Na + /K + -ATPase regulates the K + /Na + homeostasis in the intertidal macroalgae, Neoporphyra haitanensis, in response to salt stress

In plants under hypersaline stress, the main transporter that extrudes sodium ions (Na + ) is the Na + /H + antiporter SOS1. Different from land plants, the intertidal macroalgae, Neopyropia/Neoporphyra contains an animal-type Na + /K + -ATPase as well as the SOS1 system. However, the contribution of Na + /K + -ATPase to the K + /Na + homeostasis of intertidal macroalgae remains unclear. In this study, we analyzed the function of Na + /K + -ATPase in the response of Neoporphyra haitanensis to salt stress from the perspective of ion transport dynamics. Both the transcript level of NhNKA2 and enzyme activity of Na + /K + -ATPase increased in the early response of N. haitanensis thalli to hypersaline stress. Addition of ouabain, an inhibitor of Na + /K + -ATPase, resulted in Na + accumulation in the cells, severe K + leakage from the thalli, and then remarkably disturbed the K + /Na + homeostasis in N. haitanensis thalli. This disruption might induce a significant decrease in photosynthesis and a severe oxidative damage in thalli. Accordingly, these results suggested that the important role of Na + /K + -ATPase in the resistance of intertidal macroalgae to hypersaline stress, and shed light on the diversity of K + /Na + homeostasis maintenance mechanisms in plants.

[1]  Shao-hong You,et al.  Application of Non-invasive Micro-test Technology (NMT) in environmental fields: A comprehensive review. , 2022, Ecotoxicology and environmental safety.

[2]  Zhenhua Ma,et al.  A Comparative Study on Low and High Salinity Tolerance of Two Strains of Pinctada fucata , 2021, Frontiers in Marine Science.

[3]  Changle Ma,et al.  Regulation of Plant Responses to Salt Stress , 2021, International journal of molecular sciences.

[4]  S. Isayenkov,et al.  Evolution of Plant Na+-P-Type ATPases: From Saline Environments to Land Colonization , 2021, Plants.

[5]  S. Hussain,et al.  Recent progress in understanding salinity tolerance in plants: Story of Na+/K+ balance and beyond. , 2021, Plant physiology and biochemistry : PPB.

[6]  C. Toyoshima,et al.  Binding of cardiotonic steroids to Na+,K+-ATPase in the E2P state , 2020, Proceedings of the National Academy of Sciences.

[7]  Heng Zhang,et al.  Thriving under Stress: How Plants Balance Growth and the Stress Response. , 2020, Developmental cell.

[8]  Kai Xu,et al.  Salt stress-induced H2O2 and Ca2+ mediate K+/Na+ homeostasis in Pyropia haitanensis , 2020, Journal of Applied Phycology.

[9]  J. Kumari,et al.  Na+/K+-ATPase a Primary Membrane Transporter: An Overview and Recent Advances with Special Reference to Algae , 2020, The Journal of Membrane Biology.

[10]  Juan Zhu,et al.  Root vacuolar Na+ sequestration but not exclusion from uptake correlates with barley salt tolerance. , 2019, The Plant journal : for cell and molecular biology.

[11]  Kai Xu,et al.  K+ and Na+ transport contribute to K+/Na+ homeostasis in Pyropia haitanensis under hypersaline stress , 2019, Algal Research.

[12]  Kai Xu,et al.  Regulatory mechanisms underlying the maintenance of homeostasis in Pyropia haitanensis under hypersaline stress conditions. , 2019, The Science of the total environment.

[13]  Chunpeng Song,et al.  Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance , 2019, Nature Communications.

[14]  F. Maathuis,et al.  Plant Salinity Stress: Many Unanswered Questions Remain , 2019, Front. Plant Sci..

[15]  Yan Guo,et al.  Unraveling salt stress signaling in plants. , 2018, Journal of integrative plant biology.

[16]  S. C. Bhatla,et al.  Mechanisms of Sodium Transport in Plants—Progresses and Challenges , 2018, International journal of molecular sciences.

[17]  Juying Yan,et al.  Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta) , 2017, Proceedings of the National Academy of Sciences.

[18]  Jian‐Kang Zhu Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[19]  Baoshan Wang,et al.  Progress in Studying Salt Secretion from the Salt Glands in Recretohalophytes: How Do Plants Secrete Salt? , 2016, Front. Plant Sci..

[20]  Yan Xu,et al.  Validation of housekeeping genes as internal controls for studying the gene expression in Pyropia haitanensis (Bangiales, Rhodophyta) by quantitative real-time PCR , 2014, Acta Oceanologica Sinica.

[21]  J. Schroeder,et al.  Plant salt-tolerance mechanisms. , 2014, Trends in plant science.

[22]  K. Mikami,et al.  Functional expression of an animal type-Na⁺-ATPase gene from a marine red seaweed Porphyra yezoensis increases salinity tolerance in rice plants , 2013 .

[23]  K. Mikami,et al.  Molecular characterization and expression analysis of sodium pump genes in the marine red alga Porphyra yezoensis , 2012, Molecular Biology Reports.

[24]  Christian N. S. Pedersen,et al.  Evolution of Plant P-Type ATPases , 2012, Front. Plant Sci..

[25]  M. Sussman,et al.  The Effect of a Genetically Reduced Plasma Membrane Protonmotive Force on Vegetative Growth of Arabidopsis1[C][W][OA] , 2012, Plant Physiology.

[26]  F. Bezanilla,et al.  The dynamic relationships between the three events that release individual Na+ ions from the Na+/K+-ATPase , 2012, Nature Communications.

[27]  Kristina L. Ford,et al.  Rice plants expressing the moss sodium pumping ATPase PpENA1 maintain greater biomass production under salt stress. , 2011, Plant biotechnology journal.

[28]  Jian-xin Liu,et al.  Effect of La(NO 3 ) 3 on seedling growth and physiological characteristics of ryegrass under NaCl stress: Effect of La(NO 3 ) 3 on seedling growth and physiological characteristics of ryegrass under NaCl stress , 2011 .

[29]  B. Benito,et al.  Sodium, Potassium-ATPases in Algae and Oomycetes , 2005, Journal of bioenergetics and biomembranes.

[30]  Jia Chen,et al.  Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance , 2004 .

[31]  H. Nakayama,et al.  Yeast plasma membrane Ena1p ATPase alters alkali‐cation homeostasis and confers increased salt tolerance in tobacco cultured cells , 2004, Biotechnology and bioengineering.

[32]  Q. Qiu,et al.  Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Georgios Scheiner-Bobis,et al.  The sodium pump , 2002 .

[34]  A. Rodríguez-Navarro,et al.  Plant cells express several stress calcium ATPases but apparently no sodium ATPase , 2001, Plant and Soil.

[35]  J. Brodie,et al.  Porphyra: a marine crop shaped by stress. , 2011, Trends in plant science.

[36]  Ulrich Schreiber,et al.  Pulse-Amplitude-Modulation (PAM) Fluorometry and Saturation Pulse Method: An Overview , 2004 .