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Journal of Integrative Agriculture  2023, Vol. 22 Issue (9): 2660-2672    DOI: 10.1016/j.jia.2023.03.002
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Combining nitrogen effects and metabolomics to reveal the response mechanisms to nitrogen stress and the potential for nitrogen reduction in maize

LU Yan-li1, SONG Gui-pei1, WANG Yu-hong1, WANG Luo-bin1, XU Meng-ze1, ZHOU Li-ping2, WANG Lei1#

1 State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China/Key Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture and Rural Affairs/Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2 Tianjin Academy of Agricultural Sciences, Tianjin 300384, P.R.China
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摘要  

不同氮(N)水平下玉米的生理和代谢差异是田间合理氮素营养管理的基础,对提高氮肥利用率和减少环境污染具有重要作用。本文在明确长期不同氮肥处理下玉米氮效率和产量响应的前提下,利用非靶代谢组学方法分析了相应的差异代谢物及其代谢途径的差异。结果表明,氮胁迫(包括缺乏和过量),通过调节碳代谢产物(包括糖醇和TCA循环中间体)和氮代谢产物(包含各种氨基酸及其衍生物)影响碳氮代谢的平衡。缺氮胁迫时,L-丙氨酸、L-苯丙氨酸、L-组氨酸和L-谷氨酰胺显著下调,而过量氮时,L-缬氨酸、脯氨酸和L-组氨酸显著上调。除了上述碳氮代谢中的糖醇和氨基酸外,在该实验条件下,一些次生代谢物如黄酮类化合物(包括山奈酚、木犀草素、芸香素和香叶木素)和激素类(包括吲哚乙酸、反式玉米素和茉莉酸)可以初步被筛选作为氮胁迫诊断的指标。本研究还表明,N2处理120 kg·ha-1 N)和N3处理180 kg·ha-1 N)的叶片代谢水平相似,这与12年试验中两处理之间生理指标和产量的变化趋势一致。本研究在代谢水平上验证了氮肥减施即施用量从180 kg·ha-1(当地推荐)减少到120 kg·ha-1的可行性,为不降低产量条件下减少氮肥施用,进而提高氮肥利用率和保护生态环境提供了理论基础。



Abstract  

The physiological and metabolic differences in maize under different nitrogen (N) levels are the basis of reasonable N management, which is vital in improving fertilizer utilization and reducing environmental pollution.  In this paper, on the premise of defining the N fertilizer efficiency and yield under different long-term N fertilization treatments, the corresponding differential metabolites and their metabolic pathways were analyzed by untargeted metabolomics in maize.  N stress, including deficiency and excess, affects the balance of carbon (C) metabolism and N metabolism by regulating C metabolites (sugar alcohols and tricarboxylic acid (TCA) cycle intermediates) and N metabolites (various amino acids and their derivatives).  L-alanine, L-phenylalanine, L-histidine, and L-glutamine decreased under N deficiency, and L-valine, proline, and L-histidine increased under N excess.  In addition to sugar alcohols and the above amino acids in C and N metabolism, differential secondary metabolites, flavonoids (e.g., kaempferol, luteolin, rutin, and diosmetin), and hormones (e.g., indoleacetic acid, trans-zeatin, and jasmonic acid) were initially considered as indicators for N stress diagnosis under this experimental conditions.  This study also indicated that the leaf metabolic levels of N2 (120 kg ha–1 N) and N3 (180 kg ha–1 N) were similar, consistent with the differences in their physiological indexes and yields over 12 years.  This study verified the feasibility of reducing N fertilization from 180 kg ha–1 (locally recommended) to 120 kg ha–1 at the metabolic level, which provided a mechanistic basis for reducing N fertilization without reducing yield, further improving the N utilization rate and protecting the ecological environment.

