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Nitric oxide cross-links calcium signals to enhance cold tolerance via inhibiting calmodulin expression in watermelon

文献类型： 外文期刊

作者： Guo, Yanliang 1 ; Li, Jiayue 1 ; Liu, Lingling 1 ; Yang, Wanbang 1 ; Zhou, Yijia 1 ; Wei, Chunhua 1 ; Ma, Jianxiang 1 ; Zhang, Yong 1 ; Yang, Jianqiang 1 ; Liu, Yunqi 4 ; Zhang, Huijun 1 ; Yuan, Li 1 ; Zhang, Xian 1 ; Li, Hao 1 ;

作者机构： 1.Northwest A&F Univ, Coll Hort, Yangling 712100, Shaanxi, Peoples R China

2.Huaibei Normal Univ, Coll Life Sci, Huaibei 235000, Anhui, Peoples R China

3.Ningxia Acad Agr & Forestry Sci, Inst Hort, Yinchuan 750002, Ningxia, Peoples R China

4.Zhongguancun Xuyue Noninvas Microtest Technol Ind, Sci Res Promot Ctr, Beijing 10080, Peoples R China

期刊名称：PLANT PHYSIOLOGY （ 影响因子：6.9； 五年影响因子：7.7 ）

ISSN： 0032-0889

年卷期： 2025 年 198 卷 2 期

页码：

收录情况： SCI

摘要： Nitric oxide (NO) is a pivotal gaseous signaling molecule that plays a critical role in regulating plant tolerance to cold stress; however, the underlying mechanisms of signal transduction remain poorly elucidated. In this study, knockout of nitrate reductase 1 (ClNR1), a crucial gene for NO biosynthesis, led to reduced cold tolerance in watermelon (Citrullus lanatus), accompanied by downregulation of cycle nucleotide-gated channel (ClCNGC) 20, a key Ca2+-permeable channel gene, decreased Ca2+ influx, and upregulation of calmodulin (ClCaM) 2/5/7. Conversely, application of the NO donor sodium nitroprusside (SNP) exhibited contrasting effects compared with NR1 knockout. Silencing ClCNGC20 counteracted SNP-induced Ca2+ influx, downregulation of ClCaM 2/5/7, and cold tolerance. Silencing ClCaM2/5/7 alleviated the inhibition on C-REPEAT-BINDING FACTOR (ClCBF) expression and cold tolerance induced by ClNR1 knockout or ClCNGC20 silencing. Multiple experimental approaches revealed the interactions between ClCaM2/5/7 and voltage-dependent anion channel (ClVDAC) 1 proteins. Overexpression of ClVDAC1 hindered the induction of ClCBF expression and cold tolerance triggered by SNP or CaCl2, whereas ClVDAC1 silencing mitigated the inhibition on ClCBF expression and cold tolerance caused by ClNR1 knockout or ClCNGC20 silencing. Additionally, cold stress rapidly triggered Ca2+ influx, which stimulated NO production. These findings suggest that Ca2+ influx promotes NO generation, which leads to further Ca2+ influx via upregulating ClCNGC20, forming a positive feedback loop that enhances cold tolerance. Furthermore, ClCaM2/5/7 interacts with ClVDAC1 to negatively regulate the NO- and Ca2+ signaling-mediated C-repeat-binding factor pathway and subsequent cold tolerance. Nitric oxide-induced C-repeat-binding factor pathway and cold tolerance in watermelon are mediated by ClCNGC20-dependent calcium influx through the interaction between calmodulins and voltage-dependent anion channel 1.

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