Plant and Soil

, Volume 430, Issue 1–2, pp 37–48 | Cite as

Glucose-6-phosphate dehydrogenase plays a vital role in Achnatherum inebrians plants host to Epichloë gansuensis by improving growth under nitrogen deficiency

  • Jianfeng Wang
  • Zhibiao NanEmail author
  • Michael J. Christensen
  • Chunjie Li
Regular Article


Background and aims

Low nitrogen negatively affects soil fertility and plant productivity. Glucose-6-phosphate dehydrogenase (G6PDH) and Epichloë gansuensis endophytes are two factors that are associated with tolerance of Achnatherum inebrians to abiotic stress. However, the possibility that E. gansuensis interacts with G6PDH in enhancing low nitrogen tolerance of host grasses has not been examined.


A. inebrians plants with (E+) and without E. gansuensis (E−) were subjected to different nitrogen concentration treatments (0.1, 1, and 7.5 mM). After 90 days, physiological studies were carried out to investigate the participation of G6PDH in the adaption of host plants to low nitrogen availability.


Low nitrogen retarded the growth of A. inebrians. E+ plants had higher total dry weight, chlorophyll a and b contents, net photosynthesis rate, G6PDH activity, and GSH content, while having lower plasma membrane (PM) NADPH oxidase activity, NADPH/NADP+ ratios, and MDA and H2O2 than in E− A. inebrians plants under low nitrogen concentration.


The presence of E. gansuensis played a key role in maintaining the growth of the A. inebrians plants under low nitrogen concentration by regulating G6PDH activity and the NADPH/NADP+ ratio and improving net photosynthesis rate.


Achnatherum inebrians Epichloë gansuensis endophyte Low nitrogen Glucose-6-phosphate dehydrogenase 



We wish to thank Xingxu Zhang, Chao Xia, Shan Xu, and Yane Guo for their help and advice during the preliminary stages of this project.

Author contributions

Designed the research: Jianfeng Wang and Zhibiao Nan. Performed the research: Jianfeng Wang and Zhibiao Nan. Analyzed the data: Jianfeng Wang and Zhibiao Nan. Wrote the paper: Jianfeng Wang, Zhibiao Nan, Michael Christensen, and Chunjie Li.

Funding information

This research was financially supported by National Basic Research Program of China (2014CB138702) and the National Nature Science Foundation of China (31772665), and the Open Foundation of Research Institute of Qilian Mountains, Lanzhou University.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.


