Responses of photosynthetic characteristics and enzyme activity of nitrogen metabolism to low nitrogen in maize with different nitrogen tolerance
Keywords:
low-N, photosynthesis, nitrogen assimilation, nitrogen utilization efficiency, maizeAbstract
Understanding the physiological processes associated with leaf photosynthetic characteristics and nitrogen (N) assimilation during grain-filling stage are helpful for enhancing nitrogen utilization efficiency (NUtE) of maize. In this study, the leaf photosynthetic and N assimilation parameters in maize, including Zhengdan 958 (ZD958), a low-N tolerance cultivar and Huanong 138 (HN138), a low-N sensitive cultivar under different N rates were examined. Results showed that ZD958 displayed significant increases on grain yield and NUtE than that in HN138. Analyses on the leaf photosynthetic and N assimilation-associated processes indicated that ZD958 had higher leaf N remobilization (Rem N), net photosynthetic rate (Pn) and photosynthetic N use efficiency (PNUE) with respect to those of HN138 during grain-filling stage. In addition, ZD958 was also shown to be higher activities of leaf nitrate reductase (NR), glutamine synthetase (GS), nitrate reductase (GDH) and glutamine synthetase (GAGOT) than those of HN138. The leaf PNUE was significantly positively correlated with NR, GS, GDH, GOGAT suggesting that leaf PNUE and NR, GS, GDH, GOGAT jointly determined the N remobilization efficiency and the leaf N remobilization during post-silking. These results suggested that ZD958 possessed improved PNUE, NR and GS activities in leaves during grain-filling stage that contributes improve grain weights and yield formation capacities upon under low-N conditions. Keywords: low-N, photosynthesis, nitrogen assimilation, nitrogen utilization efficiency, maize DOI: 10.25165/j.ijabe.20201306.5891 Citation: Ji P T, Cui Y W, Li X L, Xiao K, Tao P J, Zhang Y C. Responses of photosynthetic characteristics and enzyme activity of nitrogen metabolism to low nitrogen in maize with different nitrogen tolerance. Int J Agric & Biol Eng, 2020; 13(6): 133–143.References
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[26] Xiong S P, Wu K Y, Wang X C, Zhang J, Du P, Wu Y X, et al. Analysis of root absorption characteristics and nitrogen utilization of wheat genotypes with different N efficiency. Scientia Agricultura Sinica, 2016; 49: 2267–2279.
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[29] Han J N, Wang L F, Zheng H Y, Pan X Y, L X, Chen F J, et al. ZD958 is a low-nitrogen-efficient maize cultivar at the seedling stage among five maize and two teosinte lines. Planta, 2015; 242(4): 1–16.
[30] Neal D O, Joy K W. Glutamine synthetase of pea leaves: Purification, stabilization and pH optima. Archives of biochemistry and biophysics, 1973; 159: 113–122.
[31] Lu D J, Yue S C, Lu F F, Cui Z L, Liu Z H, Zou C Q, et al. Integrated crop-N system management to establish high wheat yield population. Field Crops Research, 2016; 191: 66–74.
[32] Chen G P, Yang G H, Zhao M, Wang L C, Wang Y D, Xue J Q, et al. Studies on maize small area super-high yield trails and cultivation technique. Journal of Maize Science, 2008; 16: 1–4.
[33] Meng Q F, Sun Q P, Chen X P, Cui Z L, Yue S C, Zhang F S, et al. Alternative cropping systems for sustainable water and nitrogen use in the North China Plain. Agriculture Ecosystems and Environment, 2012; 146: 93–102.
[34] Gupta N, Gupta A K, Gaur V S. Relationship of nitrogen use efficiency with the activities of enzymes involved in nitrogen uptake and assimilation of finger millet genotypes grown under different nitrogen inputs. Scientific World Journal, 2012; 10: 625731.
