Osmosensor-mediated control of Ca2+ spiking in pollen germination

Songyu Pei, Qi Tao, Wenke Li, Guoning Qi, Borong Wang, Yan Wang, Shiwen Dai, Qiujing Shen, Xi Wang, Xiaomei Wu, Shijian Xu, Lynn Theprungsirikul, Jingyuan Zhang, Liang Liang, Yuantao Liu, Kena Chen, Yang Shen, Bridget M. Crawford, Mengjia Cheng, Qi Zhang, Yiqi Wang, Hongli Liu, Benguang Yang, Bryan Krichilsky, Jessica Pei, Karen Song, Douglas M. Johnson, Zhonghao Jiang, Feihua Wu, Gary B. Swift, Huanghe Yang, Zhonghua Liu, Xuexiao Zou, Tuan Vo-Dinh, Feng Liu (), Zhen-Ming Pei () and Fang Yuan ()
Additional contact information
Songyu Pei: Hunan Agricultural University
Qi Tao: Zhejiang University
Wenke Li: Zhejiang University
Guoning Qi: Hangzhou Normal University
Borong Wang: Hangzhou Normal University
Yan Wang: Hunan Agricultural University
Shiwen Dai: Hunan Agricultural University
Qiujing Shen: Hangzhou Normal University
Xi Wang: Zhejiang University
Xiaomei Wu: Hangzhou Normal University
Shijian Xu: Duke University
Lynn Theprungsirikul: Duke University
Jingyuan Zhang: Duke University
Liang Liang: Hangzhou Normal University
Yuantao Liu: Zhejiang University
Kena Chen: Hangzhou Normal University
Yang Shen: Hangzhou Normal University
Bridget M. Crawford: Duke University
Mengjia Cheng: Hangzhou Normal University
Qi Zhang: Zhejiang University
Yiqi Wang: Hangzhou Normal University
Hongli Liu: Hangzhou Normal University
Benguang Yang: Hangzhou Normal University
Bryan Krichilsky: Duke University
Jessica Pei: Duke University
Karen Song: Duke University
Douglas M. Johnson: Duke University
Zhonghao Jiang: Duke University
Feihua Wu: Duke University
Gary B. Swift: Duke University
Huanghe Yang: Duke University
Zhonghua Liu: Hunan Agricultural University
Xuexiao Zou: Hunan Agricultural University
Tuan Vo-Dinh: Duke University
Feng Liu: Hunan Agricultural University
Zhen-Ming Pei: Duke University
Fang Yuan: Hunan Agricultural University

Nature, 2024, vol. 629, issue 8014, 1118-1125

Abstract: Abstract 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 rehydration1,2, the molecular basis remains unknown. Because osmolarity triggers membrane tension and the osmosensing specificity of osmosensing channels can only be determined in vivo3–5, 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 proteins6. 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.

Date: 2024
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DOI: 10.1038/s41586-024-07445-6

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