Genomics of Nitrogen Use Efficiency in Maize: From Basic Approaches to Agronomic Applications

  • Bertrand Hirel
  • Peter J. Lea
Part of the Compendium of Plant Genomes book series (CPG)


Maize farming requires high amounts of nitrogen (N) fertilizer, which can have detrimental effects on agronomic sustainability and the environment. Thus, irrespective of the mode of N fertilization, an increased knowledge of the mechanisms controlling plant N metabolism is essential for improving nitrogen use efficiency (NUE) in maize. This new knowledge will reduce the excessive input of fertilizers, while maintaining an acceptable yield and a sufficient profit margin for the farmers. It is now possible to further develop whole-plant agronomic and physiological studies. These can be combined with gene, protein, and metabolite profiling to build up a comprehensive picture depicting the different steps of N uptake, assimilation, and recycling to produce either biomass in vegetative organs or proteins in storage organs. We provide an overview describing how our understanding of the physiological and molecular controls of N assimilation in maize has been advanced using combined approaches. These are based on agronomic, whole-plant physiology, genetic, modeling, and systems biology approaches. Current knowledge and prospects for selecting high-yielding maize genotypes adapted to lower N fertilizer input and for identifying biological markers representative of the plant N status for breeding and agronomic purposes are reviewed.


Agronomy Genetics Maize Nitrogen Physiology Systems biology Yield 


  1. Abad MS, Coffin M, Goldman BS (2015) Genes encoding glutamine synthetase and used for plant improvement. US patent 20150184189 A1Google Scholar
  2. Abdel-Ghani AH, Kumar B, Pace J, Jansen C, Gonzalez-Portillla PJ, Reyes-Matamoros J, San Martin JP, Lee M, Lübberstedt T (2015) Association analysis of genes involved in maize (Zea mays L.) root development with seedlings and agronomic traits under contrasting nitrogen levels. Plant Mol Biol 88:133–147PubMedCrossRefGoogle Scholar
  3. Allen SM, Guo M, Loussaert DF, Rupe M, Wang H (2014) Enhanced nitrate uptake and nitrate translocation by over-expressing maize functional low-affinity nitrate transporters in transgenic maize. US patent 20160010101 A1Google Scholar
  4. Amiour N, Imbaud S, Clement G, Agier N, Zivy M, Valot B, Balliau T, Armengaud P, Quilleré I, Cañas RA, Tercé-Laforgue T, Hirel B (2012) The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J Exp Bot 63:5017–5033PubMedCrossRefGoogle Scholar
  5. Amiour N, Imbaud S, Clément G, Agier N, Zivy M, Valot B, Balliau T, Quilleré I, Tercé-Laforgue T, Dargel-Graffin C, Hirel B (2014) An integrated “omics” approach to the characterization of maize (Zea mays L.) mutants deficient in the expression of two genes encoding cytosolic glutamine synthetase. BMC Genom 15:1005CrossRefGoogle Scholar
  6. Andrews M, Lea PJ, Raven JA, Lindsey K (2004) Can genetic manipulation of plant nitrogen assimilation enzymes result in increased crop yield and greater N-use efficiency? An assessment. Ann Appl Biol 145:25–40CrossRefGoogle Scholar
  7. Andrews M, Raven JA, Lea PJ (2013) Do plants need nitrate? The mechanisms by which nitrogen form affects plants. Ann Appl Biol 163:174–199CrossRefGoogle Scholar
  8. Bashan Y, de-Bashan LE, Prabhu, SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33CrossRefGoogle Scholar
  9. Beatty PH, Klein MS, Fisher JJ, Lewis IA, Muench DG, Good AG (2016) Understanding plant nitrogen metabolism through metabolomics and computational approaches. Plants 5:39. Scholar
  10. Becker TW, Perrot-Rechenman C, Suzuki A, Hirel B (1993) Subcellular and immunocytochemical localization of the enzymes involved in ammonia assimilation in mesophyll and bundle sheath strands of maize leaves. Planta 191:129–136CrossRefGoogle Scholar
  11. Bernard SM, Habash DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182:608–620PubMedCrossRefGoogle Scholar
  12. Bi YM, Meyer A, Downs GS, Shi X, El-kereamy A, Lukens L, Rothsten SJ (2014) High throughput RNA sequencing of a hybrid maize and its parents shows different mechanisms responsive to nitrogen limitation. BMC Genomics 15:77PubMedPubMedCentralCrossRefGoogle Scholar
  13. Binder DL, Sander DH, Walters DT (2000) Maize response to time of nitrogen application as affected by level of nitrogen deficiency. Agron J 92:1228–1236CrossRefGoogle Scholar
  14. Bloom AJ (2015) The increasing importance of distinguishing among plant nitrogen sources. Curr Opin Plant Biol 25:10–16PubMedCrossRefGoogle Scholar
  15. Bräutigam A, Gowik U (2016) Photorespiration connects C3 and C4 photosynthesis. J Exp Bot 67:2953–2962PubMedCrossRefGoogle Scholar
  16. Broyard C, Fontaine JX, Molinie R, Cailleu D, Tercé-Laforgue T, Dubois F, Hirel B, Dubois F, Mesnard F (2009) Metabolomic profiling of two cytosolic glutamine synthetase maize mutants (Zea mays L.) using 1H-nuclear magnetic resonance. Phytochem Anal 21:102–109CrossRefGoogle Scholar
  17. Cameron KC, Di HJ, Moir JL (2013) Nitrogen losses from the soil/plant system: a review. Ann Appl Biol 162:145–173CrossRefGoogle Scholar
  18. Cañas RA, Quilleré I, Christ A, Hirel B (2009) Nitrogen metabolism in the developing ear of maize (Zea mays L.): analysis of two lines contrasting in their mode of nitrogen management. New Phytol 184:340–352PubMedCrossRefGoogle Scholar
  19. Cañas RA, Quilleré I, Lea PJ, Hirel B (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isoenzymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotech J 8:966–978CrossRefGoogle Scholar
  20. Cañas RA, Amiour N, Quilleré I, Hirel B (2011) An integrated statistical analysis of the genetic variability of nitrogen metabolism in the ear of three maize inbred lines (Zea mays L). J Exp Bot 62:2309–2318PubMedCrossRefGoogle Scholar
  21. Cañas RA, Quilleré I, Gallais A, Hirel B (2012) Can genetic variability for nitrogen metabolism in the developing ear of maize be exploited to improve yield? New Phytol 194:440–452PubMedCrossRefGoogle Scholar
  22. Cañas RA, Yesbergenova-Cuny Z, Simons M, Chardon F, Armengaud P, Quilleré I, Cukier C, Gibon G, Limami AM, Nicolas S, Brulé L, Lea PJ, Maranas CD, Hirel B (2017) Exploiting the genetic diversity of maize using a combined metabolomic, enzyme activity profiling, and metabolic modeling approach to link leaf physiology to kernel yield. Plant Cell 29:919–943PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cao H, Qi S, Sun M, Li Z, Yang Y, Crawford NM, Yong W (2017) Overexpression of the maize ZmNLP6 and ZmNLP8 can complement the Arabidopsis nitrate regulatory mutant nlp7 by restoring nitrate signaling and assimilation. Front Plant Sci 8:1703PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cassán F, Diaz-Zorita M (2016) Azospirillum sp. in current agriculture: from the laboratory to the field. Soil Biol Biochem 103:117–130CrossRefGoogle Scholar
