Advertisement

Molecular Targets for Improvement of Crop Nitrogen Use Efficiency: Current and Emerging Options

  • Vikas Kumar Mandal
  • Narendra Sharma
  • Nandula Raghuram
Chapter

Abstract

Unused fertilizers are the single largest source of nitrous oxide greenhouse gas emissions globally, apart from causing N-pollution in ground and surface waters and eutrophication. While short-term improvements in N-use efficiency (NUE) can be made by agronomic practices, long-term crop improvement is only possible through biological interventions. The lack of clearly defined phenotype and genotype has delayed this process till recently, but the advent of omics and reverse genetics is opening up new avenues to improve crop NUE. It is becoming increasingly evident that several genes and pathways contribute to NUE. Many N-responsive regulators of root development, sensing and signaling, transportation, utilization and remobilization have been targeted to improve NUE, such as C-terminally encoded peptides (CEPs), CLAVATA3/endosperm surrounding region-related peptides (CLE), MADS-box transcription factors, and NAC transcription factors. The nitrate transporter of NRT1.1 is proposed to be a sensor or transceptor, which regulates the crop yield by acting as a component in the Ca2+-mediated signaling cascade. Several other signaling pathways involving target of rapamycin (TOR) complex, general amino acid control non-derepressible 2 (GCN2), ionotropic glutamate-like receptor (iGLR), and PII proteins have been found to play a important roles in maintaining proper N balance in plants. In cereals, cytosolic glutamine synthase, glutamate synthetase, and alanine/aspartate aminotransferases are important targets, as they are involved in remobilization of N from senescing leaves during grain filling and in maintaining proper C/N balance. Several post-transcriptional regulators such as non-coding small RNAs and post-translational regulators such as kinases and phosphatases regulate the expression level of genes involved in N-response/NUE and are emerging as novel targets.

Keywords

Nitrogen N-use efficiency NUE Nutrients Nitrate Ammonium Urea Root development Signal transduction 

Notes

Acknowledgements

This work was supported in part by research grant to NR and fellowship to NS from the Department of Biotechnology, Govt. of India under the Indo-UK Virtual Nitrogen Centre on Nitrogen Efficiency of Whole cropping Systems (NEWS) BT/IN/UK-VNC/44/NR/2015-16. VM is a recipient of DBT fellowship (BCIL/HRD/DBT-JRF/FLSP).

References

  1. Abdula SE, Lee HJ, Kim J, Niño MC, Jung Y-J, Cho Y-C abd Cho Y-G (2016) BrUGE1transgenic rice showed improved growth performance with enhanced drought tolerance. Breed Sci 66(2), 226–233Google Scholar
  2. Alvarez JM, Riveras E, Vidal EA, Gras DE, Contreras‐López O, Tamayo KP, Aceituno F, Gómez I, Ruffel S, Lejay L, Jordana X (2014) Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. The Plant J 80(1):1–3Google Scholar
  3. Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S, Tsuchiya YN, Sawa S, Fukuda H, von Wirén N, Takahashi H (2014) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. P Natl A Sci 111(5):2029–2034Google Scholar
  4. Araya T, von Wirén N, Takahashi H (2016) CLE peptide signaling and nitrogen interactions in plant root development. Plant Mol Biol 91(6):607–615Google Scholar
  5. Bargmann BOR, Marshall-Colon A, Efroni I, Ruffel S, Birnbaum KD, Coruzzi GM, Krouk G (2013) TARGET: A Transient Transformation System for Genome-Wide Transcription Factor Target Discovery. Mol Pla 6(3):978–980Google Scholar
  6. Bellegarde F, Gojon A, Martin A (2017) Signals and players in the transcriptional regulation of root responses by local and systemic N signaling in Arabidopsis thaliana. J Exp Bot 68(10):2553–2565CrossRefPubMedGoogle Scholar
  7. Bouguyon E, Brun F, Meynard D, Kubeš M, Pervent M, Leran S, Lacombe B, Krouk G, Guiderdoni E, Zažímalová E, Hoyerová K (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat Plants 1(3):15015Google Scholar
  8. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet‐Mercey S, Taconnat L, Renou J, Daniel‐Vedele F, Fernandez E, Meyer C, Krapp, A (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. The Plant J 57(3):426–435CrossRefPubMedGoogle Scholar
  9. Calatrava V, Chamizo-Ampudia A, Sanz-Luque E, Ocaña-Calahorro F, Llamas A, Fernandez E, Galvan A (2017) How Chlamydomonas handles nitrate and the nitric oxide cycle. J Exp Bot 68(10):2593–2602CrossRefPubMedGoogle Scholar
  10. Chakraborty N. and Raghuram N. (2011) Nitrate sensing and signaling in genomewide plant N response. In Nitrogen Use Efficiency in Plants, V. Jain, P. Anandakumar (eds) New India Publishing Agency, New Delhi. pp. 45–62Google Scholar
  11. Chen L, Liao H (2017) Engineering crop nutrient efficiency for sustainable agriculture. J Integr Plant Biol 59(10):710–735Google Scholar
  12. Chien P-S, Chiang C-B, Wang Z, Chiou T-J (2017) MicroRNA-mediated signaling and regulation of nutrient transport and utilization. Curr Opinion in Plant Biol 39:73–79CrossRefPubMedGoogle Scholar
  13. Das SK, Pathak RR, Choudhury D, Raghuram N (2007) Genomewide computational analysis of nitrate response elements in rice and Arabidopsis. Mol Genet Genomics 278(5):519–525Google Scholar
  14. Dellero Y, Lamothe-Sibold M, Jossier M, Hodges M (2015) Arabidopsis thaliana ggt1 photorespiratory mutants maintain leaf carbon: nitrogen balance by reducing RuBisCO content and plant growth. The Plant J 83(6):1005–1018Google Scholar
  15. Dobrenel T, Caldana C, Hanson J, Robaglia C, Vincentz M, Veit B, Meyer C (2016) TOR signaling and nutrient sensing. Ann Rev Plant Biol 67(1):261–285CrossRefGoogle Scholar
  16. 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 yields. P Natl A Sci 113(26):7118–7123Google Scholar
  17. Fan X, Naz M, Fan X, Xuan W, Miller AJ, Xu G (2017) Plant nitrate transporters: from gene function to application. J Exp Bot 68(10):2463–2475CrossRefPubMedGoogle Scholar
  18. Forde BG (2014). Nitrogen signalling pathways shaping root system architecture: an update. Curr Opin Plant Biol 21:30–36Google Scholar
  19. Forde BG, Cutler SR, Zaman N, Krysan PJ (2013) Glutamate signalling via a MEKK1 kinase-dependent pathway induces changes in Arabidopsis root architecture. The Plant J 75(1):1–10Google Scholar
  20. Gaju O, Allard V, Martre P, Snape JW, Heumez E, LeGouis J,  Moreau D, Bogard M, Griffiths S, Orford S, Hubbart S (2011) Identification of traits to improve the nitrogen-use efficiency of wheat genotypes. Field Crops Res 123(2):139–152CrossRefGoogle Scholar
  21. Gan Y, Bernreiter A, Filleur S, Abram B, Forde BG (2012) Overexpressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development. Plant Cell Physiol 53(6):1003–1016Google Scholar
  22. Gent L, Forde BG (2017) How do plants sense their nitrogen status? J Exp Bot 68(10):2531–2539Google Scholar
  23. Gifford ML, Banta JA, Katari MS, Hulsmans J, Chen L, Ristova D, Tranchina D, Purugganan MD, Coruzzi GM, Birnbaum KD (2013) Plasticity regulators modulate specific root traits in discrete nitrogen environments. PLoS Genet 9(9):e1003760Google Scholar
  24. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2017) Cell-specific nitrogen responses mediate developmental plasticity. P Natl A Sci 105(2):803–808Google Scholar
  25. Gutiérrez RA, Stokes TL, Thum K, Xu X, Obertello M, Katari MS, Tanurdzic M, Dean A, Nero DC, McClung CR, Coruzzi GM (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. P Natl A Sci 105(12):4939–4944Google Scholar
  26. He X, Qu B, Li W, Zhao X, Teng W, Ma W,  Ren Y, Li B, Li Z,Tong Y (2015) The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiol 169(3):1991–2005Google Scholar
  27. Havé M, Marmagne A, Chardon F, Masclaux-Daubresse C (2016) Nitrogen remobilisation during leaf senescence: lessons from Arabidopsis to crops. J Exp Bot 68(10):2513–2529Google Scholar
  28. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138(6):1184–1194CrossRefPubMedGoogle Scholar
  29. Hu B, Wang W, Ou S, Tang J, Li H, Che R, Zhang Z, Chai X, Wang H, Wang Y, Liang C, Liu L, Piao Z, Deng Q, Deng K, Xu C, Liang Y, Zhang L, Li L, Chu C (2015) Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nature Genetics 47(7):834–838CrossRefPubMedGoogle Scholar
  30. Huang S, Chen S, Liang Z, Zhang C, Yan M, Chen J, Xu G, Fan X, Zhang Y (2015) Knockdown of the partner protein OsNAR2.1 for high-affinity nitrate transport represses lateral root formation in a nitrate-dependent manner. Sci Rep 5:18192Google Scholar
  31. Klemens PAW, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus HE (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol 163(3):1338–1352CrossRefPubMedPubMedCentralGoogle Scholar
  32. Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince A-S, Chaillou S, Ferrario-Méry S, Meyer C, Daniel-Vedele F (2014) Nitrate transport and signaling in Arabidopsis. J Exp Bot 65(3):789–798CrossRefPubMedGoogle Scholar
  33. Li H, Hu B, Chu C (2017) Nitrogen use efficiency in crops: lessons from Arabidopsis and rice. J Exp Bot 68(10):2477–2488Google Scholar
  34. Li X, Zeng R, Liao H (2016) Improving crop nutrient efficiency through root architecture modifications. J Integr Plant Biol 58(3):193–202CrossRefPubMedGoogle Scholar
  35. Liu KH, Niu Y, Konishi M, Wu Y, Du H, Chung HS, Li L, Boudsocq M, McCormack M, Maekawa S, Ishida T (2017) Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature 545(7654):311–316CrossRefPubMedPubMedCentralGoogle Scholar
  36. Liu W, Han X, Zhan G, Zhao Z, Feng Y, Wu C (2015) A novel sucrose-regulatory MADS-box transcription factor GmNMHC5 promotes root development and nodulation in soybean (Glycine max [L.] Merr.). Int J Mol Sci 16(9):20657–20673CrossRefPubMedPubMedCentralGoogle Scholar
  37. Liu W, Sun Q, Wang K, Du Q, Li W-X (2016) Nitrogen limitation adaptation (NLA) is involved in source-to-sink remobilization of nitrate by mediating the degradation of NRT1.7 in Arabidopsis. New Phytol 214(2):734–744Google Scholar
  38. Liu Y, von Wirén N (2017) Ammonium as a signal for physiological and morphological responses in plants. J Exp Bot 68(10):2581–2592CrossRefPubMedGoogle Scholar
  39. Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112(2):347–357CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ma W, Li J, Qu B, He X, Zhao X, Li B, Fu X, Tong Y (2014) Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. The Plant J 78(1):70–79CrossRefPubMedGoogle Scholar
  41. Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E, Colot V, Meyer C, Krapp A (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4:1713CrossRefPubMedGoogle Scholar
  42. Młodzińska E, Kłobus G, Christensen MD, Fuglsang AT (2015) The plasma membrane H(+)-ATPase AHA2 contributes to the root architecture in response to different nitrogen supply. Physiol Plant 154(2):270–282CrossRefPubMedGoogle Scholar
  43. Mochizuki S, Jikumaru Y, Nakamura H, Koiwai H, Sasaki K, Kamiya Y, Kamiya Y, Ichikawa H, Minami E, Nishizawa Y (2014) Ubiquitin ligase EL5 maintains the viability of root meristems by influencing cytokinin-mediated nitrogen effects in rice. J Exp Bot 65(9):2307–2318CrossRefPubMedPubMedCentralGoogle Scholar
  44. Morita S, Suga T, Yamazaki K (1988) The relationship between root length density and yield in rice plants. Jpn J Crop Sci 57(3):438–443CrossRefGoogle Scholar
  45. Murray JD, Liu C-W, Chen Y, Miller AJ (2016) Nitrogen sensing in legumes. J Exp Bot 68(8):1919–1926Google Scholar
  46. Nishizawa Y, Mochizuki S, Koiwai H, Kondo K, Kishimoto K, Katoh E, Minami E (2015) Rice ubiquitin ligase EL5 prevents root meristematic cell death under high nitrogen conditions and interacts with a cytosolic GAPDH. Plant Signal Behav 10(3):e990801CrossRefPubMedPubMedCentralGoogle Scholar
  47. Noguero M, Lacombe B (2016) Transporters involved in root nitrate uptake and sensing by Arabidopsis. Front Plant Sci (7):1391Google Scholar
  48. O’Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutiérrez RA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9(6):837–856CrossRefGoogle Scholar
  49. Ohyama K, Ogawa M, Matsubayashi Y (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. The Plant J 55(1):152–160CrossRefPubMedGoogle Scholar
  50. Okamoto S, Suzuki T, Kawaguchi M, Higashiyama T, Matsubayashi Y (2015) A comprehensive strategy for identifying long-distance mobile peptides in xylem sap. The Plant J 84(3):611–620CrossRefGoogle Scholar
  51. Okumoto S, Versaw W (2017) Genetically encoded sensors for monitoring the transport and concentration of nitrogen-containing and phosphorus-containing molecules in plants. Curr Opin Plant Biol 39:129–135Google Scholar
  52. Ondzighi-Assoume CA, Chakraborty S, Harris JM (2016) Environmental nitrate stimulates abscisic acid accumulation in Arabidopsis root tips by releasing it from inactive stores. Plant Cell 28(3):729–745CrossRefPubMedPubMedCentralGoogle Scholar
  53. Pathak RR, Ahmad A, Lochab S, Raghuram N (2008) Molecular physiology of plant N-use efficiency and biotechnological options for its enhancement. Curr Sci 94(11):1394–1403Google Scholar
  54. Pathak RR, Das SK, Choudhury D, Raghuram N (2009) Genomewide bioinformatic analysis negates any specific role for Dof, GATA and Ag/cTCA motifs in nitrate responsive gene expression in Arabidopsis. Physiol Mol Biol Pla 15(2):145–150Google Scholar
  55. Pathak RR, Lochab S, Raghuram N (2011) Improving nitrogen use efficiency. In Compr Biotechnol, vol 4, 2nd edn. Elsevier, Oxford, pp 209–218CrossRefGoogle Scholar
  56. Qin S, Sun X, Hu C, Tan Q, Zhao X, Xin J, Wen X (2017) Effect of NO3:NH4+ ratios on growth, root morphology and leaf metabolism of oilseed rape (Brassica napus L.) seedlings. Acta Physiol Plant 39(9):198CrossRefGoogle Scholar
  57. Qu B, He X, Wang J, Zhao Y, Teng W, Shao A, Zhao X, Ma W, Wang J, Li B, Li Z (2015) A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiol 167(2):411–423CrossRefPubMedGoogle Scholar
  58. Reddy MM, Ulaganathan K (2015) Nitrogen nutrition, its regulation and biotechnological approaches to improve crop productivity. Am J Plant Sci 6(18):2745–2798CrossRefGoogle Scholar
  59. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103(50):19206–19211CrossRefPubMedGoogle Scholar
  60. Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutiérrez RA (2015) The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis 1. Plant Physiol 177(1):00961Google Scholar
  61. Roberts I, Smith S, Stes E, De Rybel B, Staes A, Van De Cotte B, Njo MF, Dedeyne L, Demol H, Lavenus J, Audenaert D (2016) CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis. J Exp Bot 67(16):4889–4899Google Scholar
  62. Rosas U, Cibrian-Jaramillo A, Ristova D, Banta JA, Gifford ML, Fan AH, Zhou RW, Kim GJ, Krouk G, Birnbaum KD, Purugganan MD (2013) Integration of responses within and across Arabidopsis natural accessions uncovers loci controlling root systems architecture. P Natl A Sci 110(37):15133–15138Google Scholar
  63. Rothstein SJ, Bi Y-M, Coneva V, Han M, Good A (2014) The challenges of commercializing second-generation transgenic crop traits necessitate the development of international public sector research infrastructure. J Exp Bot 65(19):5673–5682CrossRefPubMedGoogle Scholar
  64. Sesma A, Castresana C, Castellano MM (2017) Regulation of translation by TOR, eIF4E and eIF2α in plants: current knowledge, challenges and future perspectives. Front Plant Sci 8:644Google Scholar
  65. Shahzad Z, Amtmann A (2017) Food for thought: how nutrients regulate root system architecture. Curr Opin Plant Biol 39:80–87CrossRefPubMedPubMedCentralGoogle Scholar
  66. Sinha VB, Jangam AP, Raghuram N (2018) Biological determinants of crop N use efficiency and biotechnological avenues for improvement. In: Masso C, Bleeker A, Raghuram N, Bekunda M, Sutton M (eds) Proceedings of the N2013. SpringerGoogle Scholar
  67. Slovak R, Göschl C, Su X, Shimotani K, Shiina T, Busch W (2014) A scalable open-source pipeline for large-scale root phenotyping of Arabidopsis. Plant Cell 26(6):2390–2403CrossRefPubMedPubMedCentralGoogle Scholar
  68. Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170(2):603–617CrossRefPubMedGoogle Scholar
  69. Sun C-H, Yu J-Q, Hu D-G (2017) Nitrate: a crucial signal during lateral roots development. Front Plant Sci 8:485PubMedPubMedCentralGoogle Scholar
  70. Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Liu Q, Huang X, Yuan Q, Han R, Zhao M, Dong G, Guo L, Zhu X, Gou Z, Wang W, Wu Y, Lin H, Fu X (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46(6):652–656CrossRefPubMedGoogle Scholar
  71. Sun J, Ye M, Peng S, Li Y (2016) Nitrogen can improve the rapid response of photosynthesis to changing irradiance in rice (Oryza sativa L.) plants. Sci Rep 6(1):31305Google Scholar
  72. Sutton MA, Bleeker A, Howard CM, Bekunda M, Grizzetti B, de Vries W, van Grinsven HJM, Abrol YP, Adhya TK, Billen G,. Davidson EA, Datta A, Diaz R, Erisman JW, Liu XJ, Oenema O, Palm C, Raghuram N, Reis S, Scholz RW, Sims T, Westhoek H, Zhang FS, with contributions from Ayyappan S, Bouwman AF, Bustamante M, Fowler D, Galloway JN, Gavito ME, Garnier J, Greenwood S, Hellums DT, Holland M, Hoysall C, Jaramillo VJ, Klimont Z, Ometto JP, Pathak H, Plocq Fichelet V, Powlson D, Ramakrishna K, Roy A, Sanders K, Sharma C, Singh B, Singh U, Yan XY, Zhang Y (2013) Our nutrient world: the challenge to produce more food and energy with less pollution. Global Overview of Nutrient Management, Centre for Ecology and Hydrology, Edinburgh on behalf of the Global Partnership on Nutrient Management and the International Nitrogen InitiativeGoogle Scholar
  73. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y (2014) Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science (New York, N.Y.) 346(6207):343–346CrossRefGoogle Scholar
  74. Undurraga SF, Ibarra-Henríquez C, Fredes I, Álvarez JM, Gutiérrez RA (2017) Nitrate signaling and early responses in Arabidopsis roots. J Exp Bot 68(10):2541–2551CrossRefPubMedPubMedCentralGoogle Scholar
  75. Vidal EA, Moyano TC, Riveras E, Contreras-López O, Gutiérrez RA (2013) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. P Natl A Sci 110(31):12840–12845Google Scholar
  76. Vidal EA, Viviana A, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis Thaliana. P Natl A Sci 107(9):4477–4482Google Scholar
  77. Verzeaux J, Hirel B, Dubois F, Lea PJ, Tétu T (2017) Agricultural practices to improve nitrogen use efficiency through the use of arbuscular mycorrhizae: basic and agronomic aspects. Plant Sci 264:48–56Google Scholar
  78. Wada S, Hayashida Y, Izumi M, Kurusu T, Hanamata S, Kanno K, Kojima S, Yamaya T, Kuchitsu K, Makino A, Ishida H (2015) Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice. Plant Physiol 168(1):60–73CrossRefPubMedPubMedCentralGoogle Scholar
  79. Wan TE, Xue HE, TONG YP (2017) Transgenic approaches for improving use efficiency of nitrogen, phosphorus and potassium in crops. J Integr Agri 16 (12):60345–60347Google Scholar
  80. Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136(1):2512–2522CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wang X, Peng F, Li M, Yang L, Li G (2012) Expression of a heterologous SnRK1 in tomato increases carbon assimilation, nitrogen uptake and modifies fruit development. J Plant Physiol 169(12):1173–1182CrossRefPubMedGoogle Scholar
  82. Weiland M, Mancuso S, Baluska F (2014) Signalling via glutamate and GLRs in Arabidopsis thaliana. Funct Plant Biol 43(1):1–25Google Scholar
  83. Xuan W, Beeckman T, Xu G (2017) Plant nitrogen nutrition: sensing and signaling. Curr Opin Plant Biol 39:57–65CrossRefPubMedGoogle Scholar
  84. Xu N, Wang R, Zhao L, Zhang C, Li Z, Lei Z, Liu F, Guan P, Chu Z, Crawford NM,Wang Y (2016) The Arabidopsis NRG2 protein mediates nitrate signaling and interacts with and regulates key nitrate regulators. The Plant Cell 28(2):485–504CrossRefPubMedPubMedCentralGoogle Scholar
  85. 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(12):3763–3775CrossRefPubMedGoogle Scholar
  86. Yang JC, Zhang H, Zhang JH (2012) Root morphology and physiology in relation to the yield formation of rice. J Integr Agri 11(6):920–926CrossRefGoogle Scholar
  87. Yan Y, Wang H, Hamera S, Chen X, Fang R (2014) MiR444a has multiple functions in the rice nitrate-signaling pathway. The Plant J 78(1):44–55CrossRefPubMedGoogle Scholar
  88. Yu C, Liu Y, Zhang A, Su S, Yan A, Huang L, Ali I, Liu Y, Forde BG, Gan Y (2015) MADS-box transcription factor OsMADS25 regulates root development through affection of nitrate accumulation in rice. PLoS One 10(8):e0135196.Google Scholar
  89. Yu LH, Miao ZQ, Qi GF, Wu J, Cai XT, Mao JL, Xiang CB (2014) MADS-box transcription factor AGL21 regulates lateral root development and responds to multiple external and physiological signals. Mol Plant 7:1653–1669CrossRefPubMedPubMedCentralGoogle Scholar
  90. Yu LH, Wu J, Tang H, Yuan Y, Wang S-M, Wang Y-P, Zhu QS, Li SG, Xiang C-B (2016) Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and -sufficient conditions by enhancing nitrogen and carbon assimilation. Scientific reports 6:27795Google Scholar
  91. Zeng D-D, Qin R, Li M, Alamin M, Jin X-L, Liu Y, Shi C-H (2016) The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and the nitrogen remobilization in rice. Mol Genet Genomics 292(2):385–395CrossRefPubMedGoogle Scholar
  92. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science (New York, N.Y.) 279(5349):407–409CrossRefGoogle Scholar
  93. Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature 528(7580):51Google Scholar
  94. Zuluaga DL, De Paola D, Janni M, Curci PL, Sonnante G (2017) Durum wheat miRNAs in response to nitrogen starvation at the grain filling stage. PLoS One 12(8):e0183253CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Vikas Kumar Mandal
    • 1
  • Narendra Sharma
    • 1
  • Nandula Raghuram
    • 1
  1. 1.School of BiotechnologyGuru Gobind Singh Indraprastha UniversityDwarkaIndia

Personalised recommendations