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cGMP regulates hydrogen peroxide accumulation in calcium-dependent salt resistance pathway in Arabidopsis thaliana roots

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Abstract

3′,5′-cyclic guanosine monophosphate (cGMP) is an important second messenger in plants. In the present study, roles of cGMP in salt resistance in Arabidopsis roots were investigated. Arabidopsis roots were sensitive to 100 mM NaCl treatment, displaying a great increase in electrolyte leakage and Na+/K+ ratio and a decrease in gene expression of the plasma membrane (PM) H+-ATPase. However, application of exogenous 8Br-cGMP (an analog of cGMP), H2O2 or CaCl2 alleviated the NaCl-induced injury by maintaining a lower Na+/K+ ratio and increasing the PM H+-ATPase gene expression. In addition, the inhibition of root elongation and seed germination under salt stress was removed by 8Br-cGMP. Further study indicated that 8Br-cGMP-induced higher NADPH levels for PM NADPH oxidase to generate H2O2 by regulating glucose-6-phosphate dehydrogenase (G6PDH) activity. The effect of 8Br-cGMP and H2O2 on ionic homeostasis was abolished when Ca2+ was eliminated by glycol-bis-(2-amino ethyl ether)-N,N,N′,N′-tetraacetic acid (EGTA, a Ca2+ chelator) in Arabidopsis roots under salt stress. Taken together, cGMP could regulate H2O2 accumulation in salt stress, and Ca2+ was necessary in the cGMP-mediated signaling pathway. H2O2, as the downstream component of cGMP signaling pathway, stimulated PM H+-ATPase gene expression. Thus, ion homeostasis was modulated for salt tolerance.

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Abbreviations

8Br-cGMP:

8Bromo-3,5-cyclic guanosine monophosphate

DPI:

Diphenylene iodonium

DTT:

1,4-Dithiothreitol

EDTA:

Ethylenediaminetetraacetic acid

EGTA:

Glycol-bis-(2-amino ethyl ether)-N,N,N′,N′-tetraacetic acid

EL:

Electrolyte leakage

G6PDH:

Glucose-6-phosphate dehydrogenase

H2O2 :

Hydrogen peroxide

Ly83583:

6-Anilino-5,8-quinolinedione

PM:

Plasma membrane

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Acknowledgments

This work was supported by the National High Technology Research and Development Program (2007AA021401), the Major Project of Cultivating New Varieties of Transgenic Organisms (2009ZX08009-029B), the Doctoral Program of Higher Education of China (Ratification No. 20100211110009) and the National Natural Science Foundation of China (No. 90917019). The Arabidopsis seeds used in this study were kindly provided by Dr. Ning Li (Department of Biology, The Hong Kong University of Science and Technology).

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  1. School of Life Sciences, Lanzhou University, Lanzhou, 730000, People’s Republic of China

    Jisheng Li, Xiaomin Wang, Yanli Zhang, Honglei Jia & Yurong Bi

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  1. Jisheng Li
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  2. Xiaomin Wang
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  3. Yanli Zhang
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  4. Honglei Jia
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  5. Yurong Bi
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Correspondence to Yurong Bi.

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J. Li and X. Wang contributed equally to the paper.

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Li, J., Wang, X., Zhang, Y. et al. cGMP regulates hydrogen peroxide accumulation in calcium-dependent salt resistance pathway in Arabidopsis thaliana roots. Planta 234, 709–722 (2011). https://doi.org/10.1007/s00425-011-1439-3

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