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Nitric oxide-mediated cytosolic glucose-6-phosphate dehydrogenase is involved in aluminum toxicity of soybean under high aluminum concentration

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Abstract

Aims

Glucose-6-phosphate dehydrogenase (G6PDH) has been reported to be involved in resistance to various environmental stresses. However, the role of G6PDH in aluminum (Al) toxicity remains unclear.

Methods

Physiological and biochemical methods together with histochemical analysis were used to investigate the participation of G6PDH in Al-induced inhibition of root growth.

Results

Exposure to high Al concentration caused a significant increase in the activities of total and cytosolic G6PDH in roots of soybean. Al-induced inhibition of root growth and oxidative stress were alleviated by a G6PDH inhibitor. Reactive oxygen species (ROS) accumulation in Al-treated root apexes could be abolished by a NADPH oxidase inhibitor. Furthermore, treatment with a G6PDH inhibitor reduced NADPH content and NADPH oxidase activity in Al-treated root apexes. Further investigation demonstrates that nitric oxide (NO) mediates Al-induced increase in cytosolic G6PDH activity by modulating the expression of genes encoding cytosolic G6PDH. In addition, nitrate reductase pathway is mainly responsible for Al-induced NO production in root apexes.

Conclusions

These results indicate that NADPH produced by NO-modulated cytosolic G6PDH in root apexes is responsible for ROS accumulation mediated by NADPH oxidase under Al stress, subsequently suffering from oxidative stress and thus causing the inhibition of root elongation.

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Abbreviations

DAB:

Diaminobenzidine

DPI:

Diphenylene iodonium

G6PDH:

Glucose-6-phosphate dehydrogenase

GN6P:

Glucosamine 6-phosphate

L-NNA:

N ω-nitro-L-Arg

MDA:

Malondialdehyde

NBT:

Nitroblue tetrazolium

NOS:

Nitric oxide synthase

NR:

Nitrate reductase

PTIO:

2-phenyl-4,4,5,5-tetramethyl-imidazoline-1-oxyl-3-oxide

ROS:

Reactive oxygen species

SNP:

Sodium nitroprusside

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 31301252), Science Foundation of the Henan Normal University for Outstanding Young Scholars (No. 14YQ003), and Program for Innovative Research Team (in Science and Technology) in University of Henan Province (No. 15IRSTHN020).

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Authors and Affiliations

  1. College of Life Sciences, Henan Normal University, Xinxiang, Henan, 453007, China

    Huahua Wang, Junjie Hou, Yan Li, Yangyang Zhang, Junjun Huang & Weihong Liang

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  1. Huahua Wang
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  2. Junjie Hou
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  3. Yan Li
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  4. Yangyang Zhang
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  5. Junjun Huang
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  6. Weihong Liang
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Corresponding author

Correspondence to Huahua Wang.

Additional information

Responsible Editor: Jian Feng Ma.

Electronic supplementary material

Fig. S1

Root elongation in response to GN6P and AlCl3 separately. Seedlings were pretreated with GN6P for 12 h and then exposed to AlCl3 for 24 h. Data represent means ± SD of at least three biological replicates. Bars with different letters indicate significant differences at P < 0.05. CK, control. (JPEG 53 kb)

High Resolution Image (TIFF 2305 kb)

Fig. S2

Effect of NADPH oxidase inhibitor on the lipid peroxidation under Al stress. Treatments for seedlings were performed as described in Fig. 5. Data represent means ± SD of at least three biological replicates. Bars with different letters indicate significant differences at P < 0.05. CK, control. (JPEG 49 kb)

High Resolution Image (TIFF 2126 kb)

Fig. S3

Effect of different Al concentrations on NO production in soybean roots. Seedlings were exposed to the indicated Al concentrations for 24 h. Representative images showing endogenous NO production are given. CK, control. (JPEG 34 kb)

High Resolution Image (TIFF 2499 kb)

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Wang, H., Hou, J., Li, Y. et al. Nitric oxide-mediated cytosolic glucose-6-phosphate dehydrogenase is involved in aluminum toxicity of soybean under high aluminum concentration. Plant Soil 416, 39–52 (2017). https://doi.org/10.1007/s11104-017-3197-x

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  • DOI: https://doi.org/10.1007/s11104-017-3197-x

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