Please wait a minute...
Journal of Integrative Agriculture  2015, Vol. 14 Issue (7): 1295-1308    DOI: 10.1016/S2095-3119(14)60957-6
Physiology·Biochemistry·Cultivation·Tillage Advanced Online Publication | Current Issue | Archive | Adv Search |
Growth traits and nitrogen assimilation-associated physiological parameters of wheat (Triticum aestivum L.) under low and high N conditions
 ZHANG Fei-fei, GAO Si, ZHAO Yuan-yuan, ZHAO Xiao-lei, LIU Xiao-man, XIAO Kai
College of Agronomy, Agricultural University of Hebei, Baoding 071001, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  In this study, 14 wheat cultivars with contrasting yield and N use efficiency (NUE) were used to investigate the agronomic and NUE-related traits, and the N assimilation-associated enzyme activities under low and high N conditions. Under deficient-N, the cultivars with high N uptake efficiency (UpE) and high N utilization efficiency (UtE) exhibited higher plant biomass, yields, and N contents than those with medium and low NUEs. The high UpE cultivars accumulated more N than other NUE type cultivars. Under sufficient-N, the tested cultivars showed similar patterns in biomass, yield, and N content to those under deficient-N, but the varietal variations in above traits were smaller. In addition, the high UpE cultivars displayed much more of root biomass and larger of root length, surface area, and volume than other NUE type cultivars, indicating that the root morphological traits under N deprivation are closely associated with the plant biomass through its improvement of the N acquisition. The high UtE cultivars showed higher activities of nitrate reductase (NR), nitrite reductase (NIR), and glutamine synthetase (GS) at stages of seediling, heading and filling than other NUE type cultivars under both low and high N conditions. Moreover, the high UpE and UtE cultivars also displayed higher photosynthetic rate under deficient-N than the medium and low NUE cultivars. Together, our results indicated that the tested wheat cultivars possess dramatically genetic variations in biomass, yield, and NUE. The root morphological traits and the N assimilation enzymatic acitivities play critical roles in regulating N accumulation and internal N translocation under the N-starvation stress, respectively. They can be used as morphological and biochemical references for evaluation of UpE and UtE in wheat.

Abstract  In this study, 14 wheat cultivars with contrasting yield and N use efficiency (NUE) were used to investigate the agronomic and NUE-related traits, and the N assimilation-associated enzyme activities under low and high N conditions. Under deficient-N, the cultivars with high N uptake efficiency (UpE) and high N utilization efficiency (UtE) exhibited higher plant biomass, yields, and N contents than those with medium and low NUEs. The high UpE cultivars accumulated more N than other NUE type cultivars. Under sufficient-N, the tested cultivars showed similar patterns in biomass, yield, and N content to those under deficient-N, but the varietal variations in above traits were smaller. In addition, the high UpE cultivars displayed much more of root biomass and larger of root length, surface area, and volume than other NUE type cultivars, indicating that the root morphological traits under N deprivation are closely associated with the plant biomass through its improvement of the N acquisition. The high UtE cultivars showed higher activities of nitrate reductase (NR), nitrite reductase (NIR), and glutamine synthetase (GS) at stages of seediling, heading and filling than other NUE type cultivars under both low and high N conditions. Moreover, the high UpE and UtE cultivars also displayed higher photosynthetic rate under deficient-N than the medium and low NUE cultivars. Together, our results indicated that the tested wheat cultivars possess dramatically genetic variations in biomass, yield, and NUE. The root morphological traits and the N assimilation enzymatic acitivities play critical roles in regulating N accumulation and internal N translocation under the N-starvation stress, respectively. They can be used as morphological and biochemical references for evaluation of UpE and UtE in wheat.
Keywords:  wheat (Triticum aestivum L.)       low and high N       biomass       yield       nitrogen use efficiency       root morphological traits       N assimilzation-associated enzyme       photosynthetic rate  
Received: 22 August 2014   Accepted:
Fund: 

This work was supported by the Chinese National Programs of Science and Technology for High Yielding Crop Production (2011BAD16B08, 2012BAD04B06, and 2013BAD07B05) and the Key Laboratory of Crop Growth Regulation of Hebei Province, China.

Corresponding Authors:  XIAO Kai, Tel: +86-312-7520153, Fax: +86-312-7528400, E-mail: xiaokai@hebau.edu.cn   
About author:  These authors contributed equally to this study.

Cite this article: 

ZHANG Fei-fei, GAO Si, ZHAO Yuan-yuan, ZHAO Xiao-lei, LIU Xiao-man, XIAO Kai. 2015. Growth traits and nitrogen assimilation-associated physiological parameters of wheat (Triticum aestivum L.) under low and high N conditions. Journal of Integrative Agriculture, 14(7): 1295-1308.

Barraclough P B, Howarth J R, Jones J, Lopez-Bellido R,Parmar S, Shepherd C E, Hawkesford M J. 2010. Nitrogenefficiency of wheat: Genotypic and environmental variationand prospects for improvement. European Journal of Agronomy, 33, 1-11

Barraclough P B, Lopez-Bellido R, Hawkesford M 2014.Genotypic variation in the uptake, partitioning andremobilisation of nitrogen during grain-filling in wheat. FieldCrops Research, 156, 242-248

Beman J M, Arrigo K, Matson P M 2005. Agricultural runofffuels large phytoplankton blooms in vulnerable areas of theocean. Nature, 434, 211-214

Borrell A K, Garside A L, Fukai S, Reid D J. 1998. Season,nitrogen rate, and plant type affect nitrogen uptake andnitrogen use efficiency in rice. Australian Journal ofAgriculture Research, 49, 829-843

Brancourt-Hulmel M, Heumez E, Pluchard P, Béghin D,Depatureaux C, Giraud A, Le Gouis J. 2005. Indirect versusdirect selection of winter wheat for low input or high inputlevels. Crop Science, 45, 1427-1431

Coque M, Gallais A. 2006. Genomic regions involved inresponse to grain yield selection at high and low nitrogenfertilization in maize. Theoretical and Applied Genetics,112, 1205-1220

Croy L I, Hageman R H. 1970. Relationship of nitrate reductaseactivity to grain protein production in wheat. Crop Science,10, 280-285

Drew M C, Saker L R. 1975. Nutrient supply and the growth ofthe seminal root system in barley. Journal of ExperimentalBotany, 26, 79-90

Eckes P, Schmitt P, Daub W, Wengenmayer F. 1989.Overproduction of alfalfa glutamine synthetase in transgenictobacco plants. Molecular and General Genetics, 217,263-268

Fuentes A, Allen D J, Ortiz-Lopez A, Hernandez G. 2001. Overexpressionof cytosolic glutamine synthetase increasesphotosynthesis and growth at low nitrogen concentrations.Journal of Experimental Botany, 52, 1071-1081

Gaju O, Martre A P, Snape J W, LeGouis H J, Moreau D, BogardM, Griffiths S, Orford S, Hubbart S, Foulkes M J. 2011.Identification of traits to improve the nitrogen-use efficiencyof wheat genotypes. Field Crops Research, 123, 139-152

Gallado F, Fu J, Canton F R, Garcia-Gutierrez A, CanovasF M, Kirby E G. 1999. Expression of a conifer glutaminesynthetase gene in transgenic popular. Planta, 210, 19-26

Gaudinová A. 1990. The effect of cytokinins on nitrate reductaseactivity. Biologia Plantarum, 32, 89-96

Guingo E, Herbert Y, Charcosset A. 1998. Genetic analysis ofroot traits in maize. Agronomie, 18, 225-235

Guo C, Chang W, Zhang L, Cui X, Li S, Xiao K. 2011. Effectsof chromosome substitution on the utilization efficiency ofnitrogen, phosphorus, and potassium in wheat. Frontiersof Agriculture in China, 5, 253-261

Habash D Z, Bernard S, Shondelmaier J, Weyen Y, Quarrie SA. 2006. The genetics of nitrogen use on hexaploid wheat: Nutilization, development and yield. Theoretical and AppliedGenetics, 114, 403-419

Hemon P, Robbins M, Cullimore J. 1990. Targeting of glutaminesynthetase to the mitochondrioa of transgenic tobacco.Plant Molecular Biology, 15, 895-904

Hirel B, Bertin P, Quillere I, Bourdoncle W, Attagnant C, DellayC, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A.2001. Towards a better understanding of the genetic andphysiological basis for nitrogen use efficiency in maize.Plant Physiology, 125, 1258-1270

