High Temperature at Grain-filling Stage Affects Nitrogen Metabolism Enzyme Activities in Grains and Grain Nutritional Quality in Rice

Abstract

Abstract: Rice plants would more frequently suffer from high temperature (HT) stress at the grain-filling stage in future. A japonica rice variety Koshihikari and an indica rice variety IR72 were used to study the effect of high temperature on dynamic changes of glutamine synthetase (GS) activity, glutamate synthase (GOGAT) activity, glutamic oxalo-acetic transminase (GOT) activity, glutamate pyruvate transminase (GPT) activity in grains and grain nutritional quality at the grain-filling stage. Under HT, the activities of GOGAT, GOT, GPT and soluble protein content in grains significantly increased, whereas GS activity significantly decreased at the grain-filling stage. In addition to the increase of protein and amino acids contents, it was suggested that GOGAT, GOT and GPT in grains played important roles in nitrogen metabolism at the grain-filling stage. Since the decrease of GS activity in grains did not influence the accumulations of amino acids and protein, it is implied that GS might not be the key enzyme in regulating glutamine content in grains.

Key words: high temperature, nitrogen metabolism enzyme, protein, amino acid, rice

LIANG Cheng-gang, CHEN Li-ping, WANG Yan, LIU Jia, XU Guang-li, LI Tian. High Temperature at Grain-filling Stage Affects Nitrogen Metabolism Enzyme Activities in Grains and Grain Nutritional Quality in Rice[J]. RICE SCIENCE, 2011, 18(3): 210-216.

