Glucose-6-Phosphate Dehydrogenase Is Involved in the Tolerance of Soybean Seedlings to Low Nitrogen Stress

Nitrogen (N) deficiency affects plant growth and crop yield. In this study, we investigated the role of glucose-6-phosphate dehydrogenase (G6PDH) in response to N availability in three soybean cultivars, JINDOU 19 (JD19), LONGHUANG 3 (LH3), and LONGDOU 2 (LD2), that have different tolerances to low-N stress. The results showed that the leaf area and primary root length of JD19 and LH3 were greater than that of LD2 under low-N stress, suggesting that the growth of JD19 and LH3 were impaired less than LD2, and thus are more tolerant to low-N stress than LD2 is. Interestingly, the G6PDH expression showed different degrees of change in these soybean cultivars under low-N conditions, and the G6PDH activity in JD19 and LH3 was higher than that in LD2. When G6PDH was inhibited by glucosamine (GlcN), the contents of malondialdehyde (MDA) and H2O2 were dramatically increased under low-N stress. Meanwhile, the activities of N metabolism-related enzymes were inhibited. These results indicate that G6PDH is involved in the tolerance of soybean cultivars to low-N stress through affecting the N metabolism. Furthermore, under low-N conditions, the contents of NADP+ and reduced glutathione (GSH) in JD19 and LH3 were increased more than that in LD2. In contrast, the activity of the plasma membrane (PM), NADPH oxidase, and the NADPH content in JD19 and LH3 were lower than that in LD2. In conclusion, G6PDH reduces the accumulation of ROS in plant cells by modulating NADPH/NADP+ and GSH levels to maintain the growth of soybeans under low-N conditions.

[1]  Xiaomin Wang,et al.  The response mechanism to salt stress in Arabidopsis transgenic lines over-expressing of GmG6PD. , 2021, Plant physiology and biochemistry : PPB.

[2]  Xiaomin Wang,et al.  Nitric oxide and hydrogen peroxide increase glucose-6-phosphate dehydrogenase activities and expression upon drought stress in soybean roots , 2019, Plant Cell Reports.

[3]  Xiaomin Wang,et al.  Cytosolic Glucose-6-Phosphate Dehydrogenase Is Involved in Seed Germination and Root Growth Under Salinity in Arabidopsis , 2019, Front. Plant Sci..

[4]  Z. Nan,et al.  Effect of Epichloë gansuensis Endophyte on the Nitrogen Metabolism, Nitrogen Use Efficiency, and Stoichiometry of Achnatherum inebrians under Nitrogen Limitation. , 2018, Journal of agricultural and food chemistry.

[5]  Bin Hu,et al.  Nitrogen use efficiency in crops: lessons from Arabidopsis and rice. , 2017, Journal of experimental botany.

[6]  Huahua Wang,et al.  Nitric oxide-mediated cytosolic glucose-6-phosphate dehydrogenase is involved in aluminum toxicity of soybean under high aluminum concentration , 2017, Plant and Soil.

[7]  Huahua Wang,et al.  Involvement of ABA- and H2O2-dependent cytosolic glucose-6-phosphate dehydrogenase in maintaining redox homeostasis in soybean roots under drought stress. , 2016, Plant physiology and biochemistry : PPB.

[8]  M. Lentini,et al.  Glucose-6-phosphate dehydrogenase plays a central role in the response of tomato (Solanum lycopersicum) plants to short and long-term drought. , 2016, Plant physiology and biochemistry : PPB.

[9]  S. Esposito.  Nitrogen Assimilation, Abiotic Stress and Glucose 6-Phosphate Dehydrogenase: The Full Circle of Reductants , 2016, Plants.

[10]  C. Jonak,et al.  The GSK3/Shaggy-Like Kinase ASKα Contributes to Pattern-Triggered Immunity1[OPEN] , 2016, Plant Physiology.

[11]  Ping Li,et al.  Alternative pathway is involved in the tolerance of highland barley to the low-nitrogen stress by maintaining the cellular redox homeostasis , 2016, Plant Cell Reports.

[12]  Simone Landi,et al.  Expression and characterization of a cytosolic glucose 6 phosphate dehydrogenase isoform from barley (Hordeum vulgare) roots. , 2015, Protein expression and purification.

[13]  K. N. Reddy,et al.  Effects of Row-Type, Row-Spacing, Seeding Rate, Soil-Type, and Cultivar Differences on Soybean Seed Nutrition under US Mississippi Delta Conditions , 2015, PloS one.

[14]  Ping Li,et al.  Glucose-6-phosphate dehydrogenase and alternative oxidase are involved in the cross tolerance of highland barley to salt stress and UV-B radiation. , 2015, Journal of plant physiology.

[15]  Joshua D. Rabinowitz,et al.  The return of metabolism: biochemistry and physiology of the pentose phosphate pathway , 2014, Biological reviews of the Cambridge Philosophical Society.

[16]  X. Chen,et al.  Arabidopsis Enhanced Drought Tolerance1/HOMEODOMAIN GLABROUS11 Confers Drought Tolerance in Transgenic Rice without Yield Penalty1[W][OA] , 2013, Plant Physiology.

[17]  Xiaomin Wang,et al.  Hydrogen peroxide is involved in the regulation of rice (Oryza sativa L.) tolerance to salt stress , 2013, Acta Physiologiae Plantarum.

[18]  Xiaomin Wang,et al.  Glucose-6-phosphate dehydrogenase plays a pivotal role in tolerance to drought stress in soybean roots , 2013, Plant Cell Reports.

[19]  Xiaomin Wang,et al.  Glucose-6-phosphate dehydrogenase acts as a regulator of cell redox balance in rice suspension cells under salt stress , 2013, Plant Growth Regulation.

