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Plant Cell Reports

, Volume 39, Issue 1, pp 63–73 | Cite as

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

  • Xiaomin Wang
  • Mengjiao Ruan
  • Qi Wan
  • Wenliang He
  • Lei Yang
  • Xinyuan Liu
  • Li He
  • Lili Yan
  • Yurong BiEmail author
Original Article

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.

Keywords

Drought Glucose-6-phosphate dehydrogenase Hydrogen peroxide Nitric oxide Redox homeostasis Soybean 

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

Notes

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].

Author contribution statement

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.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

Supplementary material

299_2019_2473_MOESM1_ESM.doc (5.6 mb)
Supplementary material 1 (DOC 5707 kb)

References

  1. Auh CK, Murphy TM (1995) Plasma membrane redox enzyme is involved in the synthesis of O2 and H2O2 by phytophthora elicitor-stimulated rose cells. Plant Physiol 107:1241–1247CrossRefGoogle Scholar
  2. Cardi M, Chibani K, Cafasso D, Rouhier N, Jacquot JP, Esposito S (2011) Abscisic acid effects on activity and expression of barley (Hordeum vulgare) plastidial glucose-6-phosphate dehydrogenase. J Exp Bot 62:4013–4023CrossRefGoogle Scholar
  3. Cardi M, Zaffagnini M, De Lillo A, Castiglia D, Chibani K, Gualberto JM, Rouhier N, Jacquot JP, Esposito S (2016) Plastidic P2 glucose-6P dehydrogenase from poplar is modulated by thioredoxin m-type: distinct roles of cysteine residues in redox regulation and NADPH inhibition. Plant Sci 252:257–266CrossRefGoogle Scholar
  4. Dal Santo S, Stampfl H, Krasensky J, Kempa S, Gibon Y, Petutschnig E, Rozhon W, Heuck A, Clausen T, Jonak C (2012) Stress-induced GSK3 regulates the redox stress response by phosphorylating glucose-6-phosphate dehydrogenase in Arabidopsis. Plant Cell 24:3380–3392CrossRefGoogle Scholar
  5. De Lillo A, Cardi M, Landi S, Esposito S (2018) Mechanism(s) of action of heavy metals to investigate the regulation of plastidic glucose-6-phosphate dehydrogenase. Sci Rep 8(1):13481CrossRefGoogle Scholar
  6. Debnam PM, Fernie AR, Leisse A, Golding A, Bowsher CG, Grimshaw C, Knight JS, Emes MJ (2004) Altered activity of the P2 isoform of plastidic glucose 6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves. Plant J 38:49–59CrossRefGoogle Scholar
  7. Esposito S, Guerriero G, Vona V, Di Martino Rigano V, Carfagna S, Rigano C (2005) Glutamate synthase activities and protein changes in relation to nitrogen nutrition in barley: the dependence on different plastidic glucose-6P dehydrogenase isoforms. J Exp Bot 56:55–64PubMedGoogle Scholar
  8. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875CrossRefGoogle Scholar
  9. Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103CrossRefGoogle Scholar
  10. Hauschild R, von Schaewen A (2003) Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato. Plant Physiol 133:47–62CrossRefGoogle Scholar
  11. Hutchings D, Rawsthorne S, Emes MJ (2005) Fatty acid synthesis and the oxidative pentose phosphate pathway in developing embryos of oilseed rape (Brassica napus L.). J Exp Bot 56:577–585CrossRefGoogle Scholar
  12. Kruger NJ, von Schaewen A (2003) The oxidative pentose phosphate pathway: structure and organisation. Curr Opin Plant Biol 6:236–246CrossRefGoogle Scholar
  13. Landi S, Nurcato R, De Lillo A, Lentini M, Grillo S, Esposito S (2016) Glucose-6-phosphate dehydrogenase plays a central role in the response of tomato (Solanum lycopersicum) plants to short and long-term drought. Plant Physiol Biochem 105:79–89CrossRefGoogle Scholar
  14. Leterrier M, Barroso JB, Valderrama R, Begara-Morales JC, Sanchez-Calvo B, Chaki M, Luque F, Vinegla B, Palma JM, Corpas FJ (2016) Peroxisomal NADP-isocitrate dehydrogenase is required for Arabidopsis stomatal movement. Protoplasma 253:403–415CrossRefGoogle Scholar
  15. Lin Y, Lin S, Guo H, Zhang Z, Chen X (2013) Functional analysis of PsG6PDH, a cytosolic glucose-6-phosphate dehydrogenase gene from Populus suaveolens, and its contribution to cold tolerance improvement in tobacco plants. Biotechnol Lett 35:1509–1518CrossRefGoogle Scholar
  16. Liu J, Wang X, Hu Y, Hu W, Bi Y (2013) Glucose-6-phosphate dehydrogenase plays a pivotal role in tolerance to drought stress in soybean roots. Plant Cell Rep 32:415–429CrossRefGoogle Scholar
