Plant Molecular Biology

, Volume 91, Issue 6, pp 599–606 | Cite as

Hormones and nitrate: a two-way connection



During their sessile mode of life, plants need to endure variations in their environment such as a drastic variability in the nutrient concentration in soil solution. It is almost trivial to say that such fluctuations in the soil modify plant growth, development and phase transitions. However, the signaling pathways underlying the connections between nitrogen related signaling and hormonal signaling controlling growth are still poorly documented. This review is meant to present how nitrate/nitrogen controls hormonal pathways. Furthermore, it is very interesting to highlight the increasing evidence that the hormonal signaling pathways themselves seem to feed back control of the nitrate/nitrogen transport and assimilation to adapt nutrition to growth. This thus defines a feed-forward cycle that finely coordinates plant growth and nutrition.


Nitrate Hormones Auxin Cytokinin ABA Ethylene Signal interactions Nitrogen NRT1.1 CHL1 ABI2 



I thank Sandrine Ruffel and Benoit Lacombe for helpful comments and corrections on the manuscript. This work was supported by the Centre National de la Recherche Scientifique.


  1. Adamowski M, Friml J (2015) PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27:20–32CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alboresi A, Gestin C, Leydecker MT et al (2005) Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Environ 28:500–512CrossRefPubMedGoogle Scholar
  3. Avery GS, Pottorf L (1945) Auxin and nitrogen relationships in green plants. Am J Bot 32:666–669CrossRefGoogle Scholar
  4. Avery GS, Burkholder PR, Creighton HB (1937) Nutrient deficiencies and growth hormone concentration in Helianthus and Nicotiana. Am J Bot 24:553–557CrossRefGoogle Scholar
  5. Barbez E, Kubes M, Rolcik J et al (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485:119–122CrossRefPubMedGoogle Scholar
  6. Bougyon E, Brun F, Meynard M et al (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nature Plants 1:15015Google Scholar
  7. Boursiac Y, Leran S, Corratge-Faillie C et al (2013) ABA transport and transporters. Trends Plant Sci 18:325–333CrossRefPubMedGoogle Scholar
  8. Britto DT, Siddiqi MY, Glass AD et al (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258CrossRefPubMedPubMedCentralGoogle Scholar
  9. Caba JM, Centeno ML, Fernandez B et al (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211:98–104CrossRefPubMedGoogle Scholar
  10. Chen JG, Cheng SH, Cao W et al (1998) Involvement of endogenous plant hormones in the effect of mixed nitrogen source on growth and tillering of wheat. J Plant Nutr 21:87–97CrossRefGoogle Scholar
  11. Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395CrossRefGoogle Scholar
  12. De Smet I, Signora L, Beeckman T et al (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33:543–555CrossRefPubMedGoogle Scholar
  13. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445CrossRefPubMedGoogle Scholar
  14. Dharmasiri S, Swarup R, Mockaitis K et al (2006) AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312:1218–1220CrossRefPubMedGoogle Scholar
  15. Ding Z, De Smet I (2013) Localised ABA signalling mediates root growth plasticity. Trends Plant Sci 18:533–535CrossRefPubMedPubMedCentralGoogle Scholar
  16. Drew MC (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75:479–490CrossRefGoogle Scholar
  17. Findenegg GR (1987) A comparative study of ammonium toxicity at different constant pH of the nutrient solution. Plant Soil 103:239–244CrossRefGoogle Scholar
  18. Fujii H, Chinnusamy V, Rodrigues A et al (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gifford ML, Dean A, Gutierrez RA et al (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gojon A, Krouk G, Perrine-Walker F et al (2011) Nitrate transceptor(s) in plants. J Exp Bot 62:2299–2308CrossRefPubMedGoogle Scholar
  21. Guo Y, Chen F, Zhang F et al (2005) Auxin transport from shoot to root is involved in the response of lateral root growth to localized supply of nitrate in maize. Plant Sci 169:894–900CrossRefGoogle Scholar
  22. Gutierrez RA, Lejay LV, Dean A et al (2007) Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8:R7CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ho CH, Lin SH, Hu HC et al (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194CrossRefPubMedGoogle Scholar
  24. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278CrossRefPubMedGoogle Scholar
  25. Huang NC, Liu KH, Lo HJ et al (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
  26. Jaillais Y, Fobis-Loisy I, Miege C et al (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109CrossRefPubMedGoogle Scholar
  27. Joshi-Saha A, Valon C, Leung J (2011) A brand new START: abscisic acid perception and transduction in the guard cell. Sci Signal 4:re4CrossRefPubMedGoogle Scholar
  28. Kanno Y, Hanada A, Chiba Y et al (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci USA 109:9653–9658CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kanno Y, Kamiya Y, Seo M (2013) Nitrate does not compete with abscisic acid as a substrate of AtNPF4.6/NRT1.2/AIT1 in Arabidopsis. Plant Signal Behav 8:e26624CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis Book 12:e0168CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kronzucker HJ, Britto DT, Davenport RJ et al (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337CrossRefPubMedGoogle Scholar
  32. Krouk G, Lacombe B, Bielach A et al (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell 18:927–937CrossRefPubMedGoogle Scholar
  33. Krouk G, Ruffel S, Gutierrez RA et al (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16:178–182CrossRefPubMedGoogle Scholar
  34. Krouk G, Carre C, Fizames C et al (2015) GeneCloud reveals semantic enrichment in lists of gene descriptions. Mol Plant 8:971–973CrossRefPubMedGoogle Scholar
  35. Leran S, Varala K, Boyer JC et al (2014) A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends Plant Sci 19:5–9CrossRefPubMedGoogle Scholar
  36. Leran S, Edel KH, Pervent M et al (2015) Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci Signal 8:ra43CrossRefPubMedGoogle Scholar
  37. Li Y, Krouk G, Coruzzi GM et al (2014) Finding a nitrogen niche: a systems integration of local and systemic nitrogen signalling in plants. J Exp Bot 65:5601–5610Google Scholar
  38. Liu KH, Tsay YF (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005–1013CrossRefPubMedPubMedCentralGoogle Scholar
  39. Liu J, An X, Cheng L et al (2010) Auxin transport in maize roots in response to localized nitrate supply. Ann Bot 106:1019–1026Google Scholar
  40. Ma W, Li J, Qu B et al (2014) Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. Plant J 78:70–79CrossRefPubMedGoogle Scholar
  41. Marin IC, Loef I, Bartetzko L et al (2010) Nitrate regulates floral induction in Arabidopsis, acting independently of light, gibberellin and autonomous pathways. Planta 233:539–552Google Scholar
  42. Matakiadis T, Alboresi A, Jikumaru Y et al (2009) The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiol 149:949–960CrossRefPubMedPubMedCentralGoogle Scholar
  43. Medici A, Krouk G (2014) The primary nitrate response: a multifaceted signalling pathway. J Exp Bot 65:5567–5576CrossRefPubMedGoogle Scholar
  44. Muller D, Waldie T, Miyawaki K et al (2015) Cytokinin is required for escape but not release from auxin mediated apical dominance. Plant J 82:874–886CrossRefPubMedPubMedCentralGoogle Scholar
  45. Okamoto M, Kuwahara A, Seo M et al (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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 Google Scholar
  47. Park SY, Fung P, Nishimura N et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedPubMedCentralGoogle Scholar
  48. Parker JL, Newstead S (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507:68–72CrossRefPubMedPubMedCentralGoogle Scholar
  49. Parry G, Calderon-Villalobos LI, Prigge M et al (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545CrossRefPubMedPubMedCentralGoogle Scholar
  50. Patterson K, Walters L, Cooper A et al (2015) Nitrate-regulated glutaredoxins control Arabidopsis thaliana primary root growth. Plant Physiol 170:989–999Google Scholar
  51. Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688CrossRefPubMedGoogle Scholar
  52. Rahayu YS, Walch-Liu P, Neumann G et al (2005) Root-derived cytokinins as long-distance signals for NO3 induced stimulation of leaf growth. J Exp Bot 56:1143–1152CrossRefPubMedGoogle Scholar
  53. Remans T, Nacry P, Pervent M et al (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci USA 103:19206–19211CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ruffel S, Krouk G, Ristova D et al (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci USA 108:18524–18529CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ruffel S, Poitout A, Krouk G et al (2015) Long-distance nitrate signaling displays cytokinin dependent and independent branches. J Integr Plant Biol. doi:10.1111/jipb.12453
  56. Sakakibara H, Suzuki M, Takei K et al (1998) A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J 14:337–344CrossRefPubMedGoogle Scholar
  57. Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11:440–448CrossRefPubMedGoogle Scholar
  58. Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48CrossRefPubMedGoogle Scholar
  59. Signora L, De Smet I, Foyer CH et al (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662CrossRefPubMedGoogle Scholar
  60. Sun J, Bankston JR, Payandeh J et al (2014) Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507:73–77CrossRefPubMedPubMedCentralGoogle Scholar
  61. Takei K, Sakakibara H, Taniguchi M et al (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42:85–93CrossRefPubMedGoogle Scholar
  62. Takei K, Takahashi T, Sugiyama T et al (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977CrossRefPubMedGoogle Scholar
  63. Takei K, Ueda N, Aoki K et al (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45:1053–1062CrossRefPubMedGoogle Scholar
  64. Tamaki V, Mercier H (2007) Cytokinins and auxin communicate nitrogen availability as long-distance signal molecules in pineapple (Ananas comosus). J Plant Physiol 164:1543–1547CrossRefPubMedGoogle Scholar
  65. Tian Q, Chen F, Liu J et al (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J Plant Physiol 165:942–951CrossRefPubMedGoogle Scholar
  66. Tian QY, Sun P, Zhang WH (2009) Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana. New Phytol 184:918–931CrossRefPubMedGoogle Scholar
  67. Tsay YF, Schroeder JI, Feldmann KA et al (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713CrossRefPubMedGoogle Scholar
  68. Vega A, Canessa P, Hoppe G et al (2015) Transcriptome analysis reveals regulatory networks underlying differential susceptibility to Botrytis cinerea in response to nitrogen availability in Solanum lycopersicum. Front Plant Sci 6:911CrossRefPubMedPubMedCentralGoogle Scholar
  69. Vidal EA, Araus V, Lu C et al (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:4477–4482CrossRefPubMedPubMedCentralGoogle Scholar
  70. Vidal EA, Moyano TC, Riveras E et al (2013) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proc Natl Acad Sci USA 110:12840–12845CrossRefPubMedPubMedCentralGoogle Scholar
  71. Vidal EA, Moyano TC, Canales J et al (2014) Nitrogen control of developmental phase transitions in Arabidopsis thaliana. J Exp Bot 65:5611–5618CrossRefPubMedGoogle Scholar
  72. Vuylsteker C, Huss B, Rambour S (1997a) Nitrate reductase activity in chicory roots following excision. J Exp Bot 48:59–65CrossRefGoogle Scholar
  73. Vuylsteker C, Leleu O, Rambour S (1997b) Influence of BAP and NAA on the expression of nitrate reductase in excised chicory roots. J Exp Bot 48:1079–1085CrossRefGoogle Scholar
  74. Walch-Liu P, Neumann G, Bangerth F et al (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51:227–237CrossRefPubMedGoogle Scholar
  75. Walch-Liu P, Ivanov II, Filleur S et al (2006) Nitrogen regulation of root branching. Ann Bot (Lond) 97:875–881CrossRefGoogle Scholar
  76. Wang R, Tischner R, Gutierrez RA et al (2004) Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136:2512–2522CrossRefPubMedPubMedCentralGoogle Scholar
  77. Werner T, Schmulling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538CrossRefPubMedGoogle Scholar
  78. Yang Y, Hammes UZ, Taylor CG et al (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr Biol 16:1123–1127CrossRefPubMedGoogle Scholar
  79. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409CrossRefPubMedGoogle Scholar
  80. Zhang H, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59CrossRefPubMedGoogle Scholar
  81. Zhang H, Jennings A, Barlow PW et al (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534CrossRefPubMedPubMedCentralGoogle Scholar
  82. Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Laboratoire de Biochimie et Physiologie Moléculaire des Plantes, Institut de Biologie Intégrative des Plantes ‘Claude Grignon’UMR CNRS, INRA, SupAgro, UMMontpellier CedexFrance

Personalised recommendations