[20]  Y. Gibon,et al.  Stress-Induced GSK3 Regulates the Redox Stress Response by Phosphorylating Glucose-6-Phosphate Dehydrogenase in Arabidopsis[C][W][OA] , 2012, Plant Cell.

[21]  Guohua Xu,et al.  Plant nitrogen assimilation and use efficiency. , 2012, Annual review of plant biology.

[22]  Zishan Zhang,et al.  The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves , 2012, BMC Plant Biology.

[23]  Zishan Zhang,et al.  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. , 2011, Physiologia plantarum.

[24]  Hironari Nomura,et al.  A plastidic glucose-6-phosphate dehydrogenase is responsible for hypersensitive response cell death and reactive oxygen species production , 2011, Journal of General Plant Pathology.

[25]  Xiaomin Wang,et al.  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. , 2011, Physiologia plantarum.

[26]  K. Kim,et al.  Enhanced drought tolerance in Arabidopsis via genetic manipulation aimed at the reduction of glucosamine-induced ROS generation , 2010, Plant Molecular Biology.

[27]  S. Yadav.  Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants , 2010 .

[28]  Guo-ping Zhang,et al.  Drought-stimulated activity of plasma membrane nicotinamide adenine dinucleotide phosphate oxidase and its catalytic properties in rice. , 2009, Journal of integrative plant biology.

[29]  Shao Hongbo,et al.  Roles of plant soluble sugars and their responses to plant cold stress , 2009 .

[30]  J. Specht,et al.  Nitrogen uptake, fixation and response to fertilizer N in soybeans: A review , 2008 .

[31]  Xiaomin Wang,et al.  Involvement of glucose-6-phosphate dehydrogenase in reduced glutathione maintenance and hydrogen peroxide signal under salt stress , 2008, Plant signaling & behavior.

[32]  H. Shao,et al.  Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells , 2007, International journal of biological sciences.

[33]  Yong-song Zhang,et al.  Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.). , 2007, Plant, cell & environment.

[34]  C. Benning,et al.  Functional Analyses of Cytosolic Glucose-6-Phosphate Dehydrogenases and Their Contribution to Seed Oil Accumulation in Arabidopsis1[OA] , 2007, Plant Physiology.

[35]  Zhaopu Liu,et al.  Physiological and ecological characters studies on Aloe vera under soil salinity and seawater irrigation , 2007 .

[36]  R. Tewari,et al.  Oxidative Stress and Antioxidant Responses in Young Leaves of Mulberry Plants Grown Under Nitrogen, Phosphorus or Potassium Deficiency , 2007 .

[37]  A. Wachter,et al.  Maturation of Arabidopsis Seeds Is Dependent on Glutathione Biosynthesis within the Embryo1[C] , 2006, Plant Physiology.

[38]  P. Mullineaux,et al.  Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression , 2005, Photosynthesis Research.

[39]  C. Foyer,et al.  Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses , 2005, The Plant Cell Online.

[40]  A. Miller,et al.  Root Nitrogen Acquisition and Assimilation , 2005, Plant and Soil.

[41]  C. Benning,et al.  Genome-wide analysis of glucose-6-phosphate dehydrogenases in Arabidopsis. , 2004, The Plant journal : for cell and molecular biology.

[42]  D. Salt,et al.  Increased Glutathione Biosynthesis Plays a Role in Nickel Tolerance in Thlaspi Nickel Hyperaccumulators , 2004, The Plant Cell Online.

[43]  A. S. Raghavendra,et al.  Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. , 2003, Trends in plant science.

[44]  R. Mittler.  Oxidative stress, antioxidants and stress tolerance. , 2002, Trends in plant science.

[45]  N. Crawford,et al.  Molecular and Developmental Biology of Inorganic Nitrogen Nutrition , 2002, The arabidopsis book.

[46]  K. Niyogi,et al.  Non-photochemical quenching. A response to excess light energy. , 2001, Plant physiology.

[47]  V. Vona,et al.  Glucose-6-phosphate dehydrogenase in barley roots: kinetic properties and localisation of the isoforms , 2001, Planta.

[48]  M. Emes,et al.  Isolation and characterisation of a full-length genomic clone encoding a plastidic glucose 6-phosphate dehydrogenase from Nicotiana tabacum , 2001, Planta.

[49]  L. Luzzatto,et al.  Solution of the structure of tetrameric human glucose 6-phosphate dehydrogenase by molecular replacement. , 1999, Acta crystallographica. Section D, Biological crystallography.

[50]  C. Forney,et al.  Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds , 1999, Planta.

[51]  S. Filosa,et al.  Enhanced Glutathione Levels and Oxidoresistance Mediated by Increased Glucose-6-phosphate Dehydrogenase Expression* , 1999, The Journal of Biological Chemistry.

[52]  C. Foyer,et al.  ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control. , 1998, Annual review of plant physiology and plant molecular biology.

[53]  José,et al.  A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes. , 1998, The Biochemical journal.

[54]  H. Asard,et al.  Solubilization and Separation of a Plant Plasma Membrane NADPH-O2- Synthase from Other NAD(P)H Oxidoreductases , 1997, Plant physiology.

[55]  N. Crawford,et al.  Nitrate: nutrient and signal for plant growth. , 1995, The Plant cell.

[56]  P. Saradhi,et al.  Proline accumulation under heavy metal stress , 1991 .

[57]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[58]  I. D. Teare,et al.  Rapid determination of free proline for water-stress studies , 1973, Plant and Soil.

[59]  M. M. Chaves,et al.  Photosynthesis and drought: can we make metabolic connections from available data? , 2011, Journal of experimental botany.

[60]  Q. Qiu,et al.  The influence of extracellular-side Ca2+ on the activity of the plasma membrane H+-ATPase from wheat roots , 1998 .