  1. Abenavoli MR, Longo C, Lupini A, Miller AJ, Araniti F, Mercati F, Princi MP, Sunseri F (2016) Phenotyping two tomato genotypes with different nitrogen use efficiency. Plant Physiol Biochem 107:21–32CrossRefPubMedGoogle Scholar
  2. Anderson JV, Chevone BI, Hess JL (1992) Seasonal variation in the antioxidant system of eastern white pine needles evidence for thermal dependence. Plant Physiol 98:501–508CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bilodeau-Gauthier S, Paré D, Messier C, Bélanger N (2011) Juvenile growth of hybrid poplars on acidic boreal soil determined by environmental effects of soil preparation, vegetation control, and fertilization. For Ecol Manag 261:620–629CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  5. Brouwer R (1962) Nutritive influences on the distribution of dry matter in the plant [sn]Google Scholar
  6. Chen L, Li X, Swoboda GA, Young CA, Sugawara K, Leuchtmann A, Schardl CL (2015) Two distinct Epichloë species symbiotic with Achnatherum inebrians, drunken horse grass. Mycologia 107(4):863–873CrossRefPubMedGoogle Scholar
  7. Chen N, He R, Chai Q, Li C, Nan Z (2016) Transcriptomic analyses giving insights into molecular regulation mechanisms involved in cold tolerance by Epichloë endophyte in seed germination of Achnatherum inebrians. Plant Growth Regul 80:367–375CrossRefGoogle Scholar
  8. Christensen MJ, Bennett RJ, Ansari HA, Koga H, Johnson RD, Bryan GT, Simpson WR, Koolaard JP, Nickless EM, Voisey CR (2008) Epichloë endophytes grow by intercalary hyphal extension in elongating grass leaves. Fungal Genet Biol 45:84–93CrossRefPubMedGoogle Scholar
  9. DeLong JM, Steffen KL (1997) Photosynthetic function, lipid peroxidation, and α-tocopherol content in spinach leaves during exposure to UV-B radiation. Can J Plant Sci 77:453–459CrossRefGoogle Scholar
  10. Deng K, Peng H, Li W, Warren B, Fletcher I (1998) The ergonovine content and the nutritive value of ammoniated drunken horse grass with urea. Pratacul Sci 15:10–13Google Scholar
  11. Desclaux D, Huynh T-T, Roumet P (2000) Identification of soybean plant characteristics that indicate the timing of drought stress. Crop Sci 40:716–722CrossRefGoogle Scholar
  12. Drew M, Saker L (1975) Nutrient supply and the growth of the seminal root system in barley: II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. J Exp Bot 26:79–90CrossRefGoogle Scholar
  13. Duan ZQ, Bai L, Zhao ZG, Zhang GP, Cheng FM, Jiang LX, Chen KM (2009) Drought-stimulated activity of plasma membrane nicotinamide adenine dinucleotide phosphate oxidase and its catalytic properties in rice. J Integr Plant Biol 51:1104–1115CrossRefPubMedGoogle Scholar
  14. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefPubMedGoogle Scholar
  15. Fleetwood DJ, Scott B, Lane GA, Tanaka A, Johnson RD (2007) A complex ergovaline gene cluster in Epichloë endophytes of grasses. Appl Environ Microbiol 73:2571–2579CrossRefPubMedPubMedCentralGoogle Scholar
  16. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25CrossRefPubMedGoogle Scholar
  17. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gundel PE, Hamilton CE, Seal CE, Helander M, Martínez-Ghersa MA, Ghersa CM, Vázquez de Aldana BR, Zabalgogeazcoa I, Saikkonen K (2012) Antioxidants in Festuca rubra L. seeds affected by the fungal symbiont Epichloë festucae. Symbiosis 58:73–80CrossRefGoogle Scholar
  19. Gundel PE, Garibaldi LA, Helander M, Saikkonen K (2013) Symbiotic interactions as drivers of trade-offs in plants: effects of fungal endophytes on tall fescue. Fungal Divers 60:5–14CrossRefGoogle Scholar
  20. Hauschild R, von Schaewen A (2003) Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato. Plant Physiol 133:47–62CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hufstetler EV, Boerma HR, Carter TE, Earl HJ (2007) Genotypic variation for three physiological traits affecting drought tolerance in soybean. Crop Sci 47:25–35CrossRefGoogle Scholar
  22. Jones MA, Raymond MJ, Yang Z, Smirnoff N (2007) NADPH oxidase-dependent reactive oxygen species formation required for root hair growth depends on ROP GTPase. J Exp Bot 58:1261–1270CrossRefPubMedGoogle Scholar
  23. Ju XT, Xing GX, Chen XP, Zhang SL, Zhang LJ, Liu XJ, Cui ZL, Yin B, Christie P, Zhu ZL (2009) Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proc Natl Acad Sci U S A 106:3041–3046CrossRefPubMedPubMedCentralGoogle Scholar
  24. Khamis S, Lamaze T, Lemoine Y, Foyer C (1990) Adaptation of the photosynthetic apparatus in maize leaves as a result of nitrogen limitation relationships between electron transport and carbon assimilation. Plant Physiol 94:1436–1443CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kletzien R, Harris P, Foellmi L (1994) Glucose-6-phosphate dehydrogenase: a “housekeeping” enzyme subject to tissue-specific regulation by hormones, nutrients, and oxidant stress. FASEB J 8:174–181CrossRefPubMedGoogle Scholar
  26. Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53:773–787CrossRefPubMedGoogle Scholar
  27. Lea PJ, Azevedo RA (2006) Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Ann Appl Biol 149:243–247CrossRefGoogle Scholar
  28. Leopold JA, Walker J, Scribner AW, Voetsch B, Zhang YY, Loscalzo AJ, Stanton RC, Loscalzo J (2003) Glucose-6-phosphate dehydrogenase modulates vascular endothelial growth factor-mediated angiogenesis. J Biol Chem 278:32100–32106CrossRefPubMedGoogle Scholar
  29. Li C, Nan Z, Gao J, Tian P (2004) Detection and distribution of Neotyphodium-Achnatherum inebrians association in China. Proceedings of 5th international Neotyphodium/grass interactions symposium, Arkansas, USAGoogle Scholar
  30. Li C, Zhang X, Li F, Nan Z, Schardl C (2007) Disease and pests resistance of endophyte infected and non-infected drunken horse grass. Proceedings of the 6th international symposium on fungal endophytes of grasses. Dunedin, New Zealand: New Zealand Grassland AssociationGoogle Scholar
  31. Li J, Chen G, Wang X, Zhang Y, Jia H, Bi Y (2011) Glucose-6-phosphate dehydrogenase-dependent hydrogen peroxide production is involved in the regulation of plasma membrane H+-ATPase and Na+/H+ antiporter protein in salt-stressed callus from Carex moorcroftii. Physiol Plant 141:239–250CrossRefPubMedGoogle Scholar
  32. Liu Y, Wu R, Wan Q, Xie G, Bi Y (2007) Glucose-6-phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. Plant Cell Physiol 48:511–522CrossRefPubMedGoogle Scholar
  33. 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 32:415–429CrossRefPubMedGoogle Scholar
  34. Luo J, Li H, Liu T, Polle A, Peng C, Luo Z-B (2013) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64:4207–4224CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63:305–317CrossRefPubMedGoogle Scholar
  36. Marschner H (1995) Mineral nutrition of higher plants. Academic Press, LondonGoogle Scholar
  37. Matsumura H, Miyachi S (1980) [43] Cycling assay for nicotinamide adenine dinucleotides. Methods Enzymol 69:465–470CrossRefGoogle Scholar
  38. McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10:1011–1025CrossRefPubMedGoogle Scholar
  39. Müller CB, Krauss J (2005) Symbiosis between grasses and asexual fungal endophytes. Curr Opin Plant Biol 8:450–456CrossRefPubMedGoogle Scholar
  40. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566CrossRefPubMedPubMedCentralGoogle Scholar
  41. Nan Z, Li C (2000) Neotyphodium in native grasses in China and observations on endophyte/host interactions. Proceedings of the 4th international neotyphodium-grass interactions symposium, SoestGoogle Scholar
  42. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279CrossRefGoogle Scholar
  43. Noctor G, Arisi A-CM, Jouanin L, Foyer CH (1998) Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiol 118:471–482CrossRefPubMedPubMedCentralGoogle Scholar
  44. Qiu QS, Su XF (1999) The influence of extracellular-side Ca2+ on the activity of the plasma membrane H+-ATPase from wheat roots. Funct Plant Biol 25:923–928Google Scholar
  45. Rahman M, Saiga S (2005) Endophytic fungi (Neotyphodium coenophialum) affect the growth and mineral uptake, transport and efficiency ratios in tall fescue (Festuca arundinacea). Plant Soil 272:163–171CrossRefGoogle Scholar
  46. Rennenberg H, Wildhagen H, Ehlting B (2010) Nitrogen nutrition of poplar trees. Plant Biol 12:275–291CrossRefPubMedGoogle Scholar
  47. Sabzalian RM, Mirlohi A (2010) Neotyphodium endophytes trigger salt resistance in tall and meadow fescues. J Plant Nutr Soil Sci 173:952–957CrossRefGoogle Scholar
  48. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340CrossRefPubMedGoogle Scholar
  49. Shi Z (1997) Important poisonous plants of China grassland, vol 166. China Agriculture Press, Beijing, p 176Google Scholar
  50. Šindelář L, Šindelářová M (2002) Correlation of viral RNA biosynthesis with glucose-6-phosphate dehydrogenase activity and host resistance. Planta 215:862–869CrossRefPubMedGoogle Scholar
