Xu Hua DU, Fang Ren PENG, Jiang JIANG, Peng Peng TAN, Zhi Zhuang WU, You Wang LIANG, Zhe Ke ZHONG

Inorganic nitrogen fertilizers induce changes in ammonium assimilation and gas exchange in Camellia sinensis L.

Camellia sinensis L. is one of the most economically important crops in the world today. The leaves of this plant are harvested for tea production on a massive scale through a process that requires a large amount of inorganic nitrogen (N). However, knowledge of how inorganic nitrogen regulates the growth physiology of C. sinensis L. remains limited. In order to investigate its effects on gas exchange, N assimilation, and the efficiency of N use in C. sinensis L., we carried out experiments with 4 cultivars (WNZ, YS, ZN139, and LJ43) under 4 different treatments: 1) a control treatment, 2) a treatment fed only with NO3--N, 3) a treatment fed only with NH4+-N, and 4) a treatment fed with a mixture of NO3--N and NH4+-N in a 1:1 ratio. We found that the application of N, especially in a mixture, encouraged higher foliar N content per unit area (Nf), which in turn promoted glutamine synthetase (GS) activity and glutamate synthase (GOGAT) activity. Our mixture-fed treatment increased Nf, GS, and GOGAT activity by 26.18%, 110.2%, and 92.21%, respectively, for the WNZ cultivar. The mixed-fed treatment also had the highest net photosynthetic (Pn), stomatal conductance (Gs), and transpiration (Tr) rates, while the NH4+-fed treatment had the highest intercellular CO2 content (Ci). The mixture-fed and NO3--fed applications caused significant increases in photosynthetic N-use efficiency (PNUE), but the NH4+-fed application decreased PNUE and water-use efficiency (WUE). Furthermore, we observed that differences among cultivars for some of these parameters were significant due to different N solutions. We found that the YS and LJ43 cultivars showed no significant response to different N applications (excluding control) in key enzyme activity and Pn, respectively, but this was not the case for most of the other parameters. Our study indicates that the mixture-fed application promotes increased foliar N content and ammonium assimilation, which in turn increases photosynthesis rates, suggesting that the mixed-feeding of plants provides optimal conditions to promote the growth of C. sinensis L. for tea cultivation.

Anahtar Kelimeler:

Camellia sinensis L., glutamine synthetase/glutamate synthase activity, inorganic nitrogen forms, photosynthesis, photosynthetic N-use efficiency, water-use efficiency

Inorganic nitrogen fertilizers induce changes in ammonium assimilation and gas exchange in Camellia sinensis L.

Keywords:

Camellia sinensis L., glutamine synthetase/glutamate synthase activity, inorganic nitrogen forms, photosynthesis, photosynthetic N-use efficiency, water-use efficiency,

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Alpha JM, Chen JH, Zhang GP (2009). Effect of nitrogen fertilizer forms on growth, photosynthesis, and yield of rice under cadmium stress. J Plant Nutr 32: 306–317.
Bernard SM, Habash DZ (2009). The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182: 608–620.
Britto D, Kronzucker H (2002). NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159: 567–584.
Brueck H (2008). Effects of nitrogen supply on water-use efficiency of higher plants. J Plant Nutr Soil Sci 171: 210–219.
Bybordi A (2012). Effect of different ratios of nitrate and ammonium on photosynthesis and fatty acid composition of canola under saline conditions. Inter J Agri Crop Sci 4: 622–626.
Cabrera C, Artacho R, Gimenez R (2006). Beneficial effects of green tea: a review. J Am Coll Nutr 25: 79–99.
Cao CL, Li SX. (2003). Effects of N form on some physiological characteristics and yield of wheat during the vegetative and reproductive growth stage. Acta Agron Sin 29: 258–262 (in Chinese with abstract in English).
Champigny ML, Foyer C (1992). Nitrate activation of cytosolic protein kinases diverts photosynthetic carbon from sucrose to amino acid biosynthesis. Plant Physiol 100: 7–12.
Chen YL, Liu MH, Li XL (2005). Effects of different nitrogen forms and ratios on the photosynthetic characteristics of Pinus koraiensis seedlings. J Nanjing For Univ (Nat Sci Edition) 29: 77–80 (in Chinese with abstract in English).
Chen ZM (2011). Research on Sustainable Development Strategy of China’s Tea Industry. Hangzhou, Zhe Jiang, China: Zhejiang University Press.
Claussen W, Lenz F (1999). Effect of ammonium or nitrate nutrition on net photosynthesis, growth, and activity of the enzymes nitrate reductase and glutamine synthetase in blueberry, raspberry, and strawberry. Plant Soil 208: 95–102.
Cramer MD, Lewis OAM (1993). The influence of nitrate and ammonium nutrition on the growth of wheat (Triticum aestivum ) and maize (Zea mays) plants. Ann Bot 72: 359–365.
Cren M, Hirel B (1999). Glutamine synthetase in higher plant: regulation of gene and protein expression from the organ to the cell. Plant Cell Physiol 40: 1187–1193.
Domenicano S, Coll L, Messier C, Berninger F (2011). Nitrogen forms affect root structure and water uptake in the hybrid poplar. New Forests 42: 347–362.
Dong YY, Dong CX, Lu YL, Miao C, Shen QR (2006). Influence of partial replacement of NO3−-N with NH4+-N in nutrient solution on enzyme activity in nitrogen assimilation of tomato at different growing stages. Acta Pedol Sin 43: 261–266 (in Chinese with abstract in English).
Du XH, Peng FR (2010). Effect of inorganic nitrogen forms on growth and kinetics of ammonium and nitrate uptake in Camellia sinensis L. Acta Agron Sin 36: 327–334 (in Chinese with abstract in English).
Du XH, Zhou XJ, Peng FR (2008). Determination and analysis of ammonium assimilation enzyme activities in different organs of tea plants. Nonwood For Res 26: 23–28 (in Chinese with abstract in English).
Duan YH, Zhang YL, Wang SW, Shen QR (2007). Enhancement effect by nitrate on rice plant during the whole growth period and its physiological mechanisms. Acta Ecol Sin 27: 1086–1092 (in Chinese with abstract in English).
Duan Y L, Li H S, Wu S H, Yang Z M (2003). Effects of blue-light and calcium on the activities of glutamate synthetase and enzymes belonging to calcium signal systems in seedlings of wheat. Journal of Fujian Agriculture and Forestry University (Natural Science Edition) 32: 209–212.
Evans JR (1989). Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9–19.
Evans JR, Terashima I (1988). Photosynthetic characteristics of spinach leaves grown with different nitrogen treatments. Plant Cell Physiol 29: 157–165.
Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008). Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Envir 31: 602–621.
Gaur VS, Singh US, Gupta AK, Kumar A (2012). Influence of different nitrogen inputs on the members of ammonium transporter and glutamine synthetase genes in two rice genotypes having differential responsiveness to nitrogen. Mol Biol Rep 39: 8035– 8044.
Gerendás J, Zhu ZJ, Bendixen R, Ratcliffe R G, Sattelmacher B (1997). Physiological and biochemical processes related to ammonium toxicity in higher plants. Pflanz Bodenkunde 160: 239-251.
Gorny AG, Garczynski S (2002). Genotypic and nutrition-dependent variation in water use efficiency and photosynthetic activity of leaves in winter wheat (Triticum aestivum L.). J Appl Genet 43: 145–160.
Guo HX, Liu WQ, Shi YC (2006). Effects of different nitrogen forms on photosynthetic rate and the chlorophyll fluorescence induction kinetics of flue-cured tobacco. Photosynthetica 44: 140–142.
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding K, Vitousek PM, Zhang FS (2010). Significant acidification in major Chinese croplands. Science 327: 1008– 1009.
Guo S, Brück H, Sattelmacher B (2002). Effects of supplied nitrogen form on growth and water uptake of French bean (Phaseolus vulgaris L.) plants. Plant Soil 239: 267–275.
Guo S, Zhou Y, Shen Q, Zhang F (2007). Effect of ammonium and nitrate nutrition on some physiological processes in higher plants-growth, photosynthesis, photorespiration, and water Relations. Plant Bio 9: 21–29.
Habash DZ, Bernard S, Schondelmaier J, Weyen J, Quarrie SA (2007). A genetic study of nitrogen use in hexaploid wheat in relation to N utilization, development, and yield. Theor Appl Genet 114: 403–419.
Han QM, Chiba Y (2009). Leaf photosynthetic responses and related nitrogen changes associated with crown reclosure after thinning in a young Chamaecyparis obtusa stand. J For Res 14: 349–357.
Han WY, Ma LF, Shi YZ, Ruan JY (2007). Effects of a controlled- release nitrogen fertilizer on tea yield and quality and rational application technology. Plant Nutr Ferti Sci 13: 1148–1155.
Hirose S, Hayakawa T, Yamaya T (1997). Inducible accumulation of mRNA for NADH-dependent glutamate synthase in roots in response to ammonium ions. Plant Cell Physiol 38: 1295–1297.
Hikosaka K, Terashima I, Katoh S (1994). Effects of leaf age, nitrogen nutrition and photon flus density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia 97: 451-457.
Jampeetong A, Brix H (2009). Effects of NaCl salinity on growth, morphology, photosynthesis and proline accumulation of Salvinia natans. Aquat Bot 91: 181-186.
Kronzucker HJ, Glass ADM, Siddiqi MY (1999). Inhibition of nitrate uptake by ammonium in barley-analysis of component fluxes. Plant Physiol 120: 283–291.
Lam HM, Coschigano KT, Oliveira IC, Coruzzi GM (1996). The molecular genetics of nitrogen assimilation into amino acids in higher plants. Ann Rev Physiol Plant Mol Biol 47: 569–593.
Lea PJ, Miflin BJ (1974). Alternative route for nitrogen in higher plants. Nature 251: 614–616.
Li CF, Ma FM, Zhao Y, Li WH (2003). Effects of nitrogen forms on key enzyme activities and related products in sugar and nitrogen metabolism of sugar beet (Beta vulgaris L.). Acta Agron Sin 29: 128–132 (in Chinese with abstract in English).
Li X, Yan XF, Liu JF (2006). Effects of nitrogen forms on nitrogen metabolism-related enzymes and growth of Phellodendron amurense seedlings. Chinese Bull Bot 23: 255–261 (in Chinese with abstract in English).
Li XJ, Wen JL, Han SC, Cao CL, Li SX (2008). Effect of N form on physiological mechanism and biomass in corn seedlings. J Northwest Agr & For Univ (Nat Sci Edition) 36: 192–196 (in Chinese with abstract in English).
Li ZS, Zhang CF, Lin QH (1999). Effect of exogenous ammonium on glutamine synthetase, glutamate synthase, and glutamate dehydrogenase in the root of rice seedling. Wuhan Univ J Nat Sci 4: 358–362 (in Chinese with abstract in English).
Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL, Cui ZL, Vitousek PM, Erisman JW, Goulding K, Christie P et al. (2013a). Enhanced nitrogen deposition over China. Nature 494: 459–462.
Liu XP, Fan YY, Long JX, Wei RF, Kjelgren R, Gong CM, Zhao J (2013b). Effects of soil water and nitrogen availability on photosynthesis and water use efficiency of Robinia pseudoacacia seedlings. J Envir Sci 25: 585–595.
Liu YH, Zhu ZJ, Wei GQ (2004). Effects of nitrogen form on the activity of glutamine synthetase and photorespiratory rate in tomato under different light intensities. Plant Physiol Comm 40: 680–682 (in Chinese with abstract in English).
Lopes MS, Araus JL (2006). Nitrogen source and water regime effects on durum wheat photosynthesis and stable carbon and nitrogen isotope compositions. Physiol Plantarum 126: 435– 445.
Miflin BJ, Habash DZ (2002). The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J Exp Bot 53: 979–987.
Mitchell AK, Hinckley TM (1993). Effects of foliar nitrogen concentration on photosynthesis and water use efficiency in Douglas-fir. Tree Physiol 12: 403–410.
Mondal TK, Bhattacharya A, Laxmikumaran M, Ahuja PS (2004). Recent advances of tea (Camellia sinensis) biotechnology. Plant Cell Tiss Org 76: 195–254.
Niinemets U (1997). Components of leaf dry mass per area-thickness and density-alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol 144: 35–47.
Noctor G, Foyer, CH (1998). A re-evaluation of the ATP: NADPH budget during C3 photosynthesis: a contribution from nitrate assimilation and its associated respiratory activity? J Exp Bot 49: 1895–1908.
Novitskaya L, Trevanion SJ, Driscoll S, Foyer CH, Noctor G (2002). How does photorespiration modulate leaf amino acid contents? A dual approach through modelling and metabolite analysis. Plant Cell Envir 25: 821–835.
Oliveira CI, Brears T, Knight TJ, Clark A, Coruzzi GM (2002). Overexpression of cytosolic glutamine synthetase relation to nitrogen, light, and photorespiration. Plant Physiol 129: 1170– 1180.
Poorter H, Evans JR (1998). Photosynthetic nitrogen use efficiency of species that differ inherently in specific area. Oecologia 116: 26–37.
Ripullone F, Grassi G, Lauteri M, Borghetti M (2003). Photosynthesis– nitrogen relationships: interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiol 23: 137–144.
Stitt M, Krapp A (1999). The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Envir 22: 583–621.
Suzuki A, Knaff DB (2005). Glutamate synthase: structural, mechanistic, and regulatory properties, and role in the amino acid metabolism. Photosynth Res 83: 191–217.
Tabatabaei SJ, FatemiLS, Fallahi E (2006). Effect of ammonium: nitrate ratio on yield, calcium concentration, and photosynthesis rate in strawberry. J Plant Nutr 29: 1273–1285.
Takashima T, Hikosake K, Hirose T (2004). Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant Cell Envir 27: 1047–1054.
Wang XC, Yang YJ, Chen L, Ruan JY (2005). Preliminary study on physiological and biochemical indices related to nitrogen use efficiency in tea plant [Camellia sinensis (L.) O. Kuntze]. Acta Agron Sin 31: 926–931 (in Chinese with abstract in English).
Watanabe I (1995). Effect of nitrogen fertilizer application at different stages on the quality of green tea. Soil Sci Plant Nutr 41: 763–768.
Xiao K, Zhang SH, Zou DH, Zhang RX (2000). The effects of different nitrogen nutrition forms on photosynthetic characteristics in wheat leaves. Acta Agron Sin 26: 53–58 (in Chinese with abstract in English).
Yamaya T, Tanno H, Hirose N, Watanabe S, Hayakawa T (1995). A supply of nitrogen causes increase in the level of NADH- dependent glutamate synthase protein and in the activity of the enzyme in roots of rice seedlings. Plant Cell Physiol 36: 1197–1204.
Zhou YH, Zhang YL, Wang XM, Cui JX, Xia XJ, Shi K, Yu JQ (2011). Effects of nitrogen form on growth, CO2 assimilation, chlorophyll fluorescence, and photosynthetic electron allocation in cucumber and rice plants. J Zhejiang Univ Sci B (Biomed & Bio) 12: 126–134.