Hirel B, Marsolier M, Hoarau A, Horrau J, Brangeon J, SchaferR, Verma D P S. 1992. Forcing expression of a soybeanroot glutamine synthetase gene in tobacco leaves inducesa native gene encoding cytosolic enzyme. Plant MolecularBiology, 20, 207-218

Ishihara K, Lida O, Hirasawa T, Ogura T. 1979. Relationshipbetween nitrogen content in leaf blades and photosyntheticrate of rice plants with refrence to stomatal aperture andconductance. Japanese Journal of Crop Science, 48,543-550

Kamara A Y, Kling J G, Menkir A, Ibikunle G. 2003. Agronomicperformance of maize (Zea mays L.) breeding lines derivedfrom a low nitrogen maize population. Journal of AgriculturalScience, 141, 221-230

Kichey T, Heumez E, Pocholle P, Pageau K, Vanacker H,Dubois F, Le Gouis J, Hirel B. 2006. Combined agronomicand physiological aspects of nitrogen management in wheat(Triticum aestivum L.). New Phytologist, 169, 265-278

Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J. 2007. Wheatgenetic variability for post-anthesis nitrogen absorption andremobilisation revealed by 15N labelling and correlations withagronomic traits and nitrogen physiological markers. FieldCrops Research, 102, 22-32

Kirby E G, Gallardo F, Man H M, RI-Khatib R. 2006. Theoverexpression of glutamine synthetase in transgenicpopular: a review. Silvae Genetica, 55, 278-284

Lam H M, Coschigano K, Olivera I C, Melo-Olivera R, CoruzziG. 1996. The molecular genetics of nitrogen assimilationinto amino acids in higher plants. Annual Review of PlantPhysiology and Plant Molecular Biology, 47, 569-593

Lam H M, Coschigano K, Schultz C, Oliveira R M, Tjaden G,Oliveira I, Ngai N, Hsieh M H, Coruzzi G. 1995. Use ofArabidopsis mutants and genes to study amide amino acidbiosynthesis. The Plant Cell, 7, 887-898Laperche A, DEvienne-Baret F, Maury O, Le Gouis J, Ney B

2007. As implified conceptual model of carbon and nitrogenfunctioning for QTL analysis of winter wheat adaptationto nitrogen deficiency. Theoretical and Applied Genetics,113, 1131-1146

Le Gouis J, Béghin D, Heumez E, Pluchard P. 2000. Geneticdifferences for nitrogen uptake and nitrogen utilizationefficiencies in winter wheat. European Journal of Agronomy,12, 163-173

Lea P J, Blackwell R D, Chen F L, Hecht U. 1990. Enzymes ofammonium assimilation. In: Dey P M, Harborne J B, eds.,Methods in Plant Biochemistry. Academic Press, London.pp. 257-276

Lemaire G, Charrier X, Hebert Y. 1996. Nitrogen uptakecapacities of maize and sorghum crops in different nitrogenand water supply conditions. Agronomie, 16, 231-246

London J G. 2005. Nitrogen study fertilizes fears of pollution. Nature, 433, 791.Mackay A D, Barber S A. 1986. Effect of nitrogen on root growthof two corn genotypes in the field. Agronomy Journal, 78,699-703

Maizlich N A, Fritton D D, Kendall W A. 1980. Root morphologyand early development of maize at varying levels of nitrogen.Agronomy Journal, 72, 25-31

Makino A, Mae T, Ohira K. 1987. Variations in the contents andkinetic properties of ribulose-1,5-bisphosphate carboxylasesamong rice species. Plant and Cell Physiology, 28, 799-804

Masclaux C, Quillere I, Gallais A, Hirel B. 2001. The challengeof remobilisation in plant nitrogen economy. A survey ofphysio-agronomic and molecular approaches. Annals ofApplied Biology, 138, 69-81

Moll R H, Kamprath E J, Jackson W A. 1982. Analysis andinterpretation of factors which contribute to efficiency tonitrogen utilization. Agronomy Journal, 75, 562-564

Morikawa H, Takahashi M, Irifune K. 1998. Molecularmechanism of the metabolism of nitrogen dioxide as analternative fertilizer in plants. In: Satoh K, Murata N, eds.,Stress Responses of Photosynthetic Organisms. Elsevier.Dordrecht, The Netherlands. pp. 227-237