  17. Matsumura H, Miyachi S (1980) Cycling assay for nicotinamide adenine dinucleotides. Methods Enzymol 69(6):465–470CrossRefGoogle Scholar
  18. Meyer T, Holscher C, Schwoppe C, von Schaewen A (2011) Alternative targeting of Arabidopsis plastidic glucose-6-phosphate dehydrogenase G6PD1 involves cysteine-dependent interaction with G6PD4 in the cytosol. Plant J 66:745–758CrossRefGoogle Scholar
  19. Nee G, Zaffagnini M, Trost P, Issakidis-Bourguet E (2009) Redox regulation of chloroplastic glucose-6-phosphate dehydrogenase: a new role for f-type thioredoxin. FEBS Lett 583:2827–2832CrossRefGoogle Scholar
  20. Nee G, Aumont-Nicaise M, Zaffagnini M, Nessler S, Valerio-Lepiniec M, Issakidis-Bourguet E (2014) Redox regulation of chloroplastic G6PDH activity by thioredoxin occurs through structural changes modifying substrate accessibility and cofactor binding. Biochem J 457:117–125CrossRefGoogle Scholar
  21. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  22. Pugin A, Frachisse J, Tavernier E, Bligny R, Gout E, Douce R, Guern J (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9:2077–2091CrossRefGoogle Scholar
  23. Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339(1):62–66CrossRefGoogle Scholar
  24. Sairam R, Srivastava G (2002) Changes in antioxidant activity in subcellular fraction of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 162:897–904CrossRefGoogle Scholar
  25. Scharte J, Schon H, Tjaden Z, Weis E, von Schaewen A (2009) Isoenzyme replacement of glucose-6-phosphate dehydrogenase in the cytosol improves stress tolerance in plants. Proc Natl Acad Sci USA 106:8061–8066CrossRefGoogle Scholar
  26. Shanmugam V, Wang YW, Tsednee M, Karunakaran K, Yeh KC (2015) Glutathione plays an essential role in nitric oxide-mediated iron-deficiency signaling and iron-deficiency tolerance in Arabidopsis. Plant J 84:464–477CrossRefGoogle Scholar
  27. von Schaewen A, Langenkamper G, Graeve K, Wenderoth I, Scheibe R (1995) Molecular characterization of the plastidic glucose-6-phosphate dehydrogenase from potato in comparison to its cytosolic counterpart. Plant Physiol 109:1327–1335CrossRefGoogle Scholar
  28. Wakao S, Andre C, Benning C (2008) Functional analyses of cytosolic glucose-6-phosphate dehydrogenases and their contribution to seed oil accumulation in Arabidopsis. Plant Physiol 146:277–288CrossRefGoogle Scholar
  29. Wang X, Ma Y, Huang C, Wan Q, Li N, Bi Y (2008) Glucose-6-phosphate dehydrogenase plays a central role in modulating reduced glutathione levels in reed callus under salt stress. Planta 227:611–623CrossRefGoogle Scholar
  30. Wang H, Yang L, Li Y, Hou J, Huang J, Liang W (2016) Involvement of ABA- and H2O2-dependent cytosolic glucose-6-phosphate dehydrogenase in maintaining redox homeostasis in soybean roots under drought stress. Plant Physiol Biochem 107:126–136CrossRefGoogle Scholar
  31. Wang H, Hou J, Li Y, Zhang Y, Huang J, Liang W (2017) Nitric oxide-mediated cytosolic glucose-6-phosphate dehydrogenase is involved in aluminum toxicity of soybean under high aluminum concentration. Plant Soil 416:39–52CrossRefGoogle Scholar
  32. Wendt UK, Wenderoth I, Tegeler A, Von Schaewen A (2000) Molecular characterization of a novel glucose-6-phosphate dehydrogenase from potato (Solanum tuberosum L.). Plant J 23:723–733CrossRefGoogle Scholar
  33. Yang Y, Fu Z, Su Y, Zhang X, Li G, Guo J, Que Y, Xu L (2014) A cytosolic glucose-6-phosphate dehydrogenase gene, ScG6PDH, plays a positive role in response to various abiotic stresses in sugarcane. Sci Rep 4:7090CrossRefGoogle Scholar
  34. Yang L, Wang SW, Sun LL, Ruan MJ, Li SF, He R, Zhang WY, Liang CF, WangXM Bi YR (2019a) Involvement of G6PD5 in ABA response during seed germination and root growth in Arabidopsis. BMC Plant Biol 19:44CrossRefGoogle Scholar
  35. Yang L, Wang XM, Chang N, Nan WB, Wang SW, Ruan MJ, Sun LL, Li SF, Bi YR (2019b) Cytosolic glucose-6-phosphate dehydrogenase is involved in seed germination and root growth under salinity in Arabidopsis. Front Plant Sci 10:182CrossRefGoogle Scholar
  36. Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Cell Activities and Stress Adaptations, Ministry of Education, School of Life SciencesLanzhou UniversityLanzhouChina
  2. 2.State Key Laboratory of Plateau Ecology and AgricultureQinghai UniversityXiningChina

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