  25. Castaing L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercier S, Taconat L, Renou JP, Daniel-Vedele F, Fernandez E, Meyer C, Krapp A (2009) The nodule interception-like protein 7 modulates nitrate sensing and metabolism in maize. Plant J 57:426–435CrossRefGoogle Scholar
  26. Cavalar M, Phlippen Y, Kreuzaler F, Peterhaensel C (2007) A drastic reduction in DOF1 transcript levels does not affect C4 specific gene expression in maize. J Plant Physiol 164:1665–1674PubMedCrossRefGoogle Scholar
  27. Ceccarelli S (2014) GM crops, organic agriculture and breeding for sustainability. Sustainability 6:4273–4286CrossRefGoogle Scholar
  28. Chae L, Kim T, Nilo-Poyanco Rhee SY (2014) Genomic signatures of specialized metabolism in plants. Science 244:510–513CrossRefGoogle Scholar
  29. Chalk PM (2016) The strategic role of 15N in quantifying the contribution of endophytic N2 fixation to the nutrition of non-legumes. Symbiosis 69:63–80CrossRefGoogle Scholar
  30. Chen Q, Liu Z, Wang B, Wang X, Lai J, Tian F (2015) Transcriptome sequencing reveals the roles of transcription factors in modulating genotype by nitrogen interaction in maize. Plant Cell Rep 34:1761–1771PubMedPubMedCentralCrossRefGoogle Scholar
  31. Ciampitti IA, Vyn TJ (2013) Grain nitrogen source changes over time in maize: a review. Crop Sci 53:366–377CrossRefGoogle Scholar
  32. Colmsee C, Masher M, Czauderna T, Hartman A, Schlüter U, Zellerhoff N, Schmitz J, Bräutigam A, Pick TR, Alter P, Gahrtz M, Witt S, Fernie AR, Börnke F, Fahenenstich H, Bucher M, Dresselahaus T, Weber APM, Schreiber F, Scholtz U, Sonnewald U (2012) OPTIMAS-DW: a comprehensive transcriptomics, metabolomics, ionomics, proteomics and phenomics data resource for maize. BMC Plant Biol 12:245PubMedPubMedCentralCrossRefGoogle Scholar
  33. Coque M, Gallais A (2007) Genetic variation among European maize varieties for nitrogen use efficiency under low and high nitrogen fertilization. Maydica 52:383–397Google Scholar
  34. Cren M, Hirel B (1999) Glutamine synthetase in higher plants: regulation of gene and protein expression from the organ to the cell. Plant Cell Physiol 40:1187–1193CrossRefGoogle Scholar
  35. Davenport S, Lay PL, Sanchez-Tamburrino JP (2015) Nitrate metabolism in tobacco leaves overexpressing Arabidopsis nitrite reductase. Plant Physiol Biochem 97:96–107PubMedCrossRefGoogle Scholar
  36. De Abreu e Lima F, Westhues M, Cuardos-Inostroza A, Willmitzer L, Melchinger AE, Nikoloski F (2017) Metabolic robustness in young roots underpins a predictive model of maize hybrid performance in the field. Plant J 90:319–329PubMedCrossRefGoogle Scholar
  37. Dechorgnat J, Francis KL, Dhugga KS, Rafalski JA, Tyerman SD, Kaiser BN (2018) Root ideotype influences nitrogen transport and assimilation in maize. Front plant Sci 9:531PubMedPubMedCentralCrossRefGoogle Scholar
  38. Dell’Acqua M, Gatti DM, Pea G, Cattonaro F, Coppens F, Magris G, Hliaing AL, Aung HH, Nelissen H, Baute J, Frascaroli E, Churchill GA, Inzé D, Morgante M, Pè ME (2015) Genetic properties of the MAGIC maize population: a new platform for high definition QTL mapping in Zea mays. Genome Biol 16:167PubMedPubMedCentralCrossRefGoogle Scholar
  39. Deng M, Li D, Lou J, Xiao Y, Liu H, Pan Q, Zhang X, Jin M, Zhao M, Yan J (2017) The genetic architecture of amino acid dissection by association and linkage analysis in maize. Plant Biotech J 1–14Google Scholar
  40. de Souza R, Ambrosini A, Passaglla LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419PubMedPubMedCentralCrossRefGoogle Scholar
  41. Dubois F, Tercé-Laforgue T, Gonzalez-Moro MB, Estavillo MB, Sangwan R, Gallais A, Hirel B (2003) Glutamate dehydrogenase in plants: is there a new story for an old enzyme? Plant Physiol Biochem 41:565–576CrossRefGoogle Scholar
  42. Edwards KD, Fernandez-Pozo N, Drake-Stowe K, Humphry M, Evans AD, Bombarely A, Allen F, Hurst R, White B, Kernodle SP, Bromley JR, Sanchez-Tamburrino JP, Lewis RS, Mueller LA (2017) A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC Genomics 18:448PubMedPubMedCentralCrossRefGoogle Scholar
  43. EEA (2012) Air quality in Europe, 2012-report, EAA report no. 4/2012. European Environment Agency, Copenhagen, Denmark, p 104.
  44. Erdal S, Turk H (2016) Cysteine-induced upregulation of nitrogen metabolism-related genes and enzymes activities enhance tolerance of maize seedlings to cadmium stress. Environ Exp Bot 132:92–99CrossRefGoogle Scholar
  45. Espejo-Herrera N, Gràcia-Lavedan E, Boldo E et al (2016) Colorectal cancer risk and nitrate exposure through drinking water and diet. Int J Cancer 139:334–346PubMedCrossRefGoogle Scholar
  46. Fageria NK (2008) The use of nutrients in crop plants. CRC Press, Taylor & Francis group, Boca Raton, London, New YorkGoogle Scholar
  47. Fan X, Tang Z, Tan Y, Zhang Y, Luo B, Yang M, Lian X, Shen Q, Miller AJ, Xu G (2016) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yield. Proc Natl Acad Sci USA 113:7118–7123PubMedCrossRefGoogle Scholar
  48. Farré G, Twyman RM, Christou P, Capell T, Zhu C (2015) Knowledge-driven approaches for engineering complex metabolic pathways in plants. Curr Opin Biotech 32:54–60PubMedCrossRefGoogle Scholar
  49. Fernie AR, Stitt M (2012) On the discordance of metabolomics with proteomics and transcriptomics: coping with increasing complexity in logic, chemistry, and network interactions. Plant Physiol 158:1139–1145PubMedPubMedCentralCrossRefGoogle Scholar
  50. Fischer JJ, Beatty PH, Good AG, Muench DG (2013) Manipulation of microRNA expression to improve nitrogen use efficiency. Plant Sci 210:70–81PubMedCrossRefGoogle Scholar
  51. Fixen P, Brentup F, Bruuslema TW, Garcia F, Norton R, Zingore S (2015). Nutrient/fertilizer use efficiency: measurement, current situation and trends. In: Drechel P, Heffer P, Magen H, Mikkelsen R, Wilchelns D (eds) Managing water and fertilizer for sustainable agricultural intensification. International Fertilizer Industry Association (IFA), International Water Management Institute (IWMI), International Plant Nutrition Institute (IPNI), and International Potash Institute (IPI), Paris, France, January 2015, p 8Google Scholar
  52. Fontaine JX, Tercé-Laforgue T, Armengaud P, Clément G, Renou JP, Pelletier S, Catterou M, Azzopardi M, Gibon Y, Lea PJ, Hirel B, Dubois F (2012) Characterization of a NADH-dependent glutamate dehydrogenase mutant of Arabidopsis demonstrates the key role of this enzyme in root carbon and nitrogen metabolism. Plant Cell 24:4044–4065PubMedPubMedCentralCrossRefGoogle Scholar
  53. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358PubMedCrossRefGoogle Scholar
  54. Fowler D, Steadman CE, Stevenson D, Coyle M, Ress RM, Skiba UM, Sutton MA, Cape JN, Dore AJ, Vieno M, Simpson D, Zaehle S, Stocker BD, Rinaldi M, Facchini MC, Flecahrd CR, Nemitz E, Twigg M, Erisman JW, Butterbach-Bahlk K, Galloway JN (2015) Effects of global change during the 21st century on the nitrogen cycle atmos. Chem Phys 15:13849–13893Google Scholar
  55. Fox T, DeBruin J, Haug Collet K, Trimnel M, Clapp J, Leonard A, LI B, Scolaro E, Collinson S, Glassman K, Miller M, Schlusser J, Dolan D, Lu L, Gho C, Albertsen M, Loussaert D, Shen B (2017) A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize. Plant Biotech J 15:942–952PubMedPubMedCentralCrossRefGoogle Scholar
  56. Freund DM, Hegeman AD (2017) Recent advances in stable isotope-anabled mass spectrometry-based plant metabolomics. Curr Opin Plant Biol 43:41–48Google Scholar
  57. Fukushima A, Kusano M (2013) Recent progress in the development of metabolome databases for plant systems biology. Front Plant Sci 4:73PubMedPubMedCentralCrossRefGoogle Scholar
  58. Fukushima A, Kusano M (2014) A network perspective on nitrogen metabolism from model to crop plants using integrated ‘omics’ approaches. J Exp Bot 65:5619–5630PubMedCrossRefGoogle Scholar
  59. Gallais A, Coque M (2005) Genetic variation and selection for nitrogen use efficiency in maize: a synthesis. Maydica 50:531–547Google Scholar
  60. Gallais A, Coque M, Quilleré I, Le Gouis J, Prioul JL, Hirel B (2007) Estimating proportions of N-remobilization and of post-silking N-uptake allocated to maize kernels by 15N-labelling. Crop Sci 47:685–691CrossRefGoogle Scholar
  61. Gallais A, Hirel B (2004) An approach to the genetics of nitrogen use efficiency in maize. J Exp Bot 55:295–306PubMedCrossRefGoogle Scholar
  62. Gallavotti A, Whipple CJ (2015) Positional cloning in maize (Zea mays Subsp. mays, Poaceae). Appl Plant Sci 3:1400092CrossRefGoogle Scholar
  63. Galloway JN, Leach AM, Bleeker A, Erisman JW (2013) A chronology of human understanding of the nitrogen cycle. Phil Trans Royal Soc Lond B 368. Scholar
  64. Garnett T, Conn V, Plett D, Conn S, Zanghellini J, Mackenzie N, Enju A, Francis K, Holtham L, Roessner U, Boughton B, Bacic A, Shirley N, Rafalski A, Dhugga K, Tester M, Kaiser BN (2013) The response of the maize nitrate transport system to nitrogen demand and supply across the lifecycle. New Phytol 198:82–94PubMedCrossRefGoogle Scholar
  65. Garnett T, Plett D, Conn V, Conn S, Rabie H, Rafalski JA, Dhugga K, Tester MA, Kaiser B (2015) Variation for N uptake system in maize: genotypic response to N supply. Front plant Sci 6:936PubMedPubMedCentralCrossRefGoogle Scholar
  66. Gehan MA, Greenham K, Mockler TC, McKlung CR (2015) Transcriptional networks-crops, clocks, and abiotic stress. Curr Opin Plant Biol 24:39–46PubMedCrossRefGoogle Scholar
  67. Gellings CW, Parmenter KE (2016) In: Gellings CW (ed) Efficient use and conservation of energy. Energy efficiency in fertilizers production and use, vol II. EOLSS Publications, p 123Google Scholar
  68. Gu R, Duan F, An X, Zhang F, von Wirén N, Yuan L (2013) Characterization of AMT—mediated high affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol 54:1515–1514PubMedCrossRefGoogle Scholar
  69. Guo S, Sun WY, Gu RL, Zhao BQ, Yuan LX, Mi GH (2014) Expression of genes related to nitrogen metabolism in maize grown under organic and inorganic nitrogen supplies. Soil Sci Plant Nutr 61:275–280CrossRefGoogle Scholar
  70. Gupta R, Hou Z, Loussaert DL, Shen B, Wood LK (2013) Engineering plants for efficient uptake and utilization of urea to improve crop production. US Patent 20140351998 A1Google Scholar
  71. Habbib H, Verzeaux J, Nivelle E, Roger D, Lacoux J, Catterou M, Hirel B, Dubois F, Tétu T (2016) Conversion to no-till improves maize nitrogen use efficiency in a continuous cover cropping system. PLOS One 11:10. Scholar
  72. Habbib H, Hirel B, Verzeaux J, Roger D, Lacoux J, Lea PJ, Dubois F, Tetu T (2017) Investigating the combined effect of tillage, nitrogen fertilization and cover crops on nitrogen use efficiency in winter wheat. Agronomy 7:66.
  73. Habermeyer M, Roth A, Guth S, Diel P, Engel KH, Epe B, Fürst P, Heinz V, Humpf HU, Joost HG, Knorr D, de Kok T, Kulling S, Lampen A, Marko D, Rechkemmer G, Rietjens I, Stadler RH, Vieths S, Vogel R, Steinberg P, Eisenbrand G (2015) Nitrate and nitrite in the diet: how to assess their benefit and risk for human health. Mol Nutr Food Res 59:106–128PubMedCrossRefGoogle Scholar
  74. Haegele JW, Cook KA, Nichols DM, Below FE (2013) Changes in nitrogen use traits associated with genetic improvement for grain yield of maize hybrids released in different decades. Crop Sci 53:1256–1268CrossRefGoogle Scholar
  75. Han J, Wang L, Zheng H, Pan X, Li H, Chen F, Li X (2015a) ZD958 is a low-nitrogen-efficient maize hybrid at the seedling stage among five maize and two teosinte lines. Planta 242:935–949PubMedCrossRefGoogle Scholar
  76. Han M, Okamoto M, Beatty PH, Rothstein SJ, Good AJ (2015b) The genetics of nitrogen use efficiency in crop plants. Ann Rev Genet 49:269–289PubMedCrossRefGoogle Scholar
  77. He C-M, Liu C-X, Liu Q, Gao X-X, Li N, Zhang J-R, Wang L-M Liu T-S (2014) Over-expression of glutamine synthetase genes Gln1-3/Gln1-4 improved nitrogen assimilation and maize yields. Maydica 59:250–256Google Scholar
  78. 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 125:1258–1270PubMedPubMedCentralCrossRefGoogle Scholar
  79. Hirel B, Gallais A (2011) Nitrogen use efficiency—physiological, molecular and genetic investigations towards crop improvement. In: Prioul JL, Thévenot C, Molnar T (eds) Advances in maize, essential reviews in experimental biology, vol 3. Society for Experimental Biology, UK, pp 285–310Google Scholar
  80. Hirel B, Lea PJ (2001) Ammonia assimilation. In: Lea PJ, Morot-Gaudry JF (eds) Plant nitrogen. Springer, INRA Editions, pp 79–99CrossRefGoogle Scholar
  81. Hirel B, Lea PJ (2002) The biochemistry, molecular biology, and genetic manipulation of primary ammonia assimilation. In: Foyer CH, Noctor G (eds) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism, advances in photosynthesis and respiration. Kluwer Academic Publishers, Dordrecht, Boston, London, pp 71–92Google Scholar
  82. Hirel B, Le Gouis J, Bernard M, Perez P, Falque M, Quétier F, Joets J, Montalent P, Rogwoski P, Murigneux A, Charcosset A (2007a) Genomics and plant breeding: maize and wheat. In: Morot-Gaudry JF, Lea PJ, Briat JF (eds) Functional plant genomics. Science Publishers, Enfield, NH, pp 614–635Google Scholar
  83. Hirel B, Le Gouis J, Ney B, Gallais A (2007b) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387PubMedPubMedCentralCrossRefGoogle Scholar
  84. Hirel B, Martin A, Tercé-Laforgue T, Gonzalez-Moro MB, Estavillo JM (2005) Physiology of maize I: a comprehensive and integrated view of nitrogen metabolism in a C4 plant. Physiol Plant 124:167–177CrossRefGoogle Scholar
  85. Hirel B, Perez P (2016) Increased kernel productivity of plants through the modulation of glutamine synthetase activity. US patent 9422571 B2Google Scholar
  86. Hirel B, Tétu T, Lea PJ, Dubois F (2011) Improving nitrogen use efficiency in crops for a sustainable agriculture. Sustainability 3:1452–1485CrossRefGoogle Scholar
  87. Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystem. Plant Soil 386:1–19CrossRefGoogle Scholar
  88. Horde NG, Conley MN (2017) Regulation of dietary nitrate and nitrite: balancing essential physiological roles with potential health risks. In: Bryan NS, Loscalzo J (eds) Nitrite and nitrate in human health and disease, nutrition and health. Springer, Heidelberg, p 153CrossRefGoogle Scholar
  89. Hu J, Rampitsch C, Bykova NV (2015) Advances in plant proteomics toward improvement of crop productivity and stress resistance. Front Plant Sci 6:209PubMedPubMedCentralGoogle Scholar
  90. Humbert S, Subedi S, Cohn J, Zeng B, Bi YM, Chen X, Zhu T, McNicholas PD, Rothstein SJ (2013) Genome-wide expression profiling of maize in response to individual and combined water and nitrogen stresses. BMC Genomics 14:3PubMedPubMedCentralCrossRefGoogle Scholar
  91. Ibrahim A, JIn X-L, Zhang YB, Cruz J, Vichyavichen P, Esiobu N, Zhang XH (2017) Tobacco plants expressing the maize nitrate transporter ZmNrt2.1 exhibit altered response of growth and gene expression to nitrate and calcium. Bot Stud 58:51Google Scholar
  92. Jansen C, Zhang Y, Liu H, Gonzalez-Portilla PJ, lauter N, Kumar B, Trucillo-Silva I, San Martin JP, Lee M, Simcox K, Schussler J, Dhugga K, Lübbersedt (2015) Genetic and agronomic assessment of cob traits in corn under low and normal nitrogen management conditions. Theor Appl Genet 128:1231–1242PubMedCrossRefGoogle Scholar
  93. Jin X, Li W, Hu D, Shi X, Zhang X, Zhang F, Fu Z, Ding D, Liu Z, Tang J (2015) Biological responses and proteomic changes in maize seedlings under nitrogen deficiency. Plant Mol Biol Rep 33:490–504CrossRefGoogle Scholar
  94. Junker BH (2014) Flux analysis in plant metabolic networks: increasing throughput and coverage. Curr Opin Plant Biol 26:18188Google Scholar
  95. Kanter DR, Zhang X, Mauzerall DL (2015) Reducing nitrogen pollution while decreasing farmer’s costs and increasing fertilizer industry profits. J Environ Qual 44:325–335PubMedCrossRefGoogle Scholar
  96. Klopfenstein TJ, Erickson GE, Berger LL (2013) Maize is critically important source of food, feed, energy and forage in the USA. Field Crop Res 153:5–11CrossRefGoogle Scholar
  97. Kou HP, Li Y, Song XX, Ou XF, Xing SC, Ma J, Von Wettstein D (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol 168:1685–1693PubMedCrossRefGoogle Scholar
  98. Kruger NJ, Ratcliffe RG (2012) Pathways and fluxes: exploring the plant metabolic network. J Exp Bot 63:2243–2246PubMedCrossRefGoogle Scholar
  99. Kruger NJ, Ratcliffe RG (2015) Fluxes through metabolic network: measurements, predictions insights and challenges. Biochem J 465:27–38PubMedCrossRefGoogle Scholar
  100. Kuan KB, Othman R, Abdul Rahim K, Shamsuddin ZH (2016) Plant growth promoting rhizobacteria inoculation to enhance vegetative growth, nitrogen fixation and nitrogen remobilization of maize under greenhouse conditions. PLOS One. Scholar
  101. Labboun S, Tercé-Laforgue T, Roscher A, Bedu M, Restivo FM, Velanis CN, Skopelitis DS, Moshou PN, Roubelakis-Angelakis KA, Suzuki A, Hirel B (2009) Resolving the role of plant glutamate dehydrogenase: I. In vivo real time nuclear magnetic resonance spectroscopy experiments. Plant Cell Physiol 50:1761–1773PubMedPubMedCentralCrossRefGoogle Scholar
  102. Lassaletta L, Billen G, Garnier J, Bouwman L, Velazquez E, Mueller ND, Gerber JS (2016) Nitrogen use in the global food system: past trends and future trajectories of agronomic performance, pollution, trade, and dietary demand. Environ Res Lett 11:095007CrossRefGoogle Scholar
  103. Lea PJ, Miflin BJ (2011) Nitrogen assimilation and its relevance to crop improvement. In: Foyer CH, Zhang H (eds) Annual plant reviews, nitrogen metabolism in plants in the post-genomic era. Wiley-Blackwell, Chichester, UK, vol 42, p 40Google Scholar
  104. Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG (2007) Asparagine in plants. Ann Appl Biol 150:1–26CrossRefGoogle Scholar
  105. Léran S, Varala K, Boyer JC, Chiurazzi M, Crawford N, Daniel-Vedele F, David L, Dickstein R, Fernandez E, Forde B, Gassmann W, Geiger D, Gojon A, Gong JM, Halkier BA, Harris JM, Hedrich R, Limami AM, Rentsh D, Seo M, Tsay LF, Zhang M, Coruzzi G, Lacombe B (2014) A unified nomenclature of nitrate TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19:5–9PubMedCrossRefGoogle Scholar
  106. Li MG, Villemur R, Hussey PJ, Silflow CD, Gantt JS, DP (1993) Differential expression of six glutamine synthetase genes in Zea mays. Plant Mol Biol 23:401–40PubMedCrossRefGoogle Scholar
  107. Li Y, Wang M, Zhang F, Xu Y, Chen X, Qin X, Wen X (2016) Effect of post-silking drought on nitrogen partitioning and gene expression pattern of glutamine synthetase and asparagine synthetase in two maize (Zea mays L.) varieties. Plant Physiol Biochem 102:62–69PubMedCrossRefGoogle Scholar
  108. Liao C, Peng Y, Ma W, Liu R, LI C, Li X (2012) Proteomic analysis revealed nitrogen-mediated metabolic, developmental, and hormonal regulation of maize (Zea mays L.) ear growth. J Exp Bot 63:5275–5288PubMedPubMedCentralCrossRefGoogle Scholar
  109. Lightfoot DA, Mungur R, Ameziane R, Nolte S, Long L, Bernhard K, Colter A, Jones K, Iqbal MJ, Varsa E, Young B (2007) Improved drought tolerance of transgenic Zea mays plants that express the glutamate dehydrogenase gene (gdhA) of E. coli. Euphytica 156:103–116CrossRefGoogle Scholar
  110. Limami AM, Rouillon C, Glevarec G, Gallais A, Hirel B (2002) Genetic and physiological analysis of germination efficiency in maize in relation to N metabolism reveals the importance of cytosolic glutamine synthetase. Plant Physiol 130:1860–1870PubMedPubMedCentralCrossRefGoogle Scholar
  111. Lisec J, Römish-Margi L, Nikoloski Z, Piepho HP, Giavalisco P, Selbig J, Gierl A, Willmitzer L (2011) Corn hybrids display lower metabolite variability and complex inheritance patterns. Plant J 66:326–336CrossRefGoogle Scholar
  112. Liu GW, Sun AL, Li DQ, Athman A, Giliham M, Liu LH (2015a) Molecular identification and functional analysis of a maize (Zea mays) DUR3 homolog that transports urea with high affinity. Planta 241:861–874PubMedCrossRefGoogle Scholar
  113. Liu H, Niu H, Gonzalez-Portilla P, Zhou Z, Wang L, Zuo T, Qin C, Tai S, Jansen C, Shen Y, Lin H, Lee M, Ware D, Zhang Z, Lübberstedt T, Pan G (2015b) An ultra-high-density map as a community resource for dissecting the genetic basis of quantitative traits in maize. BMC Genomics 16:1078Google Scholar
  114. Lohaus G, Büker M, Hubman M, Soave C, Heldt H (1998) Transport of amino acids with special emphasis on the synthesis and transport in the Illinois low protein and Illinois high protein strains of maize. Planta 205:181–188CrossRefGoogle Scholar
  115. Luo B, Tang H, Liu H, Shunzong S, Zhang S, Wu L, Liu D, Gao S (2015) Mining for low-nitrogen tolerance genes by integrating meta-analysis and large-scale gene expression data from maize. Euphytica 206:117–131CrossRefGoogle Scholar
  116. Luo J (2015) Metabolite-based genome—wide association studies in plants. Curr Opin Plant Biol 24:31–38PubMedCrossRefGoogle Scholar
  117. Lupini A, Meracti F, Araniti F, Miller AJ, Sunseri F, Abenavoli MR (2016) NAR2.1/NRT2.1 functional interaction with NO3 and H+ fluxes in high-affinity nitrate transport in maize roots. Plant Physiol Biochem 102:107–114PubMedCrossRefGoogle Scholar
  118. Lupini A, Araniti F, Mauceri A, Princi MP, Sorgonà A, Sunseri F, Varanini Z, Abenavoli MR (2018) Coumarin enhances nitrate uptake in maize roots through modulation of plasma membrane H+ATPase activity. Plant Biol 20:390–398PubMedCrossRefGoogle Scholar
  119. Lv Y, Liang Z, Ge M, Qi W, Zhang T, Lin F, Peng Z, Zhao H (2016) Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize (Zea mays L.). BMC Genomics 17:350PubMedPubMedCentralCrossRefGoogle Scholar
  120. Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatou C, Balliau T, Valot B, Davanture M, Dubois F, Tercé-Laforgue T, Coque M, Gallais A, Gonzalez-Moro MB, Bethencourt L, Quilleré I, Habash DZ, Lea PJ, Charcosset A, Perez P, Murigneux A, Sakakibara H, Edwards KJ, Hirel B (2006) Two cytosolic glutamine synthetase isoforms of maize (Zea mays L.) are specifically involved in the control of grain production. Plant Cell 18:3252–3274PubMedPubMedCentralCrossRefGoogle Scholar
  121. McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotech J 10:1011–1025CrossRefGoogle Scholar
  122. McKenzie FC, Williams J (2015) Sustainable food production: constraints, challenges and choices by 2050. Food Secur 7:221–223CrossRefGoogle Scholar
  123. McNally SF, Hirel B, Gadal P, Mann AF, Stewart GR (1983) Glutamine synthetase in higher plants. Evidence for a specific isoform content related to their possible physiological role and their compartmentation within the leaf. Plant Physiol 72:22–25PubMedPubMedCentralCrossRefGoogle Scholar
  124. Mengel K, Robin P, Salsac L (1983) Nitrate reductase activity in shoots and roots of maize seedlings as affected by the form of nitrogen nutrition and the pH of the solution. Plant Physiol 71:618–622PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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 53:979–987PubMedCrossRefGoogle Scholar
  126. Moss B (2008) Water pollution in agriculture. Phil Trans Royal Soc Lond B 363:659–666CrossRefGoogle Scholar
  127. Muhitch MJ (2003) Distribution of the glutamine syntethase isozyme GSp1 in maize (Zea mays). J Plant Physiol 160:601–605PubMedCrossRefGoogle Scholar
  128. Nakabayashi R, Saito K (2015) Integrated metabolomics for abiotic stress response in plants. Curr Opin Plant Biol 24:10–16PubMedCrossRefGoogle Scholar
  129. Nazir M, Pandey R, Siddiqi TO, Ibrahim MM, Qureshi MI, Abraham G, Vengavasi K, Ahmad A (2016) Nitrogen-deficiency stress induces protein expression differentially in low-N tolerant and low-N sensitive maize genotypes. Front Plant Sci 7:298PubMedPubMedCentralCrossRefGoogle Scholar
  130. Nieder R, Benbi DK, Scherer HW (2011) Fixation and defixation of ammonium in soils: a review. Biol Fertil Soils 47:1–14CrossRefGoogle Scholar
  131. Nouri MZ, Ghaffari MR, Sobhanain H, Hajirezaei MR (2016) Proteomics approach for identification of nutrient deficiency related proteins in crop plants. In: Salekdeh GH (ed) Agricultural proteomics, vol 2. Springer, pp 177–201Google Scholar
  132. Oaks A (1994) Efficiency of nitrogen utilization in C3 and C4 cereals. Plant Physiol 106:407–414PubMedPubMedCentralCrossRefGoogle Scholar
  133. Obata T, Witt S, Lisec J, Palacios-Rojas N, Florez-Saraza I, Yousfi S, Araus JL, Cairns JE, Fernie AR (2015) Metabolite profile of maize leaves in drought, heat, and combined stress field trials reveal the relationship between metabolism and grain yield. Plant Physiol 169:2665–2683PubMedPubMedCentralGoogle Scholar
  134. O’Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Guttiérez RA (2016) Nitrate transport, sensing, and response in plants. Mol Plant 9:837–856PubMedCrossRefGoogle Scholar
  135. Oita A, Malik A, Kanemoto K, Geschke A, Nishijima S, Lenzen M (2016) Substantial nitrogen pollution embedded in international trade. Nat Geosc 9:111–115CrossRefGoogle Scholar
  136. Pan X, Hasan MM, Li Y, Liao C, Zheng H, Liu R, Li X (2015) Asymmetric transcriptomic signatures in the maize era under optimal- and low-nitrogen conditions at silking, and functional characterization of amino acid transporters ZmAAP4 and ZmVAAT3. J Exp Bot 66:6149–6166PubMedPubMedCentralCrossRefGoogle Scholar
  137. Parnell JJ, Berka R, Young HA, Sturino JM, Kang Y, Barnhart DM, DiLeo MV (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci 7:1110PubMedPubMedCentralCrossRefGoogle Scholar
  138. Pathak RR, Lochab S, Raghuram N (2011) Improving nitrogen-use efficiency. Comprehensive biotechnology, vol 4, pp 209–218CrossRefGoogle Scholar
  139. Peña PA, Quach T, Sato S, Ge Z, Nersesian N, Changa T, Dweikat I, Soundararajan M, Clemente TE (2017) Expression of the maize Dof1 transcription factor in wheat and sorghum. Front Plant Sci 8:434PubMedPubMedCentralCrossRefGoogle Scholar
  140. Plénet D, Lemaire G (1999) Relationships between dynamics of nitrogen uptake and dry matter accumulation in maize crops. Determination of critical N concentration. Plant Soil 216:65–82CrossRefGoogle Scholar
  141. Plett D, Bauman U, Schreiber A, Holtham L, Kalashyan E, Toubia J, Nau J, Beatty M, Rafalski A, Dhugga KS, Tester M, Garnett T, Kaiser BN (2015) Maize maintains growth in response to decreased nitrate supply through a highly dynamic and developmental stage-specific transcriptional response. Plant Biotech J 14:342–353CrossRefGoogle Scholar
  142. Plett D, Holtham L, Bauman U, Kalashyan E, Francis K, Enju A, Toubia J, Roessner U, Bacic A, Rafalski A, Dhugga KS, Tester M, Garnett T, Kaiser BN (2016) Nitrogen assimilation system in maize is regulated by developmental and tissue-specific mechanisms. Plant Mol Biol 92:293–312PubMedCrossRefGoogle Scholar
  143. Poorter H, Anten NSP, Marcelis LFM (2013) Physiological mechanisms in plant growth models: do we need a supra-cellular systems biology approach? Plant Cell Environ 36:1673–1690PubMedCrossRefGoogle Scholar
  144. Prinsi B, Espen L (2015) Mineral nitrogen source differently affect root glutamine synthetase isoforms and amino acid balance among organs in maize. BMC Plant Biol 15:96PubMedPubMedCentralCrossRefGoogle Scholar
  145. Raihan MS, Liu J, Huang J, Guo H, Pan Q, Yan J (2016) Multi-environment QTL analysis of grain morphology traits and fine mapping of a kernel-width QTL in Zheng58 x SK maize population. Theor Appl Genet 129:1465–1477PubMedCrossRefGoogle Scholar
  146. Reetz HF, Heffer P, Bruulsema TW (2015) 4R nutrient stewardship: a global framework for sustainable fertilizer management. In: Drechsel P, Heffer P, Magen H, Mikkelsen R, Wilchelns (eds) Managing water and fertilizer for sustainable agricultural intensification. International Fertilizer Industry Association (IFA), International Water Management Institute (IWMI), International Plant Nutrition Institute (IPNI), and International Potash Institute (IPI), Paris, France, Jan 2015, p 65Google Scholar
  147. Ren B, Dong S, Zhao B, Liu P, Zhang J (2017) Responses of nitrogen metabolism, uptake and translocation of maize to waterlogging at different growth stages. Front Plant Sci 8:1216PubMedPubMedCentralCrossRefGoogle Scholar
  148. Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339CrossRefGoogle Scholar
  149. Riedelsheimer C, Czedick-Eysenberg A, Grieder C, Lisec J, Technow F, Sulpice R, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012a) Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nature Genet 44:217–222PubMedCrossRefGoogle Scholar
  150. Riedelsheimer C, Lisec J, Czedick-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012b) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc Natl Acad Sci USA 109:8872–8887PubMedCrossRefGoogle Scholar
  151. Roach E, Duiker SW, Chopra S (2016) Soil management affects expression of genes involved in carbon and nitrogen metabolism in maize. Crop Sci 56:1841–1856CrossRefGoogle Scholar
  152. Sakakibara H, Kawabata S, Takahashi H, Hase T, Sugiyama T (1992) Molecular cloning of the family of glutamine synthetase genes from maize: expression of genes for glutamine synthetase and ferredoxin-dependent glutamate synthase in photosynthetic and non-photosynthetic tissues. Plant Cell Physiol 33:49–58Google Scholar
  153. Salvi S, Tuberosa R (2007) Cloning QTLs in Plants. In: Varshney RK, Tuberosa R (eds) Genomics-Assisted Crop Improvement. Springer, Dordrecht, The Netherlands, vol 1, pp 207–226Google Scholar
  154. Sangwan RS, Bourgeois Y, Brown S, Vasseur G. Sangwan-Norreel B (1992) Characterization of competent cells and early events of Agrobacterium-mediated genetic transformation in Arabidopsis thaliana. Planta 188: 439–456Google Scholar
  155. Schilmiller AL, Pichersky E, Last RL (2012) Taming the hydra of specialized metabolism: how systems biology and comparative approaches are revolutionizing plant biochemistry. Cur Opin Plant Biol 15:338–344CrossRefGoogle Scholar
  156. Schlüter U, Colmsee C, Scholtz U, Bräutigam A, Weber APM, Zellerhoff N, Bucher M, Fahnenstich H, Sonnewald U (2013) Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balance. BMC Genomics 14:442PubMedPubMedCentralCrossRefGoogle Scholar
  157. Schmidt RR, Miller P (1999) Polypeptides and polynucleotides relating to the and subunits of a glutamate dehydrogenase and methods of use. United States Patent no 5, 879, 941, Mar 9Google Scholar
  158. Seebauer JR, Moose SP, Fabbri BJ, Crossland LD, Below FE (2004) Amino acid metabolism in maize earshoots. Implications for assimilate preconditioning and nitrogen signaling. Plant Physiol 136:4326–4334PubMedPubMedCentralCrossRefGoogle Scholar
  159. Seebauer JR, Singletary GW, Krumpelman PM, Ruffo ML, Below FE (2010) Relationship of source and sink in determining kernel composition in maize. J Exp Bot 61:551–519PubMedPubMedCentralCrossRefGoogle Scholar
  160. Shachar-Hill Y (2013) Metabolic network flux analysis for engineering plant systems. Curr Opin Plant Biol 24:247–255Google Scholar
  161. Shen M, Broeckling CD, Chu EY, Ziegler G, Baxter IR, Prenni JE, Hoekenga OA (2013) Leveraging non-targeted metabolite profiling via statistical genomics. PLOS One 8:e5767CrossRefGoogle Scholar
  162. Simons M, Saha R, Amiour A, Kumar A, Guillard L, Clément G, Miquel M, Li Z, Mouille G, Lea PJ, Hirel B, Maranas CD (2014a) Assessing the metabolic impact of nitrogen availability using a compartmentalized maize leaf genome-scale model. Plant Physiol 166:1659–1674PubMedPubMedCentralCrossRefGoogle Scholar
  163. Simons M, Saha R, Guillard L, Clément G, Armengaud P, Cañas R, Maranas CD, Lea PJ, Hirel B (2014b) Nitrogen use efficiency in maize (Zea mays L.): from “omics” studies to metabolic modelling. J Exp Bot 65:5657–5671PubMedCrossRefGoogle Scholar
  164. Singh R, Pankaj Sahu P, Muthamilarasan M, Dhaka A, Prasad M (2017) Genomics-assisted breeding for improving stress tolerance of graminaceous crops to biotic and abiotic stresses: progress and prospects. In: Senthil-Kumar M (ed) Plant tolerance to individual and concurrent stresses. Springer, New Delhi, India, pp 59–81CrossRefGoogle Scholar
  165. Singh RP, Srivastava HS (1986) Increase in glutamate synthase (NADH) activity in maize seedlings in response to nitrate and ammonium nitrogen. Physiol Plant 66:413–416CrossRefGoogle Scholar
  166. Singletary GW, Doehlert DC, Wilson CM, Muhitch MJ, Below FE (1990) Response of enzymes and storage proteins of maize endosperm to nitrogen supply. Plant Physiol 94:858–864PubMedPubMedCentralCrossRefGoogle Scholar
  167. Sinha SK, Srinivasan R, Mandal PK (2015) MicroRNA-based approach to improve nitrogen use efficiency in crop plants. In: Rakshit A, Sigh AB, Sen A (eds) Nutrient use efficiency: from basic to advances, Springer, India, pp 221–235Google Scholar
  168. Sirohi G, Pandey B, Deveshwar P, Giri J (2016) Emerging trends in epigenetic regulation of nutrient deficiency response in plants. Mol Biotech 58:159–171CrossRefGoogle Scholar
  169. Skopelitis DS, Paranychiankis NV, Paschalidis KA, Plianokis ED, Delis ID, Yakoumakis DI, Kouvarakis A, Papadakis ED, Stephanou EG, Roubelakis-Angelakis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenase to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18:2767–2781PubMedPubMedCentralCrossRefGoogle Scholar
  170. Skopelitis DS, Paranychiankis NV, Kouvarakis A, Spyros A, Stephanou EG, Roubelakis-Angelakis KA (2007) The isoenzyme 7 of tobacco NADH-dependent glutamate dehydrogenase exhibits high deaminating and low aminating activity. Plant Physiol 145:1–9CrossRefGoogle Scholar
  171. Smith KA (2017) Changing views of nitrous oxide emissions from agricultural soil: key controlling processes and assessment at different spatial scales. Eur J Soil Sci 68:137–155CrossRefGoogle Scholar
  172. Song W, Wang B, Hauck AL, Dong X, Li J, Lai J (2016) Genetic dissection of maize seedling root system architecture traits using an ultra-high-density bin-map and recombinant inbred line population. J Int Plant Biol 58:266–279CrossRefGoogle Scholar
  173. Sorgonà A, Lupini A, Mercati F, Di Dio L, Sunseri F, Abenavoli MR (2011) Nitrate uptake along the maize primary root: an integrated physiological and molecular approach. Plant Cell Envir 34:1127–1140CrossRefGoogle Scholar
  174. Srivastava A, Kowalski GM, Callahan DL, Meikle PJ, Creek DJ (2016) Strategies for extending metabolomics studies with stable isotope labeling and fluxomics. Metabolites 6:32PubMedCentralCrossRefPubMedGoogle Scholar
  175. Su C, Wang W, Gong S, Zuo J, Li S, Xu S (2017) High density linkage map construction and mapping of yield DTLs in maize (Zea mays) using the genotyping-by-sequencing (GBS) technology. Front Plant Sci 8:706PubMedPubMedCentralCrossRefGoogle Scholar
  176. Sun CX, Li MQ, Gao XX, Liu LN, WU XF, Zhou JH (2016) Metabolic response of maize plants to multi-factorial abiotic stresses. Plant Biol 18:120–129PubMedCrossRefGoogle Scholar
  177. Swain EY, Rempelos L, Orr CH, Hall G, Chapman R, Almadni M, Stockdale EA, Kidd J, Leifert C, Cooper JM (2014) Optimizing nitrogen use efficiency in wheat and potatoes: interaction between genotypes and agronomic practices. Euphytica 199:119–136CrossRefGoogle Scholar
  178. Sweetlove LJ, Nielsen J, Fernie AR (2017) Engineering central metabolism—a grand challenge for plant biologists. Plant J 90:749–763PubMedCrossRefGoogle Scholar
  179. Tabuchi M, Abiko T, Yamaya T (2007) Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). J Exp Bot 58:2319–2327PubMedCrossRefGoogle Scholar
  180. Tercé-Laforgue T, Dubois F, Ferrario-Mery S, Pou de Crecenzo MA, Sangwan R, Hirel B (2004) Glutamate dehydrogenase of tobacco (Nicotiana tabacum L.) is mainly induced in the cytosol of phloem companion cells when ammonia is provided either externally or released during photorespiration. Plant Physiol 136:4308–4317PubMedPubMedCentralCrossRefGoogle Scholar
  181. Tercé-Laforgue T, Bedu M, Dargel-Graffin C, Dubois F, Gibon Y, Restivo FM, Hirel B (2013) Resolving the role of plant glutamate dehydrogenase: II. Physiological characterization of plants overexpressing individually or simultaneously the two enzyme subunits. Plant Cell Physiol 54:1634–1647CrossRefGoogle Scholar
  182. Tercé-Laforgue T, Clément G, Marchi L, Restivo FM, Lea PJ, Hirel B (2015) Resolving the role of plant NAD-glutamate dehydrogenase: III. Overexpressing individually or simultaneously the two enzyme subunits under salt stress induces changes in the leaf metabolic profile and increases plant biomass production. Plant Cell Physiol. 56:1918–1929PubMedCrossRefGoogle Scholar
  183. Thomsen HC, Erikson D, MØller IS, Schjoerring JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19:656–663PubMedCrossRefGoogle Scholar
  184. Todd J, Screen S, Crowley J, Peng J, Andersen S, Brown T, Qi Q, Fabbri B, Duff SMG (2008) Identification and characterization of four distinct asparagine synthetase (AsnS) genes in maize (Zea mays L.). Plant Sci 175:799–808CrossRefGoogle Scholar
  185. Tohge T, Scossa F, Fernie AR (2015) Integrative approaches to enhance understanding of plant metabolic pathway structure and regulation. Plant Physiol 169:1499–1511PubMedPubMedCentralGoogle Scholar
  186. Toubiana D, Xue W, Zhang N, Kremling K, Gur A, Pilosof S, Gibon Y Stitt M, Buckler ES, Fernie AR, Fait A (2016) Correlation based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays. Front Plant Sci 7:1022Google Scholar
  187. Trevisan S, Nonis A, Begheldo M, Manoli A, Palme K, Caporale G, Ruperti B, Quaggiotti S (2012) Expression and tissue-specific localization of nitrate-responsive miRNAs in roots of maize seedlings. Plant Cell Environ 35:1137–1155PubMedCrossRefGoogle Scholar
  188. Trevisan S, Manoli A, Ravazzolo L, Botton A, Pivato M, Masi A, Quagiotti S (2015) Nitrate sensing by the maize root apex transition zone: a merged transcriptomic and proteomic survey. J Exp Bot 66:3699–3715PubMedPubMedCentralCrossRefGoogle Scholar
  189. Trucillo Silva I, Abbaraju HKR, Fallis LP, Liu H, Lee M, Dhugga KS (2017) Biochemical and genetic analyses of N metabolism in maize testcross seedlings. Theor Appl Genet 130:1453–1466PubMedCrossRefGoogle Scholar
  190. Urano K, Kurihara Y, Seki M, Shinozaki K (2010) ‘Omics’ analysis of regulatory network in plant abiotic stresses. Curr Opin Plant Biol 13:132–138Google Scholar
  191. Uribelarrea M, Below FE, Moose SP (2004) Kernel composition and productivity of maize hybrids derived from the Illinois protein strains in response to variable nitrogen supply. Crop Sci 44:1593–1600CrossRefGoogle Scholar
  192. Valadier MH, Yoshida A, Grandjean O, Morin H, Kronenberger J, Boutet S, Raballand A, Hase T, Yoneyama T, Suzuki A (2008) Implication of the glutamine synthetase/glutamate synthase pathway in conditioning the amino acid metabolism in bundle sheath and mesophyll cells of maize. FEBS J 275:3193–3206PubMedCrossRefGoogle Scholar
  193. Verzeaux J, Alahmad A, Habbib H, Nivelle E, Roger D, Lacoux J, Decocq G, Hirel B, Catterou M, Spicher F, Dubois F, Duclercq J, TétuT (2016a) Cover crops prevent from deleterious effect of nitrogen fertilization on bacterial diversity by maintaining carbon concentration in plowed soil. Geoderma 281:49–57CrossRefGoogle Scholar
  194. Verzeaux J, Roger D, Lacoux J, Nivelle E, Adam C, Habbib H, Hirel B, Dubois F, TétuT (2016b) In winter wheat, no-till increases mycorrhizal colonization thus reducing the need for nitrogen fertilization. Agronomy 6:38CrossRefGoogle Scholar
  195. Verzeaux J, Hirel B, Dubois F, Lea PJ, TétuT (2017) Agricultural practices to improve nitrogen use efficiency through the use of arbuscular mycorrhizae: basic and agronomic aspects. Plant Sci 264:48–56PubMedCrossRefGoogle Scholar
  196. Wallace JG, Larsson SJ, Buckler ES (2014) Entering the second century of maize quantitative genetics. Heredity 112:30–38PubMedCrossRefGoogle Scholar
  197. Wang H, Loussaert DL (2015) Functional expression of yeast nitrate transporter (YNT1) and a nitrate reductase in maize. US patent 8975474 B2Google Scholar
  198. 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 Physiol Biochem 105:118–128PubMedCrossRefGoogle Scholar
  199. Wen W, Li K, Alseek S, Omranian N, Zhao L, Zhou Y, Xiao Y, Jin M, Yang N, Liu Florian A, Li W, Pan Q, Nikoloski Z, Yan J, Fernie AR (2015) Genetic determinants of the network of primary metabolism and their relationships to plant performance in a maize recombinant inbred line population. Plant Cell 27:1839–1856PubMedPubMedCentralCrossRefGoogle Scholar
  200. Wen Z, Tyerman SD, Dechorgnat J, Ovchinnikova E, Dhugga KS, Kaiser BN (2017) Maize NFP6 proteins are homologs of Arabidopsis CHL1 that are selective for both nitrate and chloride. Plant Cell. Scholar
  201. Widiez T, El Kafafi ES, Girin T, Berr A, Ruffel S, Krouk G, Vayssieres A, Shen WH, Coruzzi GM, Gojon A, Lepetit M (2011) High nitrogen insensitive 9(HNI9)-mediated systemic expression of root NO3 uptake is associated with changes in histone methylation. Proc Natl Acad Sci USA 108:13329–13334PubMedCrossRefGoogle Scholar
  202. Withers PJA, Neal C, Jarvie HP, Doody DG (2014) Agriculture and eutrophication: where do we go from here? Sustainability 6:5853–5875CrossRefGoogle Scholar
  203. Wuyts N, Dhondt S, Inzé D (2015) Measurment of plant growth in view of an integrative analysis of regulatory network. Curr Opin Plant Biol 25:90–97PubMedCrossRefGoogle Scholar
  204. Xu Z, Zhong S, Li X, Li W, Rothstein SJ, Zhang S, Bi YM, Xie C (2011) Genome-wide identification of microRNAs in response to low nitrate availability in maize leaves and roots. PLOS One 6:e28009PubMedPubMedCentralCrossRefGoogle Scholar
  205. Xu C, Ren Y, Jian Y, Guo Z, Zhang Y, Xie C, Fu J, Wang H, Wang G, Xu Y, Li P, Zou C (2017) Development of a maize 55 K SNP array with improved genome coverage for molecular breeding. Mol Breed 37:20PubMedPubMedCentralCrossRefGoogle Scholar
  206. Yanagisawa S (2004) Dof domain proteins: plant–specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391PubMedPubMedCentralCrossRefGoogle Scholar
  207. Yanagisawa S, Akiyama A, Kisaka H, Uschimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA 101:7833–7838PubMedCrossRefGoogle Scholar
  208. Yamaya T, Kusano M (2014) Evidence supporting distinct functions of three cytosolic glutamine synthetases and two NADH-glutamate synthases. J Exp Bot 19:5519–5525CrossRefGoogle Scholar
  209. Yan S, Du X, Wu F, Li L, Li C, Meng Z (2014) Proteomics insights into the basis of interspecific facilitation for maize (Zea mays) in faba bean (Vicia faba)/maize intercropping. J Proteom 109:111–124CrossRefGoogle Scholar
  210. Yang S, Wu J, Ziegler TE, Yang X, Zayed A, Rajani MS, Zhou D, Basra A, Schachtman D, Peng M, Armstrong CL, Caldo RA, Morrell JA, Lacy M, Staub JM (2011) Gene expression biomarkers provide sensitive indicators of in planta nitrogen status in maize. Plant Physiol 157:1841–1852PubMedPubMedCentralCrossRefGoogle Scholar
  211. Yesbergenova-Cuny Z, Dinant S, Martin-Magniette ML, Quillere I, Armengaud P, Monfalet P, Lea PJ, Hirel B (2016) Genetic variability of the phloem sap metabolite content of maize (Zea mays L.) during the kernel-filling period. Plant Sci 252:347–357PubMedCrossRefGoogle Scholar
  212. York LM, Silberbush M, Lynch JP (2016) Spatiotemporal variation of nitrate uptake kinetics within the maize (Zea mays L.) root system is associated with greater nitrate uptake and interactions with architectural phenes. J Exp Bot 67:3763–3775PubMedCrossRefGoogle Scholar
  213. Yu P, White P, Hochlodinger F, Li C (2014) Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta 240:667–768CrossRefGoogle Scholar
  214. Yuan L, Loqué D, Kojima S, Rauch S, Ishimaya K, Inoue E, Takahashi H, von Wirén N (2007) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19:2636–2652PubMedPubMedCentralCrossRefGoogle Scholar
  215. Yuan S, Li Z, Li D, Yuan N, Hu Q, Luo H (2015) Constitutive overexpression of rice MicroRNA528 alters plant development and enhances tolerance to salinity stress and nitrogen starvation in creeping bentgrass. Plant Physiol 169:576–593PubMedPubMedCentralCrossRefGoogle Scholar
  216. Zamboni A, Astlfi S, Zuchi S, Pii Y, Guradini K, Tonomi P, Varanini Z (2014) Nitrate induction triggers different transcriptional changes in a high and low nitrogen use efficiency maize inbred line. J Integr Plant Biol 56:1080–1094PubMedCrossRefGoogle Scholar
  217. Zanin L, Zamboni A, Monte R, Tomasi N, Varanini Z, Cesco S, Pinton R (2015) Transcriptomic analysis highlights the reciprocal interactions of urea and nitrate for nitrogen acquisition by maize roots. Plant cell Physiol 56:532–548PubMedCrossRefGoogle Scholar
  218. Zeng DD, Qin R, Li M, Alamin Md, Jin KL, Liu Y, Shi CH (2017) The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and nitrogen remobilization in rice. Mol Genet Genom 292:385–395CrossRefGoogle Scholar
  219. Zhang N, Gibon Y, Wallace JG, Lepak N, Li P, Dedow L, Chen C, So YS, Kremling K, Bradbury PJ, Brutnell T, Stitt M, Buckler ES (2015) Genome-wide association of carbon and nitrogen in the maize nested association mapping population. Plant Physiol 168:575–583PubMedPubMedCentralCrossRefGoogle Scholar
  220. Zhao M, Tai H, Sun S, Zhang F, Xu Y, Li WX (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLOS One 7:e29669PubMedPubMedCentralCrossRefGoogle Scholar
  221. Zhou X, Lin J, Zhou Y, yang Y, Liu H, Zhang C, Tang D, Zhao X, Zhu Y, Liu X (2015) Overexpressing a fungal CeGDH gene improves nitrogen utilization and growth in rice. Crop Sci 55:811–820Google Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Adaptation des Plantes à Leur EnvironnementUnité Mixte de Recherche 1318, Institut Jean-Pierre Bourgin, Institut National de La Recherche Agronomique, Centre de Versailles-GrignonVersailles CedexFrance
  2. 2.Lancaster Environment CentreLancaster UniversityLancasterUK

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