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Nitrogen Metabolism and Photosynthesis in Leymus chinensis in Response to Long-term Soil Drought

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Abstract

Key enzyme activities related to nitrogen metabolism, gas-exchange, chlorophyll fluorescence, and lipid peroxidation were determined in Leymus chinensis (Trin.) Tzvel. plants under four soil moisture regimes (control: 75%–80% of field moisture capacity, mild drought: 60%–65%, and moderate drought: 50%–55% as well as severe drought: 35%–40%). Severe drought significantly decreased the key enzyme activities of nitrogen anabolism such as nitrate reductase (NR, EC 1.6.6.1), glutamine synthetase (GS, EC 6.3.1.2), and glutamate dehydrogenase (GDH, EC 1.4.1.2) but increased the key enzyme activities of nitrogen catabolism such as asparaginase (AS, EC 6.3.5.4) and endopeptidase (EP, EC 3.4.24.11), especially after long-term soil drought. Plant biomass, leaf-biomass ratio between the green leaf and total plant biomass, net photosynthetic rate, stomatal conductance, the maximal efficiency of PSII photochemistry, the actual quantum yield, and the photochemical quenching were significantly reduced by severe water stress. Plant malondialdehyde (MDA) concentration increased with the increase in water stress, particularly at the late-growth stage. Our results suggest that the key enzymes of nitrogen metabolism may play an important role in the photosynthetic acclimation of L. chinensis plants to long-term soil drought.

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References

  • Ainsworth EA, Davey PA, Hymus GJ, Osborne CP, Rogers A, et al. 2003. Is stimulation of leaf photosynthesis by elevated carbon dioxide concentration maintained in the long term? A test with Lolium perenne grown for 10 years at two nitrogen fertilization levels under Free Air CO2 Enrichment (FACE). Plant Cell Environ 26:705–714

    Article  CAS  Google Scholar 

  • Alves AAC, Setter TM. 2004. Abscisic acid accumulation and osmotic adjustment in cassava under water deficit. Environ Exp Bot 51:259–271

    Article  CAS  Google Scholar 

  • Alvim FA, Carolina SMB, Cascardo JCM, Nunnes CC, Martinez CA, et al. 2001. Enhanced accumulation of BiP in transgenic plant confers tolerance to water stress. Plant Physiol 126:1042–1054

    Article  PubMed  CAS  Google Scholar 

  • Baki GKA-E, Siefritz F, Man H-M, Weiner H, Kaldenhoff R, et al. 2000. Nitrate reductase in Zea mays L. under salinity. Plant Cell Environ 23:515–521

    Article  Google Scholar 

  • Bondada BR, Syvertsen J. 2005. Concurrent changes in net CO2 assimilation and chloroplast ultrastructure in nitrogen deficient citrus leaves. Environ Exp Bot 54:41–48

    Article  CAS  Google Scholar 

  • Bourgeais-Chaillou P, Perez-Alfocea F, Guerrier G. 1992. Compared effects of NO3, NH4 and NO3:NH4 sources on growth and physiological responses of soybean exposed to NaCl stress. J Exp Bot 43:1225–1233

    CAS  Google Scholar 

  • Bradford MM. 1976. A rapid sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Horst WJ. 1991. Effect of aluminum on lipid peroxidation, superoxidie dismutase, catalase and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS. 2003. Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Chen PY. 1983. Plant total carbon measurement. In the Agricultural Committee of Chinese Soil Association (ed.) Soil-agricultural Chemistry Analysis Methods. Beijing, China, Science Press, pp. 272–280

    Google Scholar 

  • Chen S, Bai Y, Zhang L, Han X. 2005. Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China. Environ Exp Bot 53:65–75

    Article  Google Scholar 

  • Chen Y-Q, Yi F, Cai M, Luo J-X. 2003. Effects of amino acids, nitrate, and ammonium on the growth and taxol production in cell cultures of Taxus yunnanensis. Plant Growth Regul 44:265–268

    Article  Google Scholar 

  • Cruz LJ, Cagampang GB, Juliano BO. 1970. Biochemical factors affecting protein accumulation in the rice grain. Plant Physiol 46:743–747

    PubMed  CAS  Google Scholar 

  • Delgado E, Mitchell RAC, Parry MAJ, Driscoll SP, Mitchell VJ, et al. 1994. Interacting effects of CO2 concentration, temperature and nitrogen supply on photosynthesis and composition of winter wheat leaves. Plant Cell Environ 17:1205–1213

    Article  Google Scholar 

  • Elliot WH. 1953. Isolation of glutamine synthetase and glutamotransferase from green peas. J Biol Chem 201:661–672

    Google Scholar 

  • Eriksen J, Nielsen M, Mortensen JV, Schjørring JK. 2001. Redistribution of sulphur during generative growth of barley plants with different sulphur and nitrogen status. Plant Soil 230:239–246

