Flooding of the root system in soybean: biochemical and molecular aspects of N metabolism in the nodule during stress and recovery

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• 作者：Sarah C. R. Souza ; Paulo Mazzafera ; Ladaslav Sodek
• 关键词：Amino acids ; Nitrogenase ; 15N2 incorporation ; NifH ; Asparagine ; GABA
• 刊名：Amino Acids
• 出版年：2016
• 出版时间：May 2016
• 年：2016
• 卷：48
• 期：5
• 页码：1285-1295
• 全文大小：2,750 KB
• 参考文献：Amarante L, Sodek L (2006) Waterlogging effect on xylem sap glutamine of nodulated soybean. Biol Plant 50:405–410CrossRef
  Antunes F, Aguilar M, Pineda M, Sodek L (2008) Nitrogen stress and the expression of asparagine synthetase in roots and nodules of soybean (Glycine max). Physiol Plant 133:736–743CrossRef PubMed
  Atkins CA, Pate JS, Shelp BJ (1984) Effect of short-term N2 deficiency on N metabolism in legume nodules. Plant Physiol 76:705–710CrossRef PubMed PubMedCentral
  Atkins CA, Dakora FD, Storer PJ (1990) Effect of oxygen pressure on synthesis and export of nitrogenous solutes by nodules of cowpea. Planta 182:565–571CrossRef PubMed
  Bacanamwo M, Purcell LC (1999) Soybean dry matter and N accumulation responses to flooding stress, N sources and hypoxia. J Exp Bot 50:689–696CrossRef
  Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal Biochem 17:278–293CrossRef PubMed
  Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiol 116:651–658CrossRef PubMed PubMedCentral
  Borges A, Tsai SM, Caldas DGG (2012) Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep 31:827–838CrossRef PubMed
  Bouché N, Fromm H (2004) GABA in plants: just a metabolite? Trends Plant Sci 9:110–115CrossRef PubMed
  Bown AW, Shelp BJ (1997) The metabolism and functions of γ-aminobutyric acid. Plant Physiol 115:1–5PubMed PubMedCentral
  Carroll AD, Fox GG, Laurie S, Phillips R, Ratcliffe RG, Stewart GR (1994) Ammonium assimilation and the role of γ-aminobutyric acid in pH homeostasis in carrot cell suspensions. Plant Physiol 106:513–520PubMed PubMedCentral
  Chaves das Neves HJ, Vasconcelos AMP (1987) Capillary gas chromatography of amino acids, including asparagine and glutamine: sensitive gas chromatographic-mass spectrometric and selected ion monitoring gas chromatographic-mass spectrometric detection of the N, O(S)-tert-butyldimethylsilyl derivatives. J Chromatogr 392:249–258CrossRef PubMed
  Chueire LMO, Bangel EV, Mostasso FL, Campo RJ, Pedrosa FO, Hungria M (2003) Taxonomic classification of rhizobial strains recommended for soybean and common bean crops in Brazil based on the sequencing of the 16s rRNA gene. Rev Bras Ciênc Solo 27:833–840CrossRef
  Crawford LA, Bown AW, Breitkreuz KE, Guinel FC (1994) The synthesis of γ-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiol 104:865–871PubMed PubMedCentral
  Dakora FD (2000) Commonality of root nodulation signals and nitrogen assimilation in tropical grain legumes belonging to the tribe Phaseoleae. Aust J Plant Physiol 27:885–892
  Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage development descriptions for soybeans Glycine max (L) Merril. Crop Sci 11:929–931CrossRef
  Gil-Quintana E, Larrainzar E, Arrese-Igor C, González EM (2013a) Is N-feedback involved in the inhibition of nitrogen fixation in drought-stressed Medicago truncatula? J Exp Bot 64:281–292CrossRef PubMed PubMedCentral
  Gil-Quintana E, Larrainzar E, Seminario A, Díaz-Leal JL, Alamillo JM, Pineda M, Arrese-Igor C, Wienkoop S, González EM (2013b) Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean. J Exp Bot 64:2171–2182CrossRef PubMed PubMedCentral
  Godber IM, Parsons R (1998) Translocation of amino acids from stem nodules of Sesbania rostrata demonstrated by GC-MS in planta 15N isotope dilution. Plant, Cell Environ 21:1089–1099CrossRef
  Gout E, Boisson AM, Aubert S, Douce R, Bligny R (2001) Origin of the cytoplasmic pH changes during anaerobic stress in higher plant cells Carbon-13 and phosphorous-31 nuclear magnetic resonance studies. Plant Physiol 125:912–925CrossRef PubMed PubMedCentral
  Herridge DF, Peoples MB (1990) Ureide assay for measuring nitrogen fixation by nodulated soybean calibrated by 15N methods. Plant Physiol 93:495–503CrossRef PubMed PubMedCentral
  Herridge DF, Bergensen FJ, Peoples MB (1990) Measurement of nitrogen fixation by soybean in the field using the ureide and natural 15N abundance methods. Plant Physiol 93:708–716CrossRef PubMed PubMedCentral
  Hoagland DR, Arnon DI (1950) The water-culture method of growing plants without soil. California Agricultural Experiment Station, Bulletin, Vol 347, 2 Ed, pp 1–32
  Hyun TK, Eom SH, Jeun YC, Han SH, Kim JS (2013) Identification of glutamate decarboxylases as a γ-aminobutyric acid (GABA) biosynthetic enzyme in soybean. Ind Crop Prod 49:864–870CrossRef
  Jordan BR, Givan CV (1979) Effects of light and inhibitors on glutamate metabolism in leaf discs of Vicia faba L: sources of ATP for glutamine synthesis and photoregulation of tricarboxylic acid cycle metabolism. Plant Physiol 64:1043–1047CrossRef PubMed PubMedCentral
  Joy KW, Ireland RJ (1990) Enzymes of asparagine metabolism. In: Dey PM, Harborne JB, Lea PJ (eds) Methods in plant biochemistry. Chapter 17. Academic Press, London, pp 287–296
  Justino GC, Sodek L (2013) Recovery of nitrogen fixation after short-term flooding of the nodulated root system of soybean. J Plant Physiol 170:235–241CrossRef PubMed
  King CA, Purcell LC (2005) Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. Plant Physiol 137:1389–1396CrossRef PubMed PubMedCentral
  Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Rev Plant Sci 19:479–509CrossRef
  Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu Rev Plant Physiol Mol Biol 47:569–593CrossRef
  Layzell DB, Hunt S (1990) Oxygen and the regulation of nitrogen fixation in legume nodules. Physiol Plant 80:322–327CrossRef
  Layzell DB, Hunt S, Palmer GR (1990) Mechanism of nitrogenase inhibition in soybean nodules Pulse-modulated spectroscopy indicates that nitrogenase activity is limited by O2. Plant Physiol 92:1101–1107CrossRef PubMed PubMedCentral
  Libault M, Thibivilliers S, Bilgin DD, Radwan O, Benitez M, Clough SJ, Stacey G (2008) Identification of four soybean reference genes for gene expression normalization. Plant Gen 1:44–54CrossRef
  Lima JD, Sodek L (2003) N-stress alters aspartate and asparagine levels of xylem sap in soybean. Plant Sci 165:649–656CrossRef
  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRef PubMed
  Loureiro MF, James EK, Franco AA (1998) Nitrogen fixation by legumes in flooded regions. In: Scarano FR, Franco AC (eds) Ecophysiological strategies of xerophytic and amphibious plants in the neotropics. Oecologia Brasiliensis, (Series) Vol IV, PPGE-UFRJ, Rio de Janeiro, pp 195–233
  Masclaux-Daubresse C, Reisdorf-Cren M, Pageau K, Lelandais M, Grandjean O, Kronenberger J, Valadier MH, Feraud M, Jouglet T, Suzuki A (2006) Glutamine synthetase—glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiol 140:444–456CrossRef PubMed PubMedCentral
  McClure PR, Israel DW, Volk RJ (1980) Evaluation of the relative ureide content of xylem sap as an indicator of N2 fixation in soybeans—greenhouse studies. Plant Physiol 66:720–725CrossRef PubMed PubMedCentral
  McNeil DL, LaRue TA (1984) Effect of nitrogen source on ureides in soybean. Plant Physiol 74:227–232CrossRef PubMed PubMedCentral
  Narayan VS, Nair PM (1990) Metabolism, enzymology and possible roles of 4-aminobutyrate in higher plants. Phytochemistry 29:367–375CrossRef
  Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT (2011) Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol 190:472–487CrossRef PubMed
  Norris DO, Date RA (1976) Legume bacteriology. In: Shaw NH, Bryan WW (eds) Tropical pastures research; principles and methods. Commonwealth Bureau of pastures and Field Crops Hurley, Bulletin 51, England, pp 134–174
  Puiatti M, Sodek L (1999) Waterlogging affects nitrogen transport in the xylem of soybean. Plant Physiol Biochem 37:767–773CrossRef
  Roberts JKM, Callis J, Wemmer D, Walbot V, Jardetzky O (1984) Mechanisms of cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under hypoxia. Proc Natl Acad Sci USA 81:3379–3383CrossRef PubMed PubMedCentral
  Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010a) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513CrossRef PubMed PubMedCentral
  Rocha M, Sodek L, Licausi F, Hameed MW, Dornelas MC, van Dongen JT (2010b) Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilizers during hypoxic stress. Amino Acids 39:1043–1053CrossRef PubMed PubMedCentral
  Sánchez C, Gates AJ, Meakin GE, Uchiumi T, Girard L, Richardson DJ, Bedmar EJ, Delgado MJ (2010) Production of nitric oxide and nitrosylleghemoglobin complexes in soybean nodules in response to flooding. Mol Plant Microb Interact 23:702–711CrossRef
  Sánchez C, Tortosa G, Granados A, Delgado A, Bedmar EJ, Delgado MJ (2011) Involvement of Bradyrhizobium japonicum denitrification in symbiotic nitrogen fixation by soybean plants subjected to flooding. Soil Biol Biochem 43:212–217CrossRef
  Schubert KR (1986) Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. Ann Rev Plant Physiol 37:539–574CrossRef
  Scott-Taggart CP, Van Cauwenberghe OR, McLean MD, Shelp BJ (1999) Regulation of γ-aminobutyric acid synthesis in situ by glutamate availability. Physiol Plant 106:363–369CrossRef
  Serraj R, Shelp BJ, Sinclair TR (1998) Accumulation of γ-aminobutyric acid in nodulated soybean in response to stress. Physiol Plant 102:79–86CrossRef
  Shelp BJ, Walton CS, Snedden WA, Tuin LG, Oresnik IJ, Layzell DB (1995) GABA shunt in developing soybean seeds is associated with hypoxia. Physiol Plant 94:219–228CrossRef
  Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452CrossRef PubMed
  Shimamura S, Mochizuki T, Nada Y, Fukuyama M (2002) Secondary aerenchyma formation and its relation to nitrogen fixation in root nodules of soybean plants (Glycine max) grown under flooded conditions. Plant Prod Sci 5:294–300CrossRef
  Sulieman S, Schulze J (2010) Phloem-derived γ-aminobutyric acid (GABA) is involved in upregulating nodule N2 fixation efficiency in the model legume Medicago truncatula. Plant Cell Environ 33:2162–2172CrossRef PubMed
  Witty JF, Skøt L, Revsbech NP (1987) Direct evidence for changes in the resistance of legume root nodules to O2 diffusion. J Exp Bot 38:1129–1140CrossRef
  Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analyst 80:209–213CrossRef
  Zabalza A, Van Dongen JT, Froehlich A, Oliver SN, Faix B, Gupta KJ, Schmälzlin E, Igal M, Orcaray L, Royuela M, Geigenberger P (2009) Regulation of respiration and fermentation to control the plant internal oxygen concentration. Plant Physiol 149:1087–1098CrossRef PubMed PubMedCentral
  
• 作者单位：Sarah C. R. Souza (1)
  Paulo Mazzafera (1)
  Ladaslav Sodek (1)
  
  1. Department of Plant Biology, Institute of Biology, University of Campinas-UNICAMP, PO Box 6109, Campinas, SP, 13083-970, Brazil
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Biochemistry
  Analytical Chemistry
  Biochemical Engineering
  Life Sciences
  Proteomics
  Neurobiology
  
• 出版者：Springer Wien
• ISSN：1438-2199
• 卷排序：48

文摘

Nitrogen fixation of the nodule of soybean is highly sensitive to oxygen deficiency such as provoked by waterlogging of the root system. This study aimed to evaluate the effects of flooding on N metabolism in nodules of soybean. Flooding resulted in a marked decrease of asparagine (the most abundant amino acid) and a concomitant accumulation of γ-aminobutyric acid (GABA). Flooding also resulted in a strong reduction of the incorporation of 15N₂ in amino acids. Nodule amino acids labelled before flooding rapidly lost 15N during flooding, except for GABA, which initially increased and declined slowly thereafter. Both nitrogenase activity and the expression of nifH and nifD genes were strongly decreased on flooding. Expression of the asparagine synthetase genes SAS1 and SAS2 was reduced, especially the former. Expression of genes encoding the enzyme glutamic acid decarboxylase (GAD1, GAD4, GAD5) was also strongly suppressed except for GAD2 which increased. Almost all changes observed during flooding were reversible after draining. Possible changes in asparagine and GABA metabolism that may explain the marked fluctuations of these amino acids during flooding are discussed. It is suggested that the accumulation of GABA has a storage role during flooding stress. Keywords Amino acids Nitrogenase 15N₂ incorporation NifH Asparagine GABA