[35] Chen K., Kumudini S, Tollenaar M, Vyn T. Plant biomass and nitrogen partitioning changes between silking and maturity in newer versus older maize cultivar. Field Crops Research, 2015; 183: 315–328.
[36] Ciampitti I A, Murrell S T, Camberato J J, Tuinstra M, Xia Y, Friedemann P, et al. Physiological dynamics of maize nitrogen uptake and partitioning in response to plant density and nitrogen stress factors: II. Reproductive phase. Crop Science, 2013; 53: 2588–2602.
[37] Mon J, Bronson K F, Hunsaker D J, Thorp K R, White J W, French A N. Interactive effects of nitrogen fertilization and irrigation on grain yield canopy temperature, and nitrogen use efficiency in overhead sprinkler-irrigated durum wheat. Field Crops Research, 2016; 1: 54–65.
[38] Ning P, Li S, Yu P, Zhang Y, Li C J. Post-silking accumulation and partitioning of dry matter, nitrogen, phosphorus and potassium in maize cultivars differing in leaf longevity. Field Crops Research, 2013; 144: 19–27.
[39] Valentinuz O R, Matthijs T. Vertical profile of leaf senescence during the grain-filling period in older and newer maize hybrids. Crop Science, 2004; 44, 827–834.
[40] Mu X H, Chen Q W, Chen F J, Yuan L X, Mi G H. Dynamic remobilization of leaf nitrogen components in relation to photosynthetic rate during grain filling in maize. Plant Physiology and biochemistry, 2018; 18: 27–34.
[41] Poorter H, Evans J R. Photosynthetic nitrogen use efficiency of species that differ inherently in specific leaf area. Oecologia, 1998; 116: 26–37.
[42] Sinclair T R, Horie T. Leaf nitrogen, photosynthesis, and crop radiation use efficiency: A review. Crop Science, 1989; 29: 90–98.
[43] Hikosaka K. Interspecific difference in the photosynthesis nitrogen relationship: Patterns, physiological causes, and ecological importance. Journal of Plant Research, 2014; 117: 481–494.
[44] Pan W L, Camberato J J, Moll R H, Kamprath E J, Jackson W A. Altering source-sink relationships in prolific maize cultivars: Consequences for nitogen uptake and remobilization. Crop Science, 1995; 35: 836–845.
[45] Su W, Kamran M, Xie J, Meng X, Han Q, Liu T, Han J. Shoot and root traits of summer maize hybrid varieties with higher grain yields and higher nitrogen use efficiency at low nitrogen application rates. Peer J. 2019; 7: e7294.
[46] Bernard S V M, Habash D Z. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Physiology, 2009; 182: 608–620.
[47] Wang X C, Wang X H, Xiong S P, Ma X M, Ding S J, Wu K Y, et al. Differences in nitrogen efficiency and nitrogen metabolism of wheat varieties under different nitrogen levels. Science Agricultural Sinience, 2015; 48: 2569–2579.
[48] Ye X S, Hong J, Shi L, Xu F S. Adaptability mechanism of nitrogen-efficient germplasm of natural variation to low nitrogen stress in Brassica napu. Journal of Plant Nutrition, 2010; 33: 2028–2040.
[49] Zhu X G, de Sturler E, Long S P. Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiology, 2007; 145: 513–526.
[50] Mu X H, Chen Q W, Chen F J, Yuan L X, Mi G H. Within-leaf nitrogen allocation in adaptation to low nitrogen supply in maize during grain-filling stage. Front Plant Science, 2016; 7: 699.
[51] Zhang M W, Dong Y M, Ma G, Wang C Y, Xie X D, Kang G Z. Responses of glutamine synthetase activity and gene expression to nitrogen levels in winter wheat cultivars with different grain protein content. Journal of Cereal Science, 2017; 74: 187–193.
[2] Emmanuel A A, Chai Q, Jeffrey A. Mechanisms of nitrogen use in maize. Agronomy, 2019; 9: 775
[3] Moll R H, Kamprath E J, Jackson W A. Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal, 1982; 74: 562–568.