    Article  CAS  Google Scholar 

  • Evans JR. 1983. Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.). Plant Physiol 72:297–302

    PubMed  CAS  Google Scholar 

  • Foyer CH, Harbison J. 1994. Oxygen metabolism and the regulation of photosynthesic electron transport. In Foyer CH, Mullineaux P (ed.) Causes of Photooxidative Stresses and Amelioration of Defense Systems in Plants, Boca Raton, FL, USA, CRC Press, pp 1–42

    Google Scholar 

  • Foyer CH, Noctor G. 2002. Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359–388

    Article  Google Scholar 

  • Genty B, Briantais JM, Baker NR. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Hadži-Tašković Šukalivić V. 1986. Activity and distribution of nitrogen-metabolism enzymes in the developing maze kernel. Physiol Palnt 67:247–252

    Article  Google Scholar 

  • Heckathorn SA, Delucia EH. 1994. Drought-induced nitrogen retranslocation in perennial C4 grass of tallgrass prairie. Ecology 75:1877–1886

    Article  Google Scholar 

  • Heitholt JJ, Johnson RC, Ferris DM. 1991. Stomatal limitation to carbon dioxide assimilation in nitrogen and drought-stressed wheat. Crop Sci 31:135–139

    Article  CAS  Google Scholar 

  • Hernández JA, Almansa MS. 2002. Short-term effects of salt stress on antioxidant systems and leaf water relations of leaves. Physiol Plant 115:251–257

    Article  PubMed  Google Scholar 

  • Hsiao TC. 1973. Plant responses to water stress. Annu Rev Plant Physiol 24:519–570

    Article  CAS  Google Scholar 

  • Huang W, Chen Y. 1985. Glutamine synthetase and asparagine enzyme assay. In Shanghai members of association of plant physiology (ed.) Experimental Method Introduction to Plant Physiology. Shanghai, China, Shanghai Science and Technology Press, pp 223–227

    Google Scholar 

  • Kaiser WM. 1987. Effects of water deficit on photosynthetic capacity. Phsyiol Plant 71:142–149

    Article  CAS  Google Scholar 

  • Kichey T, Heumez E, Pocholle D, Pageau K, Vanacker H, et al. 2006. Combined agronomic and physiological aspects of nitrogen management in wheat highlight a central role for glutamine synthetase. New Phytol 169:265–278

    Article  PubMed  CAS  Google Scholar 

  • Kołodziejek I, Kozioł J, Wałęza M, Mostowska A. 2003. Ultrastructure of mesophyll cells and pigment content in senescing leaves of maize and barley. J Plant Growth Regul 22:217–227

    Article  CAS  Google Scholar 

  • Koprivova A, Suter M, den Camp RO, Brunold C, Kopriva S. 2000. Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiol 122:737–746

    Article  PubMed  CAS  Google Scholar 

  • Lam H-M, 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 Plant Mol Biol 47:569–593

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DW. 2002. Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and role of ATP. Ann Bot 89:871–885

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DW, Cornic G. 2002. Photosynthetic carbon and assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294

    Article  PubMed  CAS  Google Scholar 

  • Llorens L, Peñuelas J, Estiarte M. 2003. Ecophysiological responses of two Mediterranean shrubs, Erica multiflora and Globularia alypum, to experimentally drier and warmer conditions. Physiol Plant 119:231–243

    Article  CAS  Google Scholar 

  • Long SP, Zhu XG, Naidu SL, Ort DR. 2006. Can improvement in photosynthesis increase crop yield? Plant Cell Environ 29:315–330

    Article  CAS  PubMed  Google Scholar 

  • Loulakakis KA, Roubelakis-Angelakis KA. 1990. Intracellular localization and protein of NADH-glutamate dehydrogenase from Vitis vinifera L.: purification and characterization of the major leaf isoenzyme. J Exp Bot 41:1223–1230

    CAS  Google Scholar 

  • Lu C, Zhang J. 1999. Effects of water stress on photosystem II photochemistry and its thermostability in wheat plants. J Exp Bot 50:1139–1206

    Article  Google Scholar 

  • Lu C, Zhang J. 2000. Photosynthetic CO2 assimilation, chlorophyll fluorescence and photoinhibition as affected by nitrogen deficiency in maize plants. Plant Sci 151:135–143

    Article  PubMed  CAS  Google Scholar 

  • Mahan JR, Oliver MJ, Sherman TD. 1998. Nitrate reductase activity during desiccation and rehydration of the desiccation-tolerant moss Tortula ruralis. Environ Exp Bot 39:67–76

    Article  CAS  Google Scholar 

  • Makino A, Osmond B. 1991. Effects of nitrogen nutrition on pea and wheat. Plant Physiol 96:355–362

