Strategies for Identification of Genes Toward Enhancing Nitrogen Utilization Efficiency in Cereals

  • Alka Bharati
  • Pranab Kumar Mandal


Global cereal demand will increase up to 38% by 2025, and to achieve it in a sustainable way, 60% increase in global nitrogen (N) use will be necessary. In cereals ~30 to 50% of the applied N is taken up by the crop, and the rest is lost in the environment causing pollution. Hence, improvement of N use efficiency (NUE) in cereals is really important. The NUE is the total biomass or grain yield produced per unit of applied N fertilizer. Soil and plant management practices play a key role toward enhancing N recovery, but again it greatly depends on environmental conditions. Another option for improvement of NUE is the genetic strategy. Broadly, NUE has two components, N uptake efficiency (NUpE), which is N acquisition by the plant per unit of available N in the soil, and N utilization efficiency (NUtE), which is yield per unit of acquired N by the plant. As NUtE is directly related to the crop yield, it depends on subcomponent N assimilation, remobilization, and finally efficient utilization of assimilated N for starch biosynthesis in the grain. Understanding the mechanisms and gene regulating of these processes, exploiting genotypic variant in each subcomponent (N uptake, assimilation, and remobilization) to find genes and superior alleles is crucial for the improvement of NUE in crop plants. In addition, the studies on starch metabolism during grain filling are an important factor for N utilization. To study this, genotypes with similar background of uptake and assimilation but differing in grain filling should be taken into consideration. Global metabolomic profiling of these genotypes, transcriptome profiling, identification, and mapping of quantitative trait loci (QTLs) in combination with marker-assisted selection (MAS), analyzing mutants defective in their normal response to N limitation, and studying plants that show better growth under N-limiting conditions are different options to study the N-utilization efficiency and gene identification. In the first topic, we have highlighted the N application and its effect on yield in cereals. Introduction of N-responsive genotype during green revolution has enhanced yield, but indiscriminate use of fertilizer mainly N fertilizer has caused severe damage to environment. In the subsequent topic, we have defined NUE as a whole; later the main focus was on biological NUE and their different components. Thereafter we described strategies for genetic improvement to reduce N use without much compromising yield. Primarily we tried to highlight candidate genes and their role in NUE reported in cereals as well as model plant system. We have also described the advance molecular techniques to identify the gene in strategic manner. As a part of molecular breeding, QTL identification and its introgression are described in one of the topics at the last part.


Candidate genes Cereals Nitrogen use efficiency 



Amino acid permease


Abscisic acid


Adenosine diphosphate


Agronomic efficiency


Auxin signaling F-box


ADP glucose pyrophosphorylase


Alanine aminotransferase


Ammonium transporter


Apparent recovery efficiency


Asparagine synthase


Amino acid transporter


Branching enzyme


Biological nitrogen fixation




Cauliflower mosaic virus


Complimentary DNA


Candidate genes


Chloride channel family


Carbamoyl phosphate synthase


Clustered regularly interspaced short palindromic repeats


Deoxyribonucleic acid


DNA binding with one zinc finger


Ethyl methanesulfonate




Granule-bound starch synthase


Glutamate dehydrogenase


GDP mannose pyrophosphorylase


Glutamine-2-oxoglutarate aminotransferase or glutamate synthase


Glutamine synthetase




High-affinity transport system


Hypersensitive to \( {\mathrm{NH}}_4^{+} \)


High-yielding varieties




Low-affinity transport


Lysine/histidine transporter


Marker-assisted selection


micro RNA


Massively parallel signature sequencing


Metabolic QTLs




Nitrogen oxide


Nicotinamide adenine dinucleotide phosphate


N-acetyl glutamate kinase




Near-isogenic lines


Nitrite reductase


Nitric oxide

\( {\mathrm{NO}}_3^{-} \)



Peptide transporter family


N physiological use efficiency


\( {\mathrm{NO}}_3^{-} \) reductase


\( {\mathrm{NO}}_3^{-} \) reductase activity


\( {\mathrm{NO}}_3^{-} \) transporter


Nitrogen use efficiency


N uptake efficiency


N utilization efficiency


Partial factor productivity


Phosphoenolpyruvate carboxylase


Partial nutrient balance


Protein targeting to starch


Quantitative trait loci


Ribonucleic acid


RNA interference


Root system


Root system architecture


Serial analysis of gene expression


Senescence associated vacuoles


Soluble starch branching enzymes


Starch granules


Slow anion-associated channel homolog


Starch synthase


Suppression subtractive hybridization


Transfer DNA


Transcription activator-like effector nucleases


Tricarboxylic acid


Tonoplast intrinsic protein


Target of rifampicin


Usage index


Water use efficiency


Zinc finger nucleus


  1. Barbier-Brygoo H, DeAngeli A, Filleur S, Frachisse JM, Gambale F, Thomine S et al (2011) Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu Rev Plant Biol 62:25–51CrossRefPubMedGoogle Scholar
  2. Beman JM, Arrigo K, Matson PM (2005) Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean. Nature 434:211–214CrossRefGoogle Scholar
  3. Bordes J, Ravel C, Jaubertie JP, Duperrier B, Gardet O et al (2013) Genomic regions associated with the N limitation response revealed in a global wheat core collection. Theor Appl Genet 126:805–822CrossRefPubMedGoogle Scholar
  4. Breiman A, Graur D (1995) Wheat evolution. Isr J Plant Sci 43:85–98CrossRefGoogle Scholar
  5. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D et al (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on micro bead arrays. Nat Biotechnol 18:630–634CrossRefPubMedGoogle Scholar
  6. Bussi C, Gojon A, Passama L (1997) In situ nitrate reductase activity in leaves of adult peach trees. J Hortic Sci 72:347–353CrossRefGoogle Scholar
  7. Castaings L, Camargo A, Pocholle D et al (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435CrossRefPubMedGoogle Scholar
  8. Chopin F, Orsel M, Dorbe MF, Chardon F, Truong HN et al (2007) The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. Plant Cell 19:1590–1602CrossRefPubMedPubMedCentralGoogle Scholar
  9. Conant RT, Berdanier AB, Grace PR (2013) Patterns and trends in N use and N recovery efficiency in world agriculture. Glob Biogeochem Cycles 27:558–566CrossRefGoogle Scholar
  10. Deprost D, Yao L, Sormani R et al (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–870CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dobermann A (2005) Nutrient use efficiency – state of the art. In: IFA International Workshop on Enhanced-Efficiency Fertilizers. International Fertilizer Industry Association (IFA), Frankfurt/Paris, pp 1–16Google Scholar
  12. Dobermann A (2007) Nutrient use efficiency – measurement and management. In: Fertilizer best management practices. General principles, strategy for their adoption and voluntary initiatives vs regulations. IFA International Workshop on Fertilizer Best Management Practices. International Fertilizer Industry Association (IFA), Brussels; Paris, pp 1–28Google Scholar
  13. Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New YorkGoogle Scholar
  14. Fageria NK, Baligar VC, Li YC (2008) The role of nutrient efficient plants in improving crop yields in the twenty first century. J Plant Nutr 31:1121–1157CrossRefGoogle Scholar
  15. FAO (2015) Current world fertilizer trends and outlook to 2015. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  16. Feng HM, Yan M, Fan XR, Li BZ, Shen QR et al (2011) Spatial expression and regulation of rice high-affinity nitrate transporters by N and carbon status. J Exp Bot 62:2319–2332CrossRefGoogle Scholar
  17. Ferrario-Mery S, Valadier M, Foyer C (1998) Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA. Plant Physiol 117:293–302CrossRefPubMedPubMedCentralGoogle Scholar
  18. Ferrario-Mery S, Besin E, Pichon O, Meyer C, Hodges M (2006) The regulatory PII protein controls arginine biosynthesis in Arabidopsis. FEBS Lett 580:2015–2020CrossRefPubMedGoogle Scholar
  19. Fischer KS (2000) Frontier project on N fixation in rice: looking ahead. In: Ladha JK, Reddy PM (eds) The quest for N fixation in rice. International Rice Research Institute, Los Banos, pp 25–31Google Scholar
  20. Fixen P, Brentrup F, Bruulsema TW, Garcia F, Norton R, Zingore S (2015) Nutrient/fertilizer use efficiency: measurement, current situation and trends. In: Drechsel P, Heffer P, Magen H, Mikkelsen R, Wichelns D (eds) Managing water and fertilizer for sustainable agricultural intensification. Copyright 2015 IFA, IWMI, IPNI and IPI, Paris, pp 8–38Google Scholar
  21. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation and signalling. J Exp Biol 58:2339–2358Google Scholar
  22. Foyer CH, Noctor G, Hodges M (2011) Respiration and N assimilation: targeting mitochondria associated metabolism as a means to enhance N use efficiency. J Exp Bot 62:1467–1482CrossRefPubMedGoogle Scholar
  23. Gallais A, Hirel B (2004) An approach to the genetics of N use efficiency in maize. J Exp Bot 55:295–306CrossRefPubMedGoogle Scholar
  24. Galvan A, Quesada A, Fernandez E (1996) The use of mutants to study nitrate assimilation in green microalgae. Sci Mar 60:191–194Google Scholar
  25. Garnett T, Conn V, Plett D, Conn S, Zanghellini J, Mackenzie N et al (2013) The response of the maize nitrate transport system to N demand and supply across the lifecycle. New Phytol 198:82–94CrossRefGoogle Scholar
  26. Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wiren N (1999) Three functional transporters for constitutive, diurnally regulated, and starvation induced uptake of ammonium into Arabidopsis roots. Plant Cell 11:937–947CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gniazdowska A, Mikulska M, Rychter AM (1998) Growth, nitrate uptake and respiration rate in bean roots under phosphate deficiency. Biol Plant 41:217–226CrossRefGoogle Scholar
  28. Gniazdowska-Skoczek H (1997) Properties of nitrate reductase from seedling leaves of selected barley genotypes. Acta Physiol Plant 19:137–145CrossRefGoogle Scholar
  29. GOI (2012) Press information bureau, government of India. Ministry of Agriculture & Farmers Welfare.
  30. Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9:597–605CrossRefPubMedGoogle Scholar
  31. Habash DZ, Massiah AJ, Rong HI, Wallsgrove RM, Leigh RA (2001) The role of cytosolic glutamine synthetase in wheat. Ann Appl Biol 138:83–89CrossRefGoogle Scholar
  32. Habash DZ, Bernard S, Schondelmaier J, Weyen J, Quarrie SA (2007) The genetics of N use in hexaploid wheat: N utilisation, development and yield. Theor Appl Genet 114:403–419CrossRefPubMedGoogle Scholar
  33. Han M, Okamoto M et al (2015) The genetics of N use efficiency in crop. Plants Annu Rev Genet 49:269–289CrossRefPubMedGoogle Scholar
  34. Heidlebaugh NM, Trethewey BR, Jukanti AK, Parrott DL, Martin JM, Fischer AM (2008) Effects of a barley (Hordeum vulgare) chromosome 6 grain protein content locus on whole-plant N reallocation under two different fertilisation regimes. Funct Plant Biol 35:619–632CrossRefGoogle Scholar
  35. Hill C, Taylor J, Edwards J, Mather D (2013) Whole-genome mapping of agronomic and metabolic traits to identify novel quantitative trait loci in bread wheat grown in a water-limited environment. Plant Physiol 162:1266–1281CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving N use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387CrossRefPubMedGoogle Scholar
  37. Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194CrossRefGoogle Scholar
  39. Hoque MS, Masle J, Udvardi MK, Ryan PR, Upadhyaya NM (2006) Over-expression of the rice OsAMT1-1 gene increases ammonium uptake and content, but impairs growth and development of plants under high ammonium nutrition. Funct Plant Biol 33:153–163CrossRefGoogle Scholar
  40. Huang NC, Liu KH, Lo HJ, Tsay YF (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11:1381–1392CrossRefPubMedPubMedCentralGoogle Scholar
  41. Janssen BH, Guiking FCT, Van Der Eijk D, Smaling EMA, Wolf J, Reuler H (1990) A system for quantitative evaluation of the fertility of tropical soils (QUEFTS). Geoderma 46:299–318CrossRefGoogle Scholar
  42. Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M et al (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci 109:9653–9658CrossRefPubMedGoogle Scholar
  43. Katagiri F, Glazebrook J (2009) Overview of mRNA expression profiling using DNA microarrays. Curr Protoc Mol Biol 22:22Google Scholar
  44. Katayama H, Mori M, Kawamura Y, Tanaka T, Mori M, Hasegawa H (2009) Production and characterization of transgenic rice plants carrying a high-affinity nitrate transporter gene (OsNRT2.1). Breed Sci 59:237–243CrossRefGoogle Scholar
  45. Kearsey MJ, Farquhar AGL (1998) QTL analysis in plants; where are we now? Heredity 80:137–142CrossRefPubMedGoogle Scholar
  46. Koch W, Kwart M, Laubner M, Heineke D, Stransky H, Frommer WB, Tegeder M (2003) Reduced amino acid content in transgenic potato tubers due to antisense inhibition of the leaf H+/amino acid symporter StAAP1. Plant J 33:211–220CrossRefPubMedGoogle Scholar
  47. Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince AS et al (2014) Nitrate transport and signaling in Arabidopsis. J Exp Bot 65:789–798CrossRefPubMedGoogle Scholar
  48. Kronzucker H, Glass ADM, Siddiqi MY (1995) Nitrate induction in spruce: an approach using compartmental analysis. Planta 196:683–690CrossRefGoogle Scholar
  49. Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoki N, Ohsugi R (2011) Introduction of the ZmDof1 gene into rice enhances carbon and N assimilation under low-N conditions. Plant Biotechnol J 9:826–837CrossRefPubMedGoogle Scholar
  50. Ladha JK, Chakraborty D (2016) Solutions to improve N use efficiency for the world. In: Proceedings of the international N initiative conference, pp 4–8. December 2016, Melbourne, AustraliaGoogle Scholar
  51. Ladha JK et al (2016) Agronomic improvements can make future cereal systems in South Asia far more productive and result in lower environmental footprint. Glob Chang Biol 22:1054–1074CrossRefPubMedGoogle Scholar
  52. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM (1996) The molecular-genetics of N assimilation into amino acids in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:569–593CrossRefPubMedGoogle Scholar
  53. Lam HM, Wong P, Chan HK et al (2003) Overexpression of the ASN1 gene enhances N status in seeds of Arabidopsis. Plant Physiol 132:926–935CrossRefPubMedPubMedCentralGoogle Scholar
  54. Laperche A, Brancourt-Hulmel M, Heumez E, Gardet O, Hanocq E et al (2007) Using genotype × N interaction variables to evaluate the QTL involved in wheat tolerance to N constraints. Theor Appl Genet 115:399–415CrossRefPubMedGoogle Scholar
  55. Lassaletta L, Billen G, Grizzetti B, Anglade J Garnier J (2014) 50 year trends in N use efficiency of world cropping systems: the relationship between yield and N input to cropland. Environ Res Lett 9:105011CrossRefGoogle Scholar
  56. Lea PJ (1993) N metabolism. In: Lea PJ, Leegood RC (eds) Plant biochemistry and molecular biology. Wiley, New York, pp 155–180Google Scholar
  57. Lea PJ, Miflin B (1980) Transport and metabolism of asparagine and other N compounds within the plant, vol 40, pp 569–607Google Scholar
  58. Lea PJ, Robinson SA, Stewart GR (1990) The enzymology and metabolism of glutamine, glutamate, and asparagine. In: Miflin BJ, Lea PJ (eds) The biochemistry of plants, vol 16. Academic, New York, pp 121–159Google Scholar
  59. Lee YH, Foster J, Chen J, Voll LM, Weber AP, Tegeder M (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J 50:305–319CrossRefPubMedGoogle Scholar
  60. Léran S, Varala K, Boyer JC, Chiurazzi M, Crawford N, Daniel-Vedele F et al (2014) A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19:5–9CrossRefPubMedGoogle Scholar
  61. Léran S, Edel KH, Pervent M, Hashimoto K, Corratge-Faillie C, Offenborn JN et al (2015) Nitrate sensing and uptake in Arabidopsis are ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci Signal 8:43. CrossRefGoogle Scholar
  62. Li XZ, Oaks A (1994) Induction and turnover of nitrate reductase in Zea mays: influence of light. Plant Physiol 106:1145–1149CrossRefPubMedPubMedCentralGoogle Scholar
  63. Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y et al (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646CrossRefPubMedPubMedCentralGoogle Scholar
  64. Lima JE, Kojima S, Takahashi H, von Wiren N (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22:3621–3633CrossRefPubMedPubMedCentralGoogle Scholar
  65. Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK et al (2008) Mutation of the Arabidopsis NRT1.5nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528CrossRefPubMedPubMedCentralGoogle Scholar
  66. Liu HS, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005–1013CrossRefPubMedPubMedCentralGoogle Scholar
  67. Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–874CrossRefPubMedPubMedCentralGoogle Scholar
  68. Liu R, Zhang H, Zhao P, Zhang Z, Liang W et al (2012) Mining of candidate maize genes for N use efficiency by integrating gene expression and QTL data. Plant Mol Biol Rep 30:297–308CrossRefGoogle Scholar
  69. London JG (2005) N study fertilizes fears of pollution. Nature 433:791CrossRefGoogle Scholar
  70. Loque D, Ludewig U, Yuan L, von Wiren N (2005) Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol 137:671–680CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lupini A, Mercati 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 root regions. Plant Physiol Biochem 102:107–114CrossRefPubMedGoogle Scholar
  72. Manske GG, Vlek PL (2002) Root architecture–wheat as a model plant. In: Waisel Y, Eshel A, Beeckman T, Kafkafi U (eds) Roots: the hidden half. CRC, Boca Raton, pp 249–259CrossRefGoogle Scholar
  73. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, LondonGoogle Scholar
  74. Marwaha RS (1998) Nitrate assimilation in potato cultivars during plant growth. Indian J Plant Physiol 3:147–151Google Scholar
  75. Masclaux-Daubresse C, Reisdorf-Cren M, Pageau K et al (2006) Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source N cycle in tobacco. Plant Physiol 140:444–456CrossRefPubMedPubMedCentralGoogle Scholar
  76. Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M (2008) Leaf N remobilisation for plant development and grain filling. Plant Biol 10:23–36CrossRefPubMedGoogle Scholar
  77. Meyer C, Stitt M (2001) Plant N. In: Lea PJ, Goudry JFM (eds) Nitrate reduction and signaling. Springer, Berlin/Heidelberg, pp 37–59Google Scholar
  78. Miflin BJ, Lea PJ (1976) The pathway of N assimilation in plants. Phytochemistry 15:873–885CrossRefGoogle Scholar
  79. Miflin BJ, Lea PJ (1980) Ammonia assimilation. In: Miflin BJ (ed) The biochemistry of plants: amino acids and derivatives, vol 5. Academic, New York, pp 169–202CrossRefGoogle Scholar
  80. Mistrik I, Ullrich CI (1996) Mechanism of anion uptake in plant roots: quantitative evaluation of H+/NO3− and H+/H2PO4− stoichiometries. Plant Physiol Biochem 34:629–636Google Scholar
  81. Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of N utilisation. Agronomy 74:562–564CrossRefGoogle Scholar
  82. Mosier A, Syers JK (2004) Agriculture and the N cycle: assessing the impacts of fertilizer use on food production and the environment, vol 65. Island Press, Washington, DCGoogle Scholar
  83. Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M et al (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483–486CrossRefPubMedGoogle Scholar
  84. Obara M, Kajiura M, Fukuta Y, Yano M, Hayashi M et al (2001) Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). J Exp Bot 52:1209–1217PubMedGoogle Scholar
  85. Oliveira IC, Coruzzi GM (1999) Carbon and amino acids reciprocally modulate the expression of glutamine synthetase in Arabidopsis. Plant Physiol 121:301–310CrossRefPubMedPubMedCentralGoogle Scholar
  86. Oliveira IC, Brears T, Knight TJ, Clark A, Coruzzi GM (2002) Overexpression of cytosolic glutamate synthetase. Relation to N, light, and photorespiration. Plant Physiol 129:1170–1180CrossRefPubMedPubMedCentralGoogle Scholar
  87. Orsel M, Filleur S, Fraisier V, Daniel-Vedele F (2002a) Nitrate transport in plants: which gene and which control? J Exp Bot 53(370):825–833CrossRefPubMedGoogle Scholar
  88. Orsel M, Krapp A, Daniel-Vedele F (2002b) Analysis of the NRT2 nitrate transporter family in Arabidopsis. Structure and gene expression. Plant Physiol 129:886–896CrossRefPubMedPubMedCentralGoogle Scholar
  89. Orsel M, Chopin F, Leleu O, Smith SJ, Krapp A, Daniel-Vedele F, Miller AJ (2006) Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein protein interaction. Plant Physiol 142(3):1304–1317CrossRefPubMedPubMedCentralGoogle Scholar
  90. Pajuelo PE, Pajuelo B, Forde G, Marquez AJ (1997) Regulation of the expression of ferredoxin-glutamate synthase in barley. Planta 203:517–525CrossRefPubMedGoogle Scholar
  91. Pathak H, Aggarwal PK, Roetter R, Kalra N, Bandyopadhaya SK, Prasad S, Keulen HV (2003) Modeling the quantitative evaluation of soil nutrient supply, nutrient use efficiency, and fertilizer requirements of wheat in India. Nutr Cycl Agroecosyst 65:105–113CrossRefGoogle Scholar
  92. Pathak RR, Ahmad A, Lochab S, Raghuram N (2009) Molecular physiology of plant N use efficiency and biotechnological options for its enhancement. Curr Sci 94:1394–1403Google Scholar
  93. Peña PA, Quach T, Sato S et al (2017) Expression of the maize Dof1 transcription factor in wheat and sorghum. Front Plant Sci 8:434. CrossRefPubMedPubMedCentralGoogle Scholar
  94. Peoples MB, Gifford RM (1993) Plant physiology, biochemistry and molecular biology. In: Dennis DT, Turpin DH (eds) Long distance transport of carbon and N from sources to sinks in higher plants. Wiley, New York, pp 434–447Google Scholar
  95. Peterman TK, Goodman HM (1991) The glutamine synthetase gene family of Arabidopsis thaliana: light regulation and differential expression in leaves, roots and seeds. Mol Gen Genet 230:145–154CrossRefPubMedGoogle Scholar
  96. Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci 73:2781–2807CrossRefPubMedPubMedCentralGoogle Scholar
  97. Potel F, Valadier MH, Ferrario-Mery S et al (2009) Assimilation of excess ammonium into amino acids and N translocation in Arabidopsis thaliana – roles of glutamate synthases and carbamoylphosphate synthetase in leaves. FEBS J 276:4061–4076CrossRefPubMedGoogle Scholar
  98. Powlson DS, Addiscott TM, Benjamin N, Cassman KG, DeKok TM (2008) When does nitrate become a risk for humans? J Environ Qual 37:291–295CrossRefGoogle Scholar
  99. Qin C, Qian W, Wang W, Wu Y, Yu C et al (2008) GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proc Natl Acad Sci U S A 105:18308–18313CrossRefPubMedPubMedCentralGoogle Scholar
  100. Rabalais NN, Turner RE, Wiseman WJ (2002) Gulf of Mexico hypoxia, aka “the dead zone.”. Annu Rev Ecol Syst 33:235–263CrossRefGoogle Scholar
  101. Raghuram N, Sachdev MS, Abrol YP (2007) Towards an integrative understanding of reactive N. In: Agricultural N use and its environmental implications, pp 1–6Google Scholar
  102. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E et al (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci 103:19206–19211CrossRefPubMedGoogle Scholar
  103. Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic N compounds in plants. FEBS Lett 581:2281–2289CrossRefPubMedGoogle Scholar
  104. Robertson A (1967) The nature of quantitative genetic variation. In: Brink R (ed) Heritage from Mende, Univ. Wisc. E Styles. University of Wisconsin Press, Madison, pp 265–280Google Scholar
  105. Robertson GP, Vitousek PM (2009) N in agriculture: balancing the cost of an essential resource. Annu Rev Environ Resour 34:97–125CrossRefGoogle Scholar
  106. Rochat C, Boutin JP (1991) Metabolism of phloem-borne amino acids in maternal tissues of fruit of nodulated or nitrate-fed pea plants (Pisum sativum L.). J Exp Bot 42:207–214CrossRefGoogle Scholar
  107. Roche D, Temple SJ, Sengupta GC (1993) Two classes of differentially regulated glutamine synthetase genes are expressed in the soybean nodule: a nodule specific and a constitutively expressed class. Plant Mol Biol 22:971–983CrossRefPubMedGoogle Scholar
  108. Roldán I, Wattebled F, Mercedes Lucas M, Delvallé D, Planchot V, Jiménez S, Pérez R et al (2007) The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J 49:492–504CrossRefPubMedGoogle Scholar
  109. Rounsley SD, Glodek A, Sutton G, Adams MD, Somerville CR, Venter JC et al (1996) The construction of Arabidopsis expressed sequence tag assemblies. A new resource to facilitate gene identification. Plant Physiol 112:1177–1183CrossRefPubMedPubMedCentralGoogle Scholar
  110. Segonzac C, Boyer JC, Ipotesi E, Szponarski W, Tillard P, Touraine B et al (2007) Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. Plant Cell 19:3760–3777CrossRefPubMedPubMedCentralGoogle Scholar
  111. Seung D, Boudet J, Monroe J, Schreier TB, David LC et al (2017) Homologs of protein targeting to starch control starch granule initiation in Arabidopsis leaves. Plant Cell 29:1657–1677CrossRefPubMedPubMedCentralGoogle Scholar
  112. Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG (2008) Genetic engineering of improved N use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol J 6:722–732CrossRefPubMedGoogle Scholar
  113. Sivasankar S, Rothstein S, Oaks A (1997) Regulation of the accumulation and reduction of nitrate by N and carbon metabolites in maize seedlings. Plant Physiol 114:583–589CrossRefPubMedPubMedCentralGoogle Scholar
  114. Skopelitis D, Paranychianakis N, Paschalidis K, Pliakonis E, Delis I, Yakoumakis D, Kouvarakis A, Papadakis A, Stephanou E, Roubelakis-Anfelakis K (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18(10):2767–2781CrossRefPubMedPubMedCentralGoogle Scholar
  115. Sonoda Y, Ikeda A, Saiki S, Yamaya T, Yamaguchi J (2003) Feedback regulation of the ammonium transporter gene family AMT1 by glutamine in rice. Plant Cell Physiol 44:1396–1402CrossRefPubMedGoogle Scholar
  116. Stewart GR, Mann AF, Fentem PA (1980) Enzymes of glutamate formation: glutamate dehydrogenase, glutamine. In: Miflin BJ (ed) The biochemistry of plants: comprehensive treatise, vol. 5. Amino acids and derivatives. Academic, New York, pp 271–327Google Scholar
  117. Sulpice R, Pyl ET, Ishihara H, Trenkamp S, Steinfath M et al (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci 106:10348–10353CrossRefPubMedGoogle Scholar
  118. Svennerstam H, Ganeteg U, Nasholm T (2008) Root uptake of cationic amino acids by Arabidopsis depends on functional expression of amino acid permease 5. New Phytol 180:620–630CrossRefPubMedGoogle Scholar
  119. Taochy C, Gaillard I, Ipotesi E, Oomen R, Leonhardt N, Zimmermann S et al (2015) The Arabidopsis root stele transporter NPF2.3 contributes to nitrate translocation to shoots under salt stress. Plant J 83:466–447CrossRefGoogle Scholar
  120. Taylor L, Nunes-Nesi A, Parsley K, Leiss A, Leach G, Coates S, Wingler A, Fernie AR, Hibberd JM (2010) Cytosolic pyruvate, orthophosphatedikinase functions in N remobilization during leaf senescence and limits individual seed growth and N content. Plant J 62(4):642–652CrossRefGoogle Scholar
  121. Tilsner J, Kassner N, Struck C, Lohaus G (2005) Amino acid content and transport in oilseed rape (Brassica napus L.) under different N conditions. Planta 221:328–338CrossRefPubMedGoogle Scholar
  122. Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1of Arabidopsis encodes anitrate-inducible nitrate transporter. Cell 72:705–713CrossRefGoogle Scholar
  123. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290–2300CrossRefPubMedGoogle Scholar
  124. Uauy C, Brevis JC, Dubcovsky J (2006) The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. J Exp Bot 57:2785–2794CrossRefPubMedGoogle Scholar
  125. Ullrich WR (1987) Nitrate and ammonium uptake in green algae and higher plants: mechanism and relationship with nitrate metabolism. In: Ullrich WR, Aparicio PJ, Syrett PJ, Castillo F (eds) Inorganic N metabolism. Springer, Berlin/Heidelberg/New York, pp 32–38CrossRefGoogle Scholar
  126. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487CrossRefPubMedGoogle Scholar
  127. Vidal EA, Araus V, Lu C, Parry G, Green PJ et al (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci 107:4477–4482CrossRefPubMedGoogle Scholar
  128. Walch-Liu P, Forde BG (2008) Nitrate signaling mediated by the NRT1.1 nitrate transporter antagonizes l-glutamate-induced changes in root architecture. Plant J 54:820–828CrossRefPubMedGoogle Scholar
  129. Wang R, Liu D, Crawford NM (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci 95:15134–15139CrossRefPubMedGoogle Scholar
  130. Wang Z, Gartein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63CrossRefPubMedPubMedCentralGoogle Scholar
  131. Wang H et al (2013) Regulating effect of N fertilization on grain filling and activities of enzymes involved in starch synthesis of Yumai49-198. Plant Nutr Fertil Sci 19:288–296Google Scholar
  132. Ward M, Grimes H, Huffaker R (1989) Latent nitrate reductase activity is associated with the plasma membrane of corn roots. Planta 177:470–475CrossRefPubMedGoogle Scholar
  133. Werner T, Nehnevajova E, Kollmer I, Novak O, Strnad M, Kramer U, Schmulling T (2010) Root specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920CrossRefPubMedPubMedCentralGoogle Scholar
  134. Witt CA, Dobermann S, Abdulrachman HC, Gines W, Guanghuo R, Nagarajan S, Satawathananont TT, Son PS, Tan L, Van Tiem G, Simbahan Olk DC (1999) Internal nutrient efficiencies in irrigated lowland rice of tropical and subtropical Asia. Field Crop Res 63:113–138CrossRefGoogle Scholar
  135. Xiong et al. (2014) Effect of N fertilizer on distribution of starch granules in different regions of wheat endosperm. Crop J 46:54Google Scholar
  136. Xu G, Fan X, Miller AJ (2012) Plant N assimilation and use efficiency. Annu Rev Plant Biol 63:153–182CrossRefGoogle Scholar
  137. Yan M, Fan XR, Feng HM, Miller AJ, Shen QR, Xu GH (2011) Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges. Plant Cell Environ 34:1360–1372CrossRefGoogle Scholar
  138. Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391CrossRefPubMedGoogle Scholar
  139. Yuan L, Loque D, Ye F, Frommer WB, von Wiren N (2007) N-dependent posttranscriptional regulation of the ammonium transporter AtAMT11. Plant Physiol 143:732–744CrossRefPubMedPubMedCentralGoogle Scholar
  140. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409CrossRefPubMedGoogle Scholar
  141. Zhuo D, Okamoto M, Vidmar JJ, Glass AD (1999) Regulation of a putative high-affinity nitrate transporter (AtNrt2.1) in roots of Arabidopsis thaliana. Plant J 17(5):563–568CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Alka Bharati
    • 1
  • Pranab Kumar Mandal
    • 1
  1. 1.ICAR-National Research Center on Plant BiotechnologyNew DelhiIndia

Personalised recommendations