Cyclic nucleotide-gated ion channel 20 regulates melatonin-induced calcium signaling and cold tolerance in watermelon

文献类型: 外文期刊

第一作者: Chang, Jingjing

作者: Chang, Jingjing;Guo, Yanliang;Li, Jiayue;Liu, Lingling;Liu, Jiahe;Yuan, Li;Wei, Chunhua;Ma, Jianxiang;Zhang, Yong;Zhang, Xian;Li, Hao;Chang, Jingjing;Ahammed, Golam Jalal;Luan, Feishi;Liu, Yunqi

作者机构:

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: 2024 年 197 卷 2 期

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收录情况: SCI

摘要: Melatonin plays a crucial role in regulating plant cold tolerance, but the mechanisms underlying signal transduction remain elusive. In this study, we discovered that overexpression of the melatonin biosynthetic gene caffeic acid O-methyltransferase1 (COMT1) enhanced watermelon (Citrullus lanatus) cold tolerance, accompanied by the accumulation of cytosolic free calcium ([Ca2+]cyt), a stimulation of Ca2+ influx, and upregulation of 4 Ca2+-permeable channel genes (CNGC2/10/17/20). Conversely, the knockout of COMT1 exhibited contrasting effects compared with its overexpression. Knocking out the 4 CNGC genes revealed that only cyclic nucleotide-gated ion channel 20 (CNGC20) mediates melatonin-induced Ca2+ influx in response to cold stimuli. CNGC20 deletion impeded watermelon callus redifferentiation, prompting us to employ a virus-induced gene silencing strategy to suppress its expression. Silencing CNGC20 compromised COMT1 overexpression-induced [Ca2+]cyt accumulation, Ca2+ influx, and watermelon cold tolerance. Yeast 2-hybrid, bimolecular fluorescence complementation, firefly luciferase complementation imaging, and pull-down assays revealed an interaction between CNGC20 and calmodulin7 (CaM7). Overexpressing CaM7 inhibited melatonin-induced [Ca2+]cyt accumulation, Ca2+ influx, and watermelon cold tolerance. Conversely, silencing CaM7 increased [Ca2+]cyt accumulation, Ca2+ influx, and cold tolerance, whereas COMT1 overexpression failed to further enhance these responses in CaM7-silenced plants, indicating the negative regulation role of CaM7 in melatonin-mediated cold responses. Overall, these findings provide insights into the molecular mechanisms underlying melatonin-enhanced plant cold tolerance via Ca2+ signaling, holding potential for breeding/engineering cold-tolerant cucurbit varieties. The interaction between cyclic nucleotide-gated ion channel 20 and calmodulin7 mediates Ca2+ signaling in Citrullus lanatus, playing a pivotal role in melatonin-induced plant tolerance to cold stress.

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