Osmosensor-mediated control of Ca2+ spiking in pollen germination

Author:

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 KarenORCID,Johnson Douglas M.,Jiang Zhonghao,Wu Feihua,Swift Gary B.,Yang HuangheORCID,Liu Zhonghua,Zou Xuexiao,Vo-Dinh TuanORCID,Liu FengORCID,Pei Zhen-MingORCID,Yuan FangORCID

Abstract

AbstractHigher 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.

Publisher

Springer Science and Business Media LLC

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