Keywords:  long-term experiment        nitrogen deficiency        nitrogen excess        metabolites        UPLC-QTOF  
Received: 26 September 2022   Accepted: 07 February 2023
Fund: The authors are grateful for the useful comments from the anonymous reviewers and for the support of the National Key R&D Program of China (2021YFD1700900).
About author:  #Correspondence WANG Lei, Tel: +86-10-82105030, Fax: +86-10-82109093, E-mail: wanglei02@caas.cn

Cite this article: 

LU Yan-li, SONG Gui-pei, WANG Yu-hong, WANG Luo-bin, XU Meng-ze, ZHOU Li-ping, WANG Lei. 2023. Combining nitrogen effects and metabolomics to reveal the response mechanisms to nitrogen stress and the potential for nitrogen reduction in maize. Journal of Integrative Agriculture, 22(9): 2660-2672.

Amiour N, Imbaud S, Clément G, Agier N, Zivy M, Valot B, Balliau T, Armengaud P, Quilleré I, Cañas R, Tercet-Laforgue T, Hirel B. 2012. The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps in the control of nitrogen metabolism in crops such as maize. Journal of Experimental Botany63, 5017–5033.

Beatty P H, Klein M S, Fischer J J, Lewis I A, Muench D G, Good A G. 2016. Understanding plant nitrogen metabolism through metabolomics and computational approaches. Plants5, 39.

Beatty P, Shrawat A K, Caroll R Zhu, T, Good A G. 2009. Trancriptome analysis of nitrogen-efficient rice overexpressing alanine aminotransferase. Plant Biotechnology Journal7, 562–576.

Benton H P, Ivanisevic J, MahieuN G, Kurczy M E, Johnson, C H, Franco L, Rinehart D, Valentine E, Gowda H, Ubhi B K, Tautenhahn R, Gieschen A, Fields M W, Patti G J, Siuzdak G. 2015. Autonomous metabolomics for rapid metabolite identification in global profiling. Analytical Chemistry87, 884–891.

Cao Y W, Qu R J, Tang X Q, Miao Y J. 2020, UPLC-Triple TOF-MS/MS based metabolomics approach to reveal the influence of nitrogen levels on Isatis indigotica seedling leaf. Scientia Horticulturae266, 109280.

Chen F J , Fang Z G, Gao Q, Ye Y L, Jia L L, Yuan L X, Mi G H, Zhang F S. 2013. Evaluation of the yield and nitrogen use efficiency of the dominant maize hybrids grown in North and Northeast China. Science China-Life Sciences56, 552–560.

Fiehn O. 2002. Metabolomics - The link between genotypes and phenotypes. Plant Molecular Biology48, 155–171.

Fiehn O, Kopka J, Dörmann P, Altmann T, Trethewey R N, Willmitzer L. 2000. Metabolite profiling for plant functional genomics. Nature Biotechnology18, 1157–1161.

Gardner J, Drinkwater L. 2009. The fate of nitrogen in grain cropping systems: A meta-analysis of 15N field experiments. Ecological Applications19, 2167–2184.

Good A G, Beatty P H. 2011. Fertilizing nature: A tragedy of excess in the commons. PLoS Biology9, 1124.

Gutiérrez R A. 2012. Systems biology for enhanced plant nitrogen nutrition. Science336, 1673–1675.

Hakeem K R, Ahmad A, Iqbal M, Gucel S, Ozturk M. 2011. Nitrogen-efficient rice cultivars can reduce nitrate pollution. Environmental Science and Pollution Research18, 1184–1193.

Hawkesford M J, Barraclough P. 2011. An overview of nutrient use efficiency and strategies for crop improvement. In: Hawkesford M J, Barraclough P, eds., The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops. 1st ed. John Wiley & Sons, Inc, New Jersey, NJ, USA.

Johnson J, Franzluebbers A J, Weyers S L, Reicosky D C. 2007. Agricultural opportunities to mitigate greenhouse gas emissions. Environment Pollution150, 107–124.

Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A, Castaings L, Daniel-Vedele F. 2011. Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiology157, 1255–1282.

Li P, Chen F, Cai H, Liu J, Pan Q, Liu Z, Gu R, Mi G, Zhang F, Yuan L. 2015. A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis. Journal of Experimental Botany66, 3175–3188.