[4] Kant S, Bi Y M, Rothstein S J. Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. Journal of Experimental Botany, 2011; 62: 1490–1509.
[5] Bingham I J, Karley A J, White P J, Thomas W T B, Russell J R. Analysis of improvements in nitrogen use efficiency associated with 75 years of spring barley breeding. European Journal of Agriculture, 2012; 42: 49–58.
[6] Wu Q P, Chen F J, Chen Y L, Yuan L X, Zhang F S, Mi G H. Root growth in response to nitrogen supply in Chinese maize cultivars released between 1973 and 2009. Science China Life Sciences, 2011; 54: 642–650.
[7] Wu Y S, Liu W G, Li X H, Li M S, Zhang D G, Hao Z F, et al. Low-nitrogen stress tolerance and nitrogen agronomic efficiency among maize inbreds: comparison of multiple indices and evaluation of genetic variation. Euphytica, 2011; 180: 281–290
[8] Chen Y L, Wu D L, Mu X H, Xiao C X. Vertical distribution of photosynthetic nitrogen use efficiency and its response to nitrogen in field-grown maize. Crop. Science, 2016; 56: 397–407.
[9] Martínez D E, Costa M L, Guiamet J J. Senescenceassociated degradation of chloroplast proteins inside and outside the organelle. Plant Biology, 2008; 10: 15–22.
[10] Ning P Li, S Yu P, Zhang Y Li, C J. Post-silking accumulation and partitioning of dry matter, nitrogen, phosphorus and potassium in maize varieties differing in leaf longevity. Field Crop Research, 2013; 144: 19–27.
[11] Yan P, Yue S, Qiu M, Chen X, Cui Z, Chen F. Using maize cultivars and in-season nitrogen management to improve grain yield and grain nitrogen concentrations. Field Crop Research, 2014; 166: 38–45
[12] Chang J F., Dong P F, Wang X L, Liu W L, Li C H. Effect of nitrogen application on carbon and nitrogen metabolism of different summer maize varieties. Science Agricultural Science, 2017; 50: 2282–2293.
[13] Valentinuz O R, Matthijs T. Vertical profile of leaf senescence during the grain-filling period in older and newer maize cultivars. Crop Science, 2004; 44: 827–834.
[14] Li Q, Ma X J, Chen Q B, Dou P, Yu DH, Luo Y Q, et al. Effects of nitrogen fertilizer on post-silking dry matter production and leaves function characteristics of low-nitrogen tolerance maize. Chinese Journal of Ecological-Agriculture, 2016; 24: 17–26.
[15] Wu Y W, Li Q. Effect of low-nitrogen stress on photosynthesis and chlorophyll fluorescence characteristics of maize cultivars with different low nitrogen tolerances. Journal of Integrative Agriculture, 2019; 18: 1246–1256
[16] Su W, Kamran M, Xie J, Meng X, Han Q, Liu T, Han J. Shoot and root traits of summer maize cultivar varieties with higher grain yields and higher nitrogen use efficiency at low nitrogen application rates. PeerJ, 2019; 7: e7294.
[17] Masclaux C, Quillere I, Gallais A, Hirel B. The challenge of remobilization in plant nitrogen economy. A survey of physioagronomic and molecular approaches. Annals of Applied Biology, 2001; 138: 68–81.
[18] Buchanan W V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, et al. The molecular analysis of leaf senescence-a genomics approach. Plant Biotechnology Journal, 2003; 1: 3–22
[19] Tercé-Laforgue T, Mack G, Hirel B. New insights towards the function of glutamate dehydrogenase revealed during source-sink transition of tobacco (Nicotiana tabacum L.) plants grown under different nitrogen regimes. Physiology Plant, 2004; 120: 220–228
[20] Gallais A, Hirel B. An approach of the genetics of nitrogen use efficiency in maize. Journa.l Exerimental Botony, 2004; 396: 295–306
[21] Hirel B, Martin A, Tercé-Laforgue T, Gonzalez-Moro M B, Estavillo J M. Physiology of maize I: a comprehensive and integrated view of nitrogen metabolism in a C4 plant. Physiology Plant, 2005; 124: 167–177.
