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Salt stress-induced H2O2 and Ca2+ mediate K+/Na+ homeostasis in Pyropia haitanensis

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Abstract

Maintaining K+/Na+ homeostasis and redox homeostasis is crucial for the tolerance of P. haitanensis to hypersalinity. However, the precise link between the signaling role of reactive oxygen species (ROS) and K+/Na+ homeostasis remains poorly characterized. In this study, we analyze hydrogen peroxide (H2O2) production and flux as well as H2O2 effects on K+, Na+, and Ca2+ transport in P. haitanensis under hypersaline condition. An exposure to hypersaline stress (110‰, 15 min) rapidly increased the H2O2 content and efflux in P. haitanensis cells, which was counteracted by the rapid increase in superoxide dismutase activity and activation of defense responses. The enhanced Na+ efflux and Ca2+ influx induced by salt stress were substantially suppressed by an NADPH oxidase inhibitor (DPI) or an ROS scavenger (DMTU). Additionally, Na+ efflux decreased in response to a plasma membrane Ca2+-permeable channel inhibitor (verapamil). This suggested that NADPH oxidase-mediated H2O2 production may promote Na+ efflux via the Ca2+-dependent Na+/H+ antiporter system in salt-stressed P. haitanensis thalli. Moreover, salt-induced H2O2 accumulation also enhanced K+ efflux, which was alleviated by exogenous Ca2+. H2O2 and Ca2+ may independently mediate K+ homeostasis in P. haitanensis. H2O2-induced K+ leakage may induce cells to switch from normal metabolic activities to those associated with adaptation and repair. The present results provide new insight for clarifying the relationship between salt-induced ROS signaling and ion homeostasis in intertidal seaweed species.

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Acknowledgments

This work was supported by National Natural Science Foundation of China (Grant No: 31872567 and 41806185), National Key R&D Program of China (Grant No: 2018YFD0900106 and 2018YFD0901500), Fujian Province Science and Technology Major Project (2019NZ08003), and “China Agriculture Research System (Grant No: CARS-50)”. We thank Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

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WW and LX conducted the data analysis and wrote the first draft of the manuscript. KX, DJ, and YX participated in the sample processing and data collection. CX and CC contributed to design and interpretation of results. All authors contributed to writing, revising, and approving the submitted version of the manuscript.

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Correspondence to Chaotian Xie.

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Wang, W., Xing, L., Xu, K. et al. Salt stress-induced H2O2 and Ca2+ mediate K+/Na+ homeostasis in Pyropia haitanensis. J Appl Phycol 32, 4199–4210 (2020). https://doi.org/10.1007/s10811-020-02284-0

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