    PubMed  CAS  Google Scholar 

  • Marques da Silva J, Celeste AM. 2004. Photosynthesis in the water-stressed C4 grass Setaria sphacelata is mainly limited by stomata with both rapidly and slowly imposed water deficits. Physiol Plant 121:409–420

    Article  CAS  Google Scholar 

  • McDonald GK, Paulsen GM. 1997. High temperature effects on photosynthesis and water relations of grain legumes. Plant Soil 196:47–58

    Article  CAS  Google Scholar 

  • Moore S. 1968. Amino acid analysis: Aqueous dimethylsulfoxide as solvent for the ninhydrin reaction. J Bio Chem 243:6281–6283

    CAS  Google Scholar 

  • Munné-Bosch S, Alegre L. 2002. Plant aging increases oxidative stress in chloroplasts. Planta 214:608–615

    Article  PubMed  CAS  Google Scholar 

  • Niu SL, Jiang GM, Li YG, Gao LM, Liu MZ. 2003. Diurnal gas exchange and superior resources use efficiency of typical C4 species in Hunshandak Sandland, China. Photosynthetica 41:221–226

    Article  Google Scholar 

  • O’Connor TG, Haines LM, Snyman HA. 2001. Influence of precipitation and species composition on phytomass of a semi-arid African grassland. J Ecol 89:850–860

    Article  Google Scholar 

  • Parida AK, Das AB, Mohanty P. 2004. Investigations on the antioxidative defence responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regul 42:213–226

    Article  CAS  Google Scholar 

  • Peuke A, Rennenberg H. 2004. Carbon, nitrogen, phosphorus, and sulphur concentration and partitioning in beech ecotypes (Fagus sylvatica L.): phosphorus most affected by drought. Trees—Struct Funct 8:639–648

    Google Scholar 

  • Pommel B, Gallais A, Coque M, QuilleréI, Hirel B, et al. 2006. Carbon and nitrogen allocation and grain filling in three maize hybrids differing in leaf senescence. Eur J Agron 24:203–211

    Article  CAS  Google Scholar 

  • Price AH, Hendry GAF. 1991. Iron-catalysed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ 14:477–484

    Article  CAS  Google Scholar 

  • Ramachandra Reddy A, Chaitanya KV, Jutur PP, Sumithra K. 2004. Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environ Exp Bot 52:33–42

    Article  CAS  Google Scholar 

  • Raven JA, Handley LL, Andrews M. 2004. Global aspects of C/N interactions determining plant-environment interactions. J Exp Bot 55:11–25

    Article  PubMed  CAS  Google Scholar 

  • Roháček R. 2002. Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29

    Article  Google Scholar 

  • Saneoka H, Moghaieb REA, Premachandra GS, Fujita K. 2004. Nitrogen nutrition and water stress effects on cell membrane stability and leaf water relations in Agrostis palustris Huds. Environ Exp Bot 52:131–138

    Article  CAS  Google Scholar 

  • Sgherri CLM, Pinzino C, Navari-Izzo F. 1993. Chemical changes and O −12 production membranes under water stress. Physiol Plant 87:211–216

    Article  CAS  Google Scholar 

  • Sibout R, Guerrier G. 1998. Solute incompatibility with glutamine synthetase in water-stressed Populus nigra. Environ Exp Bot 40:173–178

    Article  CAS  Google Scholar 

  • Sicher RC, Bunce JA. 1997. Relationship of photosynthetic acclimation to changes of Rubisco activity in field-grown winter wheat and barley during growth in elevated carbon dioxide. Photosynth Res 52:27–38

    Article  CAS  Google Scholar 

  • Sinclair TR, Pinter PJ, Kimball BA, Adamsen FJ, LaMorte RL, et al. 2000. Leaf nitrogen concentration of wheat subjected to elevated [CO2] and either water or N deficits. Agr Ecosyst Environ 79:53–60

    Article  CAS  Google Scholar 

  • Singh B, Usha K. 2003. Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141

    Article  CAS  Google Scholar 

  • Sofo A, Dichio B, Xiloyannis C, Masia A. 2004. Lipoxygenase activity and proline accumulation in leaves and roots of olive trees in response to drought stress. Physiol Plant 121:58–65

    Article  PubMed  CAS  Google Scholar 

  • Solomonson LP, Barber MJ. 1990. Assimilatory nitrate reductase, functional properties and regulation. Annu Rev Plant Physiol Plant Mol Biol 41:225–253

    Article  CAS  Google Scholar 

  • Somers DA, Kuo TM, Kleinhofs A, Warner RL, Oaks A. 1983. Synthesis and degradation of barley nitrate reductase. Plant Physiol 72:949–952

    PubMed  CAS  Google Scholar 

  • Souza RP, Machado EC, Silva JAB, Lagôa AMMA, Silveir JAG. 2004. Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ Exp Bot 51:45–56

    Article  CAS  Google Scholar 

  • Srivali B, Renu KC. 1998. Drought-induced enhancement of protease activity during monocarpic senescence in wheat. Curr Sci 75:1174–1176

    Google Scholar 

  • Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible W-R, Krapp A. 2002. Steps towards an integrative view of nitrogen metabolism. J Exp Bot 53:959–970

    Article  PubMed  CAS  Google Scholar 

  • Sunarpi, Anderson JW. 1997. Effect of nitrogen nutrition on the export of sulphur from leaves in soybean. Plant Soil 188:177–187

    Google Scholar 

  • Suzuki A, Knaff DB. 2005. Glutamate synthase: structural, metchistic and regulatory properties, and role in the amino acid metabolis. Photosynth Res 83:191–217

    Article  PubMed  CAS  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T. 2004. Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Environ 27:1047–1054

    Article  CAS  Google Scholar 

  • Taylor NL, Day DA, Millar AH. 2004. Targets of stress-induced oxidative damage in plant mitochondria and their impact on cell carbon/nitrogen metabolism. J Exp Bot 55:1–10

    Article  PubMed  CAS  Google Scholar 

  • Utrillas MJ, Alegre L, Simon E. 1995. Seasonal changes in production and nutrient content of Cynodon dactylon (L.) Pers. subjected to water deficits. Plant Soil 175:153–157

    Article  CAS  Google Scholar 

  • Venekamp JH. 1989. Regulation of cytosol acidity in plants under conditions of drought. Physiol Plant 76:112–117

    Article  CAS  Google Scholar 

  • Walch-Liu P, Filleur S, Gan Y, Forde BG. 2005. Signaling mechanisms integrating root and shoot response to changes in the nitrogen supply. Photosynth Res 83:239–250

    Article  PubMed  CAS  Google Scholar 

  • Wang DL, Wang ZW, Zhang XJ. 1999. The comparison of photosynthetic physiological characteristics between the two divergent Leymus chinensis types. Acta Ecol Sin 19:837–843

    Google Scholar 

  • Wang RZ, Gao Q. 2003. Climate-driven changes in shoot density and shoot biomass in Leymus chinensis (Poaceae) on the North-east China Transect (NECT). Global Ecol Biogeogr 12:249–259

    Article  Google Scholar 

  • Wittenbach VA. 1979. Ribulose bisphosphate carboxylase and proteolytic activity in wheat leaves from anthesis through senescence. Plant Physiol 64:884–887

    Article  PubMed  CAS  Google Scholar 

  • Xu ZZ, Zhou GS. 2005a. Effects of water stress and nocturnal temperature on carbon allocation in the perennial grass, Leymus chinensis. Physiol Plant 123:272–280

    Article  CAS  Google Scholar 

  • Xu ZZ, Yu ZW, Wang D. 2006. Nitrogen translocation in wheat plants under soil water deficit. Plant Soil 280:291–303

    Article  CAS  Google Scholar 

  • Xu ZZ, Zhou GS. 2005b. Effects of water stress and high nocturnal temperature on photosynthesis and nitrogen level of a perennial grass Leymus chinensis. Plant Soil 269:131–139

    Article  CAS  Google Scholar 

  • Yang J, Zhang J, Wang Z, Xu G, Zhu Q. 2004. Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiol 1621–1629

  • Zhang JX, Kirham MB. 1994. Drought stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791

    CAS  Google Scholar 

  • Zhou G, Wang Y, Wang S. 2002. Responses of grassland ecosystems to precipitation and land use along the Northeast China Transect. J Veg Sci 13:361–368

    Article  Google Scholar 

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Acknowledgments

This study was financed by the National Natural Science Foundation of China (grant 30470338, 40231018) and the Key Project of Chinese Academy of Sciences (grant KSCX2-SW-133). We thank Bing-Rui Jia, Yan-Ling Jiang, Jian Song, Feng-Yu Wang, Yu-Hui Wang, Yun-Long Wang, and Wen-Ping Yuan for their assistance during the experiment. We also gratefully acknowledge the reviewers’ constructive comments.

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  1. Laboratory of Quantitative Vegetation Ecology, Institute of Botany, the Chinese Academy of Sciences, 20 Nanxincun, Xiangshan, Beijing, 100093, China

    Z. Z. Xu & G. S. Zhou

  2. Institute of Atmospheric Environment, China Meteorological Administration, Shenyang, 110016, China

    Z. Z. Xu & G. S. Zhou

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Xu, Z.Z., Zhou, G.S. Nitrogen Metabolism and Photosynthesis in Leymus chinensis in Response to Long-term Soil Drought. J Plant Growth Regul 25, 252–266 (2006). https://doi.org/10.1007/s00344-006-0043-4

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