Ortiz-Monasterio J I, Sayre K D, Rajaram S, McMahon M. 1997.Genetic progress in wheat yield and nitrogen use efficiencyunder four nitrogen regimes. Crop Science, 37, 898-904

Palta J A, Fillery I R P. 1995. N application increases preanthesiscontribution of dry matter to grain yield in wheatgrown on a duplex soil. Australian Journal of AgriculturalResearch, 46, 507-518

Ramos C. 1996. Effect of agricultural practices on the nitrogenlosses in the environment. In: Rodriguez-Barrueco C, ed.,Fertilizers and Environment. Kluwer Academic Publishers,Dordrecht, The Netherlands.Raun W R, Johnson G V. 1999. Improving nitrogen useefficiency for cereal production. Agronomy Journal, 91,357-363

Rowland A, Murray A J S, Wellburn A R. 1985. Oxides ofnitrogen and their impact upon vegenation. Reviews onEnvironmental Health, 5, 295-342

Sattelmacher B, Thoms K. 1995. Morphology and physiologyof the seminal root system of young maize (Zea mays L.)plants as influenced by a locally restricted nitrate supply.Journal of Plant Nutrition and Soil Science, 158, 493-497

Stulen I, Perez-Soba M, De Kok L J, Van Der Eerden L. 1998.Impact of gaseous nitrogen deposition on plant functioning.New Phytologist, 139, 61-70

Temple S, Knight T, Unkefer P, Sengupta-Gopalan C. 1993.Modulation of glutamine synthetase gene expression intobacco by introduction of an alfalfa glutamine synthetasegene in a sense and antisense orientation: molecular andbiochemica analysis. Molecular and General Genetics,236, 315-325

Tilman D. 1999. Global environmental impacts of agricultureexpansion: the need for sustainable and efficient practices.Proceedings of the National Academy of Sciences of theUnited States of America, 96, 5995-6000

Tuberosa R, Salvi S. 2006. Genomic based approaches toimprove drought tolerance of crops. Trends in Plant Science,11, 405-412

Wang Y, Mi G, Chen F, Zhang J, Zhang F. 2004. Responseof root morphology to nitrate supply and its contribution tonitrogen accumulation in maize. Journal of Plant Nutrition,7, 2189-2202

Wellborn A R. 1990. Why are atmospheric oxides of nitrogenusually phytotoxic and not alternative fertilizers? Newphytologist, 115, 395-429

Whu L, McGechan M B, Watson C A, Baddeley J A. 2005.Developing existing plant root system architecture models tomeet future agricultural challenges. Advances in Agronomy,85, 181-219

Wray J L, Fido R J. 1990. Nitrate reductase and nitritereductase. In: Dey P M, Harborne J B, eds., Methods inPlant Biochemistry. Academic Press, London. pp. 241-256

Zhang H, Forde B G. 1998. An Arabidopsis MADS box genethat controls nutrient-induced changes in root architecture.Science, 279, 407-409

Zhu Z. 2000. Loss of fertilizer N from the plant-soil system andthe strategies and techniques for its reduction in China. SoilEnvironmental Science, 9, 1-6
[1] Lichao Zhai, Shijia Song, Lihua Zhang, Jinan Huang, Lihua Lv, Zhiqiang Dong, Yongzeng Cui, Mengjing Zheng, Wanbin Hou, Jingting Zhang, Yanrong Yao, Yanhong Cui, Xiuling Jia. Subsoiling before winter wheat alleviates the kernel position effect of densely grown summer maize by delaying post-silking root–shoot senescence[J]. >Journal of Integrative Agriculture, 2025, 24(9): 3384-3402.
[2] Yuheng Wang, Furong Kang, Bo Yu, Quan Long, Huaye Xiong, Jiawei Xie, Dong Li, Xiaojun Shi, Prakash Lakshmanan, Yueqiang Zhang, Fusuo Zhang. Magnesium supply is vital for improving fruit yield, fruit quality and magnesium balance in citrus orchards with increasingly acidic soil[J]. >Journal of Integrative Agriculture, 2025, 24(9): 3641-3655.
[3] Xiaoqing Wang, Wenjiao Shi, Qiangyi Yu, Xiangzheng Deng, Lijun Zuo, Xiaoli Shi, Minglei Wang, Jun Li. Well-facilitated farmland improves nitrogen use efficiency and reduces environmental impacts in the Huang-Huai-Hai Region, China[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3264-3281.
[4] Jinpeng Li, Siqi Wang, Zhongwei Li, Kaiyi Xing, Xuefeng Tao, Zhimin Wang, Yinghua Zhang, Chunsheng Yao, Jincai Li. Effects of micro-sprinkler irrigation and topsoil compaction on winter wheat grain yield and water use efficiency in the Huaibei Plain, China[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2974-2988.
[5] Baohua Liu, Ganqiong Li, Yongen Zhang, Ling Zhang, Dianjun Lu, Peng Yan, Shanchao Yue, Gerrit Hoogenboom, Qingfeng Meng, Xinping Chen. Optimizing management strategies to enhance wheat productivity in the North China Plain under climate change[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2989-3003.
[6] Ziqiang Che, Shuting Bie, Rongrong Wang, Yilin Ma, Yaoyuan Zhang, Fangfang He, Guiying Jiang. Mild deficit irrigation delays flag leaf senescence and increases yield in drip-irrigated spring wheat by regulating endogenous hormones[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2954-2973.
[7] Zhongwei Tian, Yanyu Yin, Bowen Li, Kaitai Zhong, Xiaoxue Liu, Dong Jiang, Weixing Cao, Tingbo Dai. Optimizing planting density and nitrogen application to mitigate yield loss and improve grain quality of late-sown wheat under rice–wheat rotation[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2558-2574.
[8] Kuanyu Zhu, Yuemei Xu, Zhiwei Sun, Yajun Zhang, Weiyang Zhang, Yunji Xu, Junfei Gu, Hao Zhang, Zhiqin Wang, Lijun Liu, Jianhua Zhang, Jianchang Yang. Post-anthesis dry matter production and leaf nitrogen distribution are associated with root-derived cytokinins gradient in rice[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2106-2122.
[9] Jiaying Ma, Jian Liu, Yue Wen, Zhanli Ma, Jinzhu Zhang, Feihu Yin, Tehseen Javed, Jihong Zhang, Zhenhua Wang. Enhancing the yield and water use efficiency of processing tomatoes (Lycopersicon esculentum Miller) through optimal irrigation and salinity management under mulched drip irrigation[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2410-2424.
[10] Xiaoqiang Liu, Mingqi Li, Dong Xue, Shuai He, Junliang Fan, Fucang Zhang, Feihu Yin. Optimal drip irrigation leaching amount and timing enhanced cotton fiber yield, quality and nitrogen uptake by regulating soil salinity and nitrate nitrogen in saline-alkaline fields[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2389-2409.
[11] Xin Liu, Shuai Wang, Kang Zeng, Wenjing Li, Shenhao Wang, Sanwen Huang, Huasen Wang, Xueyong Yang. N-myristoyltransferase1 regulates biomass accumulation in cucumber (Cucumis sativus L.)[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1754-1768.
[12] Liang Wang, Nijiang Ai, Zechang Zhang, Chenhui Zhou, Guoli Feng, Sheng Cai, Ningshan Wang, Liuchun Feng, Yu Chen, Min Xu, Yingying Wang, Haoran Yue, Mengfei Chen, Liangshuai Xing, Baoliang Zhou. Development of Gossypium hirsutumGossypium raimondii introgression lines and their use in QTL mapping of agricultural traits[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1688-1703.
[13] Zhaowen Mo, Siren Cheng, Yong Ren, Longxin He, Shenggang Pan, Haidong Liu, Hua Tian, Umair Ashraf, Meiyang Duan, Xiangru Tang. Reduced tillage coupled with straw return improves the grain yield and 2-acetyl-1-pyrroline content in fragrant rice[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1718-1737.
[14] Rumeng Wang, Jinsong Luo, Jian Zeng, Yingying Xiong, Tianchu Shu, Dawei He, Zhongsong Liu, Zhenhua Zhang. BjuB05.GS1.4 promotes nitrogen assimilation and participates in the domestication of shoot nitrogen use efficiency in Brassica juncea[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1800-1812.
[15] Mengyan Cao, Shaoping Ye, Cheng Jin, Junkang Cheng, Yao Xiang, Yu Song, Guorong Xin, Chuntao He. The communities of arbuscular mycorrhizal fungi established by different winter green manures in paddy fields promote post-cropping rice production[J]. >Journal of Integrative Agriculture, 2025, 24(4): 1588-1605.
No Suggested Reading articles found!