[22] Masclaux D C, Reisdorf C M, Pageau K., Lelandais M, Grandjean O, Kronenberger J, et al. Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant. Physiology, 2006; 140: 444–456
[23] Hirel B, Bertin P, Quillere I, Bourdoncl W, Attagnant C, Dellay C, et al. Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiology, 2001; 125: 1258–1270.
[24] Liu P, Wu A L, Wang J S, Nan J K., Dong E W, Jiao X Y, et al. Nitrogen Use Efficiency and physiological responses of different sorghum genotypes influenced by nitrogen deficiency. Scientia Agricultura Sinica, 2018; 51: 3074–3083.
[25] Prester T, Groh S, Landbech M, Seitz G. Nitrogen uptake and utilization efficiency of European maize cultivars developed under conditions of low and high nitrogen input. Plant Breeding, 2010; 121: 480–486.
[26] Xiong S P, Wu K Y, Wang X C, Zhang J, Du P, Wu Y X, et al. Analysis of root absorption characteristics and nitrogen utilization of wheat genotypes with different N efficiency. Scientia Agricultura Sinica, 2016; 49: 2267–2279.
[27] Shah J M, Bukhari S A H, Zeng J B, Quan X Y, Ali E, Muhammad N, et al. Nitrogen (N) metabolism related enzyme activities, cell uitrastructure and nutrient contents as affected by N level and barley genotype. Journal of Integrative Agriculture, 2017; 1: 194–202.
[28] Li X L, Guo L G, Zhou B Y, Tang X M, Chen C C, Zhang L, et al. Characterization of low-N responses in maize (Zea mays L.) cultivars with contrasting nitrogen use efficiency in the North China Plain. Journal of Integrative Agriculture, 2019; 18(9): 2141–2152.
[29] Han J N, Wang L F, Zheng H Y, Pan X Y, L X, Chen F J, et al. ZD958 is a low-nitrogen-efficient maize cultivar at the seedling stage among five maize and two teosinte lines. Planta, 2015; 242(4): 1–16.
[30] Neal D O, Joy K W. Glutamine synthetase of pea leaves: Purification, stabilization and pH optima. Archives of biochemistry and biophysics, 1973; 159: 113–122.
[31] Lu D J, Yue S C, Lu F F, Cui Z L, Liu Z H, Zou C Q, et al. Integrated crop-N system management to establish high wheat yield population. Field Crops Research, 2016; 191: 66–74.
[32] Chen G P, Yang G H, Zhao M, Wang L C, Wang Y D, Xue J Q, et al. Studies on maize small area super-high yield trails and cultivation technique. Journal of Maize Science, 2008; 16: 1–4.
[33] Meng Q F, Sun Q P, Chen X P, Cui Z L, Yue S C, Zhang F S, et al. Alternative cropping systems for sustainable water and nitrogen use in the North China Plain. Agriculture Ecosystems and Environment, 2012; 146: 93–102.
[34] Gupta N, Gupta A K, Gaur V S. Relationship of nitrogen use efficiency with the activities of enzymes involved in nitrogen uptake and assimilation of finger millet genotypes grown under different nitrogen inputs. Scientific World Journal, 2012; 10: 625731.
[35] Chen K., Kumudini S, Tollenaar M, Vyn T. Plant biomass and nitrogen partitioning changes between silking and maturity in newer versus older maize cultivar. Field Crops Research, 2015; 183: 315–328.
[36] Ciampitti I A, Murrell S T, Camberato J J, Tuinstra M, Xia Y, Friedemann P, et al. Physiological dynamics of maize nitrogen uptake and partitioning in response to plant density and nitrogen stress factors: II. Reproductive phase. Crop Science, 2013; 53: 2588–2602.
