Salt stress-induced H 2 O 2 and Ca 2+ mediate K + /Na + homeostasis in Pyropia haitanensis
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Salt stress-induced H2O2 and Ca2+ mediate K+/Na+ homeostasis in Pyropia haitanensis Wenlei Wang 1,2,3 & Lei Xing 1,2,3 & Kai Xu 1,2,3 & Dehua Ji 1,2,3 & Yan Xu 1,2,3 & Changsheng Chen 1,2,3 & Chaotian Xie 1,2,3 Received: 3 September 2020 / Revised and accepted: 25 September 2020 # Springer Nature B.V. 2020
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. Keywords H2O2 signaling . Ca2+ signaling . K+/Na+ homeostasis . hypersaline stress . Pyropia haitanensis
Introduction Salinity stress is one of the environmental constraints limiting crop quality and yield worldwide (Flowers 2004; Zhu 2016). Characterizing the mechanism mediating the salt tolerance of plants is crucial for breeding novel varieties with enhanced salinity tolerance. A recent study revealed that, because they alternate between being immersed in seawater and exposed to air, intertidal macroalgae are more able to resist hypersaline stress than land halophytes, seagrass, and microalgae (Wang et al. 2019). For example, Pyropia haitanensis, one of the most economically and ecologically important mariculture Wenlei Wang and Lei Xing contributed equally to this work. * Chaotian Xie [email protected] 1
Fisheries College, Jimei University, Xiamen 361021, China
2
Fujian Engineering Research Center of Aquatic Breeding and Healthy Aquaculture, Xiamen 361021, China
3
Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture, Xiamen 361021, China
seaweeds, can resume normal growth after a 4-h exposure to 110‰ salt stress (Ch
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