References

Cai Y X, Wang W, Zhu Q S. 2007. Effects of water stress on nutrient quality and accumulation of protein in rice grains. J Plant Ecol, 31(3): 536–543. (in Chinese with English abstract)
Cheng F M, Liu Z H, Zhang S W. 2002. The evaluation of climatic-ecology condition for the rice quality formation and its distribution laws in China. Acta Ecol Sin, 22(5): 636–642. (in Chinese with English abstract)
Cheng H S, Wu P L, Gao Q S. 1986. Research on rice protein and amino acid content. Seed, (4): 6–10. (in Chinese)
Dalling M J, Boland G, Wilson J H. 1976. Relation between acid proteinase activity and redistribution of nitrogen during grain development in wheat. Aust J Plant Physiol, 3(6): 721–730.
Ebeid M, Eder J, Kutacek M, Piovarci A. 1981. Transaminase GOT and GPT activity in extirped sprouts of normal and opaque-2 maize (Zea mays L.) seedlings. Biol Plant, 23(5): 345–350.
Galili G. 2011. The aspartate-family pathway of plants: Linking production of essential amino acids with energy and stress regulation. Plant Signal Behav, 6(2): 192–195.
Glevarec G, Bouton S, Jaspard E, Riou M T, Cliquet J B, Suzuki A, Limami A M. 2004. Respective roles of the glutamine synthetase/ glutamate synthase cycle and glutamate dehydrogenase in ammonium and amino acid metabolism during germination and post-germinative growth in the model legume Medicago truncatula. Planta, 219(2): 286–297.
Hirel B, Bertin P, Quillere I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A. 2001. Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol, 125(3): 1258–1270.
Jagadish S V K, Craufurd P Q, Wheeler T R. 2007. High temperature stress and spikelet fertility in rice (Oryza sativa L.). J Exp Bot, 58(7): 1627–1635.
Jiao A X, Yang C L, Cao G L, Lee J H, Guo J C, Kim J H, Kim H Y, Lee K S, Ham L Z. 2008. Progress in genetic research on protein content of rice. Sci Agric Sin, 41(1): 1–8. (in Chinese with English abstract)
Jin Z X, Qian C R, Yang J, Liu H T. 2007. Changes in activity of glutamine synthetase during grain filling and their relation to rice quality. Rice Sci, 14(3): 211–216.
Kharin V V, Zwiers F W, Zhang X B, Hegerl G C. 2007. Changes in temperature and precipitation extremes in the IPCC ensemble of global coupled model simulations. J Climate, 20: 1419–1443.
Lea P J, Black well R D, Joy K W. 1992. Ammonia assimilation in higher plants. In: Mengel K, Pilbeam D J. Nitrogen Metabolism of Plants. Oxford: Clarendon Press; New York: Oxford University Press: 153–186.
Lea P J, Miflin B J. 1974. Alternative route for nitrogen in higher plants. Nature, 251(10): 614–616.
Li P P, Cheng G F, Zhang J H, Li B B, Xie X J, Yang S B. 2010. Effects of high temperature stress on physiological characteristics of rice during heading and flowering period. J Jiangsu Univ: Nat Sci, 31(2): 125–130. (in Chinese with English abstract)
Lin M F. 1994. Relationship of meteorological conditions with rice quality in the cultivars of jinzao series. J Fujian Agric Univ: Nat Sci, 23(3): 368–371. (in Chinese with English abstract)
Lu B B, Zhou W, Zhang J, Pan L, Lin Q H, Zhang C F. 2002. Effect of temperature on expression of glutamine synthetase and NADH-glutamate synthease in rice plants. J Wuhan Univ: Nat Sci, 48(2): 239–242. (in Chinese with English abstract)
Martin A, Lee J, Kichey T, Gerentes D, Ziy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, Terce-Laforgue T, Quillere I, Coque M, Gallais A, Gonzalez-Moro M B, Bethencourt L, Habash D Z, Lea P J, Edwards K J, Hirel B. 2006. Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell, 18(11): 3252– 3274.
Miflin B J, Habash D Z. 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(370): 979–987.
Neuhoff V, Stamm R, Eibl H. 1985. Clear background and highly sensitive protein staining with Coomassie Blue dyes in polyacrylamide gels: A systematic analysis. Electrophoresis, 6(9): 427–428.
Peng S B, Huang J L, Sheehy J E, Laza R C, Visperas R M, Zhong X, Centeno G S, Khush G S, Cassman K G. 2004. Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA, 101: 9971–9975.
Resurreccion A P, Hara T, Juliano B O, Yoshida S. 1977. Effect of temperature during ripening on grain quality of rice. Soil Sci Plant Nutr, 23(1): 109–112.
Tang X R, Guan C Y, Yu T Q. 1999. Studies on matter metabolism of yield and quality of different genotypic rice. J Hunan Agric Univ, 25(4): 278–282. (in Chinese with English abstract)
Teng Z H, Zhi L, Zong X F, Wang S G, He G H. 2008. Effects of high temperature on chlorophyll fluorescence, active oxygen resistance activity, and grain quality in grain-filling periods in rice plants. Acta Agron Sin, 34(9): 1662–1666. (in Chinese with English abstract)
Ufaz S, Galili G. 2008. Improving the content of essential amino acids in crop plants: Goals and opportunities. Plant Physiol, 147: 954–961.
Wang X C, Xiong S P, Ma X M, Zhang J J, Wang Z Q. 2005. Effects of different nitrogen forms on key enzyme activity involved in nitrogen metabolism and grain protein content in speciality wheat cultivars. Acta Ecol Sin, 25(4): 802–807. (in Chinese with English abstract)
Wu L H, Jiang S H, Tao Q N. 1998. The colorimetric measurement method and application of plant transaminase (GOT and GPT) activity. Chin J Soil Sci, 29(3): 136–138. (in Chinese)
Yamaya T, Hayakawa T, Tanasawa K, Kamachi K, Mae T, Ojinma K. 1992. Tissue distribution of glutamate synthase and glutamine synthetase in rice leaves: Occurrence of NADH-dependent glutamate synthase protein and activity in the unexpanded, nongreen leaf blades. Plant Physiol, 100(3): 1427–1432.
Zhang L, Wu D Y, Zhu B Y, Zhang M G, Li J Q. 2002. Effects of temperature and light on the dynamic change in soluble protein and sugar in rice leaves and grains during the milk-filling stage. J South China Norm Univ: Nat Sci, 5(2): 98–101. (in Chinese with English abstract)
Zhao Q Z, Chen J R, Liu H, Qiao J F, Gao T M, Yang H X, Wang J H. 2008. Relationship between activities of nitrogen assimilation enzymes and leaf color of rice. Sci Agric Sin, 41(9): 2607–2616. (in Chinese with English abstract)
Zhen H, Huang C L, Chen Y, Li M L, Liu X Z, Pan D J, Zhang H Q. 1997. Study on the protein content of wild rice resource. J South China Agric Univ, 18(4): 16–20. (in Chinese with English abstract)
Zhu D Q, Zhu X L, Wang Y, Qi B Z. 1991. Several physiological parameters in relation to grain protein content in winter wheat (Triticum aestivum). Acta Agron Sin, 17(2): 135–144. (in Chinese with English abstract)
Zhu X M, Rong X M, Liu Q. 2001. Differences in contents of grain protein of different genotype rice varieties: I. Differences in contents of grain protein between two varieties of early convention rice. J Hunan Agric Univ: Nat Sci, 27(1): 13–16. (in Chinese with English abstract)
Zou J, Liu A L, Chen X B, Zhou X Y, Gao G F, Wang W F, Zhang X W. 2009. Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol, 166(8): 851–861.

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