK1b）的磷酸化，TPK1b 是一种正调控系统素反应的受体样细胞质激酶。此外，SlSERKs 在与 SYR1 结合后被丁香假单胞菌效应物 HopB1 切割，进一步支持 SlSERKs 被结合 SYR1 的系统素激活的发现。最后，使用 Slserk 突变体进行的遗传分析表明，SlSERKs 是系统素介导的防御反应所必需的。总之，这些发现表明，SYR1 和 SlSERKs 介导的系统素结合激活了对草食性昆虫的防御反应。