  51. Ślaski JJ, Zhang G, Basu U, Stephens JL, Taylor GJ (1996) Aluminum resistance in wheat (Triticum aestivum) is associated with rapid, Al-induced changes in activities of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase in root apices. Physiol Plant 98:477–484CrossRefGoogle Scholar
  52. Song M, Chai Q, Li X, Yao X, Li C, Christensen MJ, Nan Z (2015a) An asexual Epichloë endophyte modifies the nutrient stoichiometry of wild barley (Hordeum brevisubulatum) under salt stress. Plant Soil 387:153–165CrossRefGoogle Scholar
  53. Song M, Li X, Saikkonen K, Li C, Nan Z (2015b) An asexual Epichloë endophyte enhances waterlogging tolerance of Hordeum brevisubulatum. Fungal Ecol 13:44–52CrossRefGoogle Scholar
  54. Tsuchida H, Tamai T, Fukayama H, Agarie S, Nomura M, Onodera H, Ono K, Nishizawa Y, Lee B-H, Hirose S (2001) High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth in a C3 plant, rice. Plant Cell Physiol 42:138–145CrossRefPubMedGoogle Scholar
  55. Van Gestelen P, Asard H, Caubergs RJ (1997) Solubilization and separation of a plant plasma membrane NADPH-O2-synthase from other NAD(P)H oxidoreductases. Plant Physiol 115:543–550CrossRefPubMedPubMedCentralGoogle Scholar
  56. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66CrossRefGoogle Scholar
  57. Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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 227:611–623CrossRefPubMedGoogle Scholar
  59. Wang X, Pan Q, Chen F, Yan X, Liao H (2011) Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza 21:173–181CrossRefPubMedGoogle Scholar
  60. Wang F, Wang X, Zhao C, Wang J, Li P, Dou Y, Bi Y (2016a) Alternative pathway is involved in the tolerance of highland barley to the low-nitrogen stress by maintaining the cellular redox homeostasis. Plant Cell Rep 35:317–328CrossRefPubMedGoogle Scholar
  61. Wang JW, Tian H, Yu X, Zheng LP (2016b) Glucose-6-phosphate dehydrogenase plays critical role in artemisinin production of Artemisia annua under salt stress. Biol Plant:1–11Google Scholar
  62. Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313CrossRefGoogle Scholar
  63. Xia C, Zhang X, Christensen MJ, Nan Z, Li C (2015) Epichloë endophyte affects the ability of powdery mildew (Blumeria graminis) to colonise drunken horse grass (Achnatherum inebrians). Fungal Ecol 16:26–33CrossRefGoogle Scholar
  64. Xia C, Li N, Zhang X, Feng Y, Christensen MJ, Nan Z (2016) An Epichloë endophyte improves photosynthetic ability and dry matter production of its host Achnatherum inebrians infected by Blumeria graminis under various soil water conditions. Fungal Ecol 22:26–34CrossRefGoogle Scholar
  65. Xia C, Christensen MJ, Zhang X, Nan Z (2018) Effect of Epichloë gansuensis endophyte and transgenerational effects on the water use efficiency, nutrient and biomass accumulation of Achnatherum inebrians under soil water deficit. Plant Soil 424(1–2):555–571CrossRefGoogle Scholar
  66. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182CrossRefPubMedGoogle Scholar
  67. Zhang X, Li C, Nan Z (2010) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175:703–709CrossRefPubMedGoogle Scholar
  68. Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2011) Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Plant 143:396–407CrossRefPubMedGoogle Scholar
  69. Zhang LT, Zhang ZS, Gao HY, Meng XL, Yang C, Liu JG, Meng QW (2012a) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:40CrossRefPubMedPubMedCentralGoogle Scholar
  70. Zhang X, Li C, Nan Z, Matthew C (2012b) Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators. Weed Res 52:70–78CrossRefGoogle Scholar
  71. Zhang L, Liu J, Wang X, Bi Y (2013) Glucose-6-phosphate dehydrogenase acts as a regulator of cell redox balance in rice suspension cells under salt stress. Plant Growth Regul 69:139–148CrossRefGoogle Scholar
  72. Zhao C, Wang X, Wang X, Wu K, Li P, Chang N, Wang J, Wang F, Li J, Bi Y (2015) Glucose-6-phosphate dehydrogenase and alternative oxidase are involved in the cross tolerance of highland barley to salt stress and UV-B radiation. J Plant Physiol 181:83–95CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Grassland Agro-Ecosystems, College of Pastoral Agriculture Science and TechnologyLanzhou UniversityLanzhouChina
  2. 2.Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture, China, College of Pastoral Agriculture Science and TechnologyLanzhou UniversityLanzhouChina
  3. 3.AgResearch, Grasslands Research CentrePalmerston NorthNew Zealand

Personalised recommendations