[37] Mon J, Bronson K F, Hunsaker D J, Thorp K R, White J W, French A N. Interactive effects of nitrogen fertilization and irrigation on grain yield canopy temperature, and nitrogen use efficiency in overhead sprinkler-irrigated durum wheat. Field Crops Research, 2016; 1: 54–65.
[38] Ning P, Li S, Yu P, Zhang Y, Li C J. Post-silking accumulation and partitioning of dry matter, nitrogen, phosphorus and potassium in maize cultivars differing in leaf longevity. Field Crops Research, 2013; 144: 19–27.
[39] Valentinuz O R, Matthijs T. Vertical profile of leaf senescence during the grain-filling period in older and newer maize hybrids. Crop Science, 2004; 44, 827–834.
[40] Mu X H, Chen Q W, Chen F J, Yuan L X, Mi G H. Dynamic remobilization of leaf nitrogen components in relation to photosynthetic rate during grain filling in maize. Plant Physiology and biochemistry, 2018; 18: 27–34.
[41] Poorter H, Evans J R. Photosynthetic nitrogen use efficiency of species that differ inherently in specific leaf area. Oecologia, 1998; 116: 26–37.
[42] Sinclair T R, Horie T. Leaf nitrogen, photosynthesis, and crop radiation use efficiency: A review. Crop Science, 1989; 29: 90–98.
[43] Hikosaka K. Interspecific difference in the photosynthesis nitrogen relationship: Patterns, physiological causes, and ecological importance. Journal of Plant Research, 2014; 117: 481–494.
[44] Pan W L, Camberato J J, Moll R H, Kamprath E J, Jackson W A. Altering source-sink relationships in prolific maize cultivars: Consequences for nitogen uptake and remobilization. Crop Science, 1995; 35: 836–845.
[45] Su W, Kamran M, Xie J, Meng X, Han Q, Liu T, Han J. Shoot and root traits of summer maize hybrid varieties with higher grain yields and higher nitrogen use efficiency at low nitrogen application rates. Peer J. 2019; 7: e7294.
[46] Bernard S V M, Habash D Z. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Physiology, 2009; 182: 608–620.
[47] Wang X C, Wang X H, Xiong S P, Ma X M, Ding S J, Wu K Y, et al. Differences in nitrogen efficiency and nitrogen metabolism of wheat varieties under different nitrogen levels. Science Agricultural Sinience, 2015; 48: 2569–2579.
[48] Ye X S, Hong J, Shi L, Xu F S. Adaptability mechanism of nitrogen-efficient germplasm of natural variation to low nitrogen stress in Brassica napu. Journal of Plant Nutrition, 2010; 33: 2028–2040.
[49] Zhu X G, de Sturler E, Long S P. Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiology, 2007; 145: 513–526.
[50] Mu X H, Chen Q W, Chen F J, Yuan L X, Mi G H. Within-leaf nitrogen allocation in adaptation to low nitrogen supply in maize during grain-filling stage. Front Plant Science, 2016; 7: 699.
[51] Zhang M W, Dong Y M, Ma G, Wang C Y, Xie X D, Kang G Z. Responses of glutamine synthetase activity and gene expression to nitrogen levels in winter wheat cultivars with different grain protein content. Journal of Cereal Science, 2017; 74: 187–193.
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2020-12-03
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Ji, P., Cui, Y., Li, X., Xiao, K., Tao, P., & Zhang, Y. (2020). Responses of photosynthetic characteristics and enzyme activity of nitrogen metabolism to low nitrogen in maize with different nitrogen tolerance. International Journal of Agricultural and Biological Engineering, 13(6), 133–143. Retrieved from https://ijabe.migration.pkpps03.publicknowledgeproject.org/index.php/ijabe/article/view/5891
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