Osmosensor-mediated control of Ca2+ spiking in pollen germination

• 成果类型: Article
• 署名作者: Pei, Songyu; Tao, Qi; Li, Wenke; Qi, Guoning; Wang, Borong; Wang, Yan; Dai, Shiwen; Shen, Qiujing; Wang, Xi; Wu, Xiaomei; Xu, Shijian; Theprungsirikul, Lynn; Zhang, Jingyuan; Liang, Liang; Liu, Yuantao; Chen, Kena; Shen, Yang; Crawford, Bridget M.; Cheng, Mengjia; Zhang, Qi; Wang, Yiqi; Liu, Hongli; Yang, Benguang; Krichilsky, Bryan; Pei, Jessica; Song, Karen; Johnson, Douglas M.; Jiang, Zhonghao; Wu, Feihua; Swift, Gary B.; Yang, Huanghe; Liu, Zhonghua; Zou, Xuexiao; Vo-Dinh, Tuan; Liu, Feng; Pei, Zhen-Ming; Yuan, Fang
• 署名单位: Hunan Agricultural University; Duke University; Duke University; Zhejiang University; Hangzhou Normal University; Duke University; Duke University; Duke University
• 刊物名称: Nature
• ISSN/ISSBN: 0028-5473
• DOI: 10.1038/s41586-024-07445-6
• 发表日期: 2024-05-30
• 页码: 1118-+
• 关键词: tube growth; mechanosensitive channels; receptor kinase; trp channels; ion channels; tip growth; cell; responses; signals; identification

摘要

Higher plants survive terrestrial water deficiency and fluctuation by arresting cellular activities (dehydration) and resuscitating processes (rehydration). However, how plants monitor water availability during rehydration is unknown. Although increases in hypo-osmolarity-induced cytosolic Ca2+ concentration (HOSCA) have long been postulated to be the mechanism for sensing hypo-osmolarity in rehydration(1,2), the molecular basis remains unknown. Because osmolarity triggers membrane tension and the osmosensing specificity of osmosensing channels can only be determined in vivo(3-5), these channels have been classified as a subtype of mechanosensors. Here we identify bona fide cell surface hypo-osmosensors in Arabidopsis and find that pollen Ca2+ spiking is controlled directly by water through these hypo-osmosensors-that is, Ca2+ spiking is the second messenger for water status. We developed a functional expression screen in Escherichia coli for hypo-osmosensitive channels and identified OSCA2.1, a member of the hyperosmolarity-gated calcium-permeable channel (OSCA) family of proteins(6). We screened single and high-order OSCA mutants, and observed that the osca2.1/osca2.2 double-knockout mutant was impaired in pollen germination and HOSCA. OSCA2.1 and OSCA2.2 function as hypo-osmosensitive Ca2+-permeable channels in planta and in HEK293 cells. Decreasing osmolarity of the medium enhanced pollen Ca2+ oscillations, which were mediated by OSCA2.1 and OSCA2.2 and required for germination. OSCA2.1 and OSCA2.2 convert extracellular water status into Ca2+ spiking in pollen and may serve as essential hypo-osmosensors for tracking rehydration in plants.