McAllister C H, Beatty P H, Good A G. 2012. Engineering nitrogen use efficient crop plants: The current status. Plant Biotechnology10, 1011–1025.

Meyer R C, Steinfath M, Lisec J, Becher M, Witucka-Wall H, Torjek O, Fiehn O, Eckardt A, Willmitzer L, Selbig J, Altmann S. 2007. The metabolic signature related to high plant growth rate in Arabidopsis thalianaProceedings of the National Academy of Sciences of the United States of America104, 4759–4764.

Montzka S, Dlugokencky E, Butler J. 2011. Non-CO2 greenhouse gases and climate change. Nature476, 43–50.

Nazir M, Pandey R, Siddiqi T O, Ibrahim M M, Qureshi M I, Abraham G, Vengavasi K, Ahmad A. 2016, Nitrogen-deficiency stress induces protein expression differentially in low-N tolerant and low-N sensitive maize genotypes. Frontiers in Plant Science7, 298.

Patterson K, Cakmak T, Cooper A, Lager I, Rasmudson A G, Escobar M A. 2010. Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell and Environment33, 1486–1501.

Richard M, Röhlig J E, Karl-Heinz E. 2009. Metabolite profiling of maize grain: differentiation due to genetics and environment. Metabolomics5, 459.

Schauer N, Fernie A R. 2006. Plant metabolomics: towards biological function and mechanism. Trends in Plant Science11, 508–516.

Schlüter U, Mascher M, Colmsee C, Scholz U, Bräutigam A, Fahnenstich H, Sonnewald U. 2012. Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Biotechnology Journal160, 1384–1406.

Shrawat A K, Carroll R T, DePauw M, Taylor G J, Good A G. 2008. Genetic engineering of improved nitrogen use efficiency in rice by the tissue - specific expression of alanine aminotransferase. Plant Biotechnology Journal6, 722–732.

Shulaev V, Cortes D, Miller G, Mittler R, 2008. Metabolomics for plant stress response. Physiologia Plantarum132, 199–208.

Simons M, Saha R, Guillard L, Clement G, Armengaud P, Canas R, Maranas C D, Lea P J, Hirel B. 2014. Nitrogen-use efficiency in maize (Zea mays L.): from ‘omics’ studies to metabolic modelling. Journal of Experimental Botany19, 5657–5671.

Tohge T, de Souza L P, Fernie A R. 2014. Genome-enabled plant metabolomics. Journal of Chromatography B966, 7–20.

Trevisan S, Borsa P, Botton A, Varotto S, Malagoli M, Ruperti B, Quaggiotti S. 2010. Expression of two maize putative nitrate transporters in response to nitrate and sugar availability. Plant Biology10, 462–475.

Wei S, Wang X, Shi D, Li Y, Zhang J, Liu P, Zhao B, Dong S. 2016. The mechanisms of low nitrogen induced weakened photosynthesis in summer maize (Zea mays L.) under field conditions. Plant Physiology and Biochemistry105, 118–128.

Xin W, Zhang L, Zhang W, Gao J, Yi J, Zhen X, Li Z, Zhao Y, Peng C, Zhao C. 2019. An integrated analysis of the rice transcriptome and metabolome reveals differential regulation of carbon and nitrogen metabolism in response to nitrogen availability. International Journal of Molecular Sciences20, 2349.

Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T. 2004. Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proceedings of the National Academy of Sciences of the United States of America101, 7833–7838.

Yang N, Jiang J, Xie H, Bai M Y, Xu Q Z, Wang X G, Yu X M, Chen Z C, Guan Y F. 2017. Metabolomics reveals distinct carbon and nitrogen metabolic responses to magnesium deficiency in leaves and roots of soybean (Glycine max (Linn.) Merr.). Frontiers in Plant Science8, 2091.

Zhang Y, Ma X M, Wang X C, Liu J H, Huang B Y, Guo X Y, Xiong S P, La G X. 2017. UPLC-QTOF analysis reveals metabolomic changes in the flag leaf of wheat (Triticum aestivum L.) under low-nitrogen stress. Plant Physiology and Biochemistry111, 30–38.

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