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Nitric oxide and hydrogen peroxide increase glucose-6-phosphate dehydrogenase activities and expression upon drought stress in soybean roots

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Abstract

Key message

Changes in glucose-6-phosphate dehydrogenase (G6PD) isoforms activities and expression were investigated in soybean roots under drought, suggesting that cytosolic G6PD plays a main role by regulating H2O2 signal and redox homeostasis.

Abstract

G6PD acts a vital role in plant growth, development and stress adaptation. Drought (PEG6000 treatment) could markedly increase the enzymatic activities of cytosolic G6PD (Cyt-G6PD) and compartmented G6PD (mainly plastidic P2-G6PD) in soybean roots. Application of G6PD inhibitor upon drought condition dramatically decreased the intracellular NADPH and reduced glutathione levels in soybean roots. Nitric oxide (NO) and hydrogen peroxide (H2O2) participated in the regulation of Cyt-G6PD and P2-G6PD enzymatic activities under drought stress. Diphenylene iodonium (DPI), an inhibitor of NADPH oxidase, abolished the drought-induced accumulation of H2O2. The exogenous application of H2O2 and its production inhibitor (DPI) could stimulate and inhibit the NO accumulation, respectively, but not vice versa. qRT-PCR analysis confirmed that NO, as the downstream signal of H2O2, positively regulated the transcription of genes encoding Cyt-G6PD (GPD5, G6PD6, G6PD7) under drought stress in soybean roots. Comparatively, NO and H2O2 signals negatively regulated the gene expression of compartmented G6PD (GPD1, G6PD2, G6PD4), indicating that a post-transcriptional mechanism was involved in compartmented G6PD regulation. Taken together, the high Cyt-G6PD activity is essential for maintaining redox homeostasis upon drought condition in soybean roots, and the H2O2-dependent NO cascade signal is differently involved in Cyt-G6PD and compartmented G6PD regulation.

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Abbreviations

Asc:

Ascorbate

cPTIO:

2-Phenyl-4,4,5,5-tetremethy-limidazolinone-1-oxyl-3-oxide

DAB:

3,3-Diaminobenzidine

DPI:

Diphenylene iodonium

GlcN:

Glucosamine

G6PD:

Glucose-6-phosphate dehydrogenase

GSH:

Reduced glutathione

GSSG:

Oxidative glutathione

H2O2 :

Hydrogen peroxide

L-NNA:

Nω-nitro-L-Arg

NBT:

Nitroblue tetrazolium

NO:

Nitric oxide

NOS:

NO synthase

NR:

Nitrate reductase

O2 − :

Superoxide anion

ROS:

Reactive oxygen species

SNP:

Sodium nitroprusside

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Acknowledgements

This work was supported by the National Natural Science Foundation of China [31671595; 31670244], The Project of Qinghai Science & Technology Department [2016-ZJ-Y01], The Open Project of State Biotechnology Research and Application Development Program of Gansu Province [GNSW-2016-23].

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Author notes

  1. Xiaomin Wang and Mengjiao Ruan contributed equally to the paper.

Authors and Affiliations

  1. Key Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, School of Life Sciences, Lanzhou University, Lanzhou, 730000, Gansu, China

    Xiaomin Wang, Mengjiao Ruan, Qi Wan, Wenliang He, Lei Yang, Xinyuan Liu, Li He, Lili Yan & Yurong Bi

  2. State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining, 810016, Qinghai, China

    Xiaomin Wang

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  1. Xiaomin Wang
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  2. Mengjiao Ruan
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Contributions

YB and XW designed the research. XW, MR, QW, XL, LH and LY conducted experiments. XW, QW, WH and MR analyzed the data. XW, YB and LY wrote the manuscript.

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Correspondence to Yurong Bi.

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Communicated by Marcelo Menossi.

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Wang, X., Ruan, M., Wan, Q. et al. Nitric oxide and hydrogen peroxide increase glucose-6-phosphate dehydrogenase activities and expression upon drought stress in soybean roots. Plant Cell Rep 39, 63–73 (2020). https://doi.org/10.1007/s00299-019-02473-3

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