, Volume 246, Issue 4, pp 585–595 | Cite as

Nitrate transporters: an overview in legumes

  • Anthoni Pellizzaro
  • Bénédicte Alibert
  • Elisabeth Planchet
  • Anis M. Limami
  • Marie-Christine Morère-Le PavenEmail author


Main conclusion

The nitrate transporters, belonging to NPF and NRT2 families, play critical roles in nitrate signaling, root growth and nodule development in legumes.

Nitrate plays an essential role during plant development as nutrient and also as signal molecule, in both cases working via the activity of nitrate transporters. To date, few studies on NRT2 or NPF nitrate transporters in legumes have been reported, and most of those concern Lotus japonicus and Medicago truncatula. A molecular characterization led to the identification of 4 putative LjNRT2 and 37 putative LjNPF gene sequences in L. japonicus. In M. truncatula, the NRT2 family is composed of 3 putative members. Using the new genome annotation of M. truncatula (Mt4.0), we identified, for this review, 97 putative MtNPF sequences, including 32 new sequences relative to previous studies. Functional characterization has been published for only two MtNPF genes, encoding nitrate transporters of M. truncatula. Both transporters have a role in root system development via abscisic acid signaling: MtNPF6.8 acts as a nitrate sensor during the cell elongation of the primary root, while MtNPF1.7 contributes to the cellular organization of the root tip and nodule formation. An in silico expression study of MtNPF genes confirmed that NPF genes are expressed in nodules, as previously shown for L. japonicus, suggesting a role for the corresponding proteins in nitrate transport, or signal perception in nodules. This review summarizes our knowledge of legume nitrate transporters and discusses new roles for these proteins based on recent discoveries.


Lotus japonicus Medicago truncatula Nitrate signaling NPF NRT2 



Authors wish to thank Pr. David C. Logan (IRHS, Beaucouzé, France) for critical reading of the manuscript and English language correction. The work was supported by the QUALISEM research program, funded by Région Pays de Loire (France).

Supplementary material

425_2017_2724_MOESM1_ESM.xlsx (29 kb)
Supplementary material 1 (XLSX 29 kb)


  1. Amarasinghe BH, de Bruxelles GL, Braddon M, Onyeocha I, Forde BG, Udvardi MK (1998) Regulation of GmNRT2 expression and nitrate transport activity in roots of soybean (Glycine max). Planta 206:44–52CrossRefPubMedGoogle Scholar
  2. Araki R, Hasegawa H (2006) Expression of rice (Oryza sativa L.) genes involved in high-affinity nitrate transport during the period of nitrate induction. Breed Sci 56:295–302CrossRefGoogle Scholar
  3. Bagchi R, Salehin M, Adeyemo OS, Salazar C, Shulaev V, Sherrier DJ, Dickstein R (2012) Functional assessment of the Medicago truncatula NIP/LATD protein demonstrates that it is a high-affinity nitrate transporter. Plant Physiol 160:906–916. doi: 10.1104/pp.112.196444 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao PX, Tang Y, Udvardi MK (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55:504–513. doi: 10.1111/j.1365-313X.2008.03519.x CrossRefPubMedGoogle Scholar
  5. Cabeza R, Koester B, Liese R, Lingner A, Baumgarten V, Dirks J, Salinas-Riester G, Pommerenke C, Dittert K, Schulze J (2014) An RNA sequencing transcriptome analysis reveals novel insights into molecular aspects of the nitrate impact on the nodule activity of Medicago truncatula. Plant Physiol 164:400–411. doi: 10.1104/pp.113.228312 CrossRefPubMedGoogle Scholar
  6. Cai C, Wang JY, Zhu YG, Shen QR, Li B, Tong YP, Li ZS (2008) Gene structure and expression of the high-affinity nitrate transport system in rice roots. J Integr Plant Biol 50:443–451. doi: 10.1111/j.1744-7909.2008.00642.x CrossRefPubMedGoogle Scholar
  7. Celis-Arámburo TJ, Carrillo-Pech M, Castro-Concha LA, Miranda-Ham ML, Martínez-Estévez M, Echevarría-Machado I (2011) Exogenous nitrate induces root branching and inhibits primary root growth in Capsicum chinense Jacq. Plant Physiol Biochem 49:1456–1464. doi: 10.1016/j.plaphy.2011.09.003 CrossRefGoogle Scholar
  8. Crawford NM, Glass AD (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395CrossRefGoogle Scholar
  9. Criscuolo G, Valkov VT, Parlati A, Alves LM, Chiurazzi M (2012) Molecular characterization of the Lotus japonicus NRT1(PTR) and NRT2 families. Plant Cell Environ 35:1567–1581. doi: 10.1111/j.1365-3040.2012.02510.x CrossRefPubMedGoogle Scholar
  10. Damiani I, Drain A, Guichard M, Balzergue S, Boscari A, Boyer JC, Brunaud V, Cottaz S, Rancurel C, Da Rocha M, Fizames C, Fort S, Gaillard I, Maillol V, Danchin EGJ, Rouached H, Samain E, Su YH, Thouin J, Touraine B, Puppo A, Frachisse JM, Pauly N, Sentenac H (2016) Nod Factor effects on root hair-specific transcriptome of Medicago truncatula: focus on plasma membrane transport systems and reactive oxygen species networks. Front Plant Sci 7:1–22. doi: 10.3389/fpls.2016.00794 Google Scholar
  11. De Smet I, Zhang H, Inzé D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439. doi: 10.1016/j.tplants.2006.07.003 CrossRefPubMedGoogle Scholar
  12. Faure-Rabasse S, Le Deunff E, Lainé P, Macduff JH, Ourry A (2002) Effects of nitrate pulses on BnNRT1 and BnNRT2 genes: mRNA levels and nitrate influx rates in relation to the duration of N deprivation in Brassica napus L. J Exp Bot 53:1711–1721CrossRefPubMedGoogle Scholar
  13. Feng H, Yan M, Fan X, Li B, Shen Q, Miller AJ, Xu G (2011) Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J Exp Bot 62:2319–2332. doi: 10.1093/jxb/erq403 CrossRefPubMedGoogle Scholar
  14. Glass AD, Kotur Z (2013) A reevaluation of the role of Arabidopsis NRT1.1 in high-affinity nitrate transport. Plant Physiol 163:1103–1106. doi: 10.1104/pp.113.229161 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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 9:597–605. doi: 10.1016/j.tplants.2004.10.008 CrossRefPubMedGoogle Scholar
  16. Harris JM (2015) Abscisic acid: hidden architect of root system structure. Plants 4:548–572. doi: 10.3390/plants4030548 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Harris JM, Dickstein R (2010) Control of root architecture and nodulation by the LATD/NIP transporter. Plant Signal Behav 5:1365–1369CrossRefPubMedPubMedCentralGoogle Scholar
  18. Heath KD, Stock AJ, Stinchcombe JR (2010) Mutualism variation in the nodulation response to nitrate. J Evol Biol 23:2494–2500. doi: 10.1111/j.1420-9101.2010.02092.x CrossRefPubMedGoogle Scholar
  19. Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R (2015) Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot 66:2877–2887. doi: 10.1093/jxb/erv051 CrossRefPubMedGoogle Scholar
  20. Ho CH, Tsay YF (2010) Nitrate, ammonium, and potassium sensing and signaling. Curr Opin Plant Biol 13:604–610. doi: 10.1016/j.pbi.2010.08.005 CrossRefPubMedGoogle Scholar
  21. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194. doi: 10.1016/j.cell.2009.07.004 CrossRefPubMedGoogle Scholar
  22. Hsu PK, Tsay YF (2013) Two phloem nitrate transporters, NRT1.11 and NRT1.12, are important for redistributing xylem-borne nitrate to enhance plant growth. Plant Physiol 163:844–856. doi: 10.1104/pp.113.226563 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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
  24. Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proc Natl Acad Sci USA 109:9653–9658. doi: 10.1073/pnas.1203567109 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M, Bréhaut V, Miller A, Daniel-Vedele F, Sakakibara H, Krapp A (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24:245–258. doi: 10.1105/tpc.111.092221 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince AS, Chaillou S, Ferrario-Méry S, Meyer C, Daniel-Vedele F (2014) Nitrate transport and signalling in Arabidopsis. J Exp Bot 65:789–798. doi: 10.1093/jxb/eru001 CrossRefPubMedGoogle Scholar
  27. Krouk G, Tillard P, Gojon A (2006) Regulation of the high-affinity NO3 uptake system by NRT1.1-mediated NO3 demand signaling in Arabidopsis. Plant Physiol 142:1075–1086. doi: 10.1104/pp.106.087510 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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, Rentsch D, Seo M, Tsay YF, Zhang M, Coruzzi G, Lacombe B (2014) A unified nomenclature of nitrate transporter 1/peptide transporter family members in plants. Trends Plant Sci 19:5–9. doi: 10.1016/j.tplants.2013.08.008 CrossRefPubMedGoogle Scholar
  29. Léran S, Edel KH, Pervent M, Hashimoto K, Corratgé-Faillie C, Offenborn JN, Tillard P, Gojon A, Kudla J, Lacombe B (2015) Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci Signal 8:ra43. doi: 10.1126/scisignal.aaa4829 CrossRefPubMedGoogle Scholar
  30. Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Li HM, Huang J, Li LG, Schroeder JI, Gassmann W, Gong JM (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646. doi: 10.1105/tpc.110.075242 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Liang Y, Mitchell DM, Harris JM (2007) Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant. Dev Biol 304:297–307. doi: 10.1016/j.ydbio.2006.12.037 CrossRefPubMedGoogle Scholar
  32. Libault M (2014) The carbon-nitrogen balance of the nodule and its regulation under elevated carbon dioxide concentration. Biomed Res Int 2014:1–7. doi: 10.1155/2014/507946 CrossRefGoogle Scholar
  33. Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK, Tillard P, Lin HL, Wang YY, Tsai CB, Gojon A, Tsay YF (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528. doi: 10.1105/tpc.108.060244 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Linkohr BI, Williamson LC, Fitter AH, Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760CrossRefPubMedGoogle Scholar
  35. 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
  36. Lodwig EM, Hosie AH, Bourdès A, Findlay K, Allaway D, Karunakaran R, Downie JA, Poole PS (2003) Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature 422:722–726. doi: 10.1038/nature01527 CrossRefPubMedGoogle Scholar
  37. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287CrossRefPubMedGoogle Scholar
  38. Marino D, Frendo P, Ladrera R, Zabalza A, Puppo A, Arrese-Igor C, González EM (2007) Nitrogen fixation control under drought stress. Localized or systemic? Plant Physiol 143:1968–1974. doi: 10.1104/pp.106.097139 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Medici A, Krouk G (2014) The Primary Nitrate Response: a multifaceted signalling pathway. J Exp Bot 65:5567–5576. doi: 10.1093/jxb/eru245 CrossRefPubMedGoogle Scholar
  40. Morère-Le Paven MC, Viau L, Hamon A, Vandecasteele C, Pellizzaro A, Bourdin C, Laffont C, Lapied B, Lepetit M, Frugier F, Legros C, Limami AM (2011) Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula. J Exp Bot 62:5595–5605. doi: 10.1093/jxb/err243 CrossRefPubMedGoogle Scholar
  41. Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29CrossRefGoogle Scholar
  42. Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48. doi: 10.1111/j.1469-8137.2008.02751.x CrossRefPubMedGoogle Scholar
  43. Okamoto M, Vidmar JJ, Glass AD (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol 44:304–317CrossRefPubMedGoogle Scholar
  44. Orsel M, Filleur S, Fraisier V, Daniel-Vedele F (2002a) Nitrate transport in plants: which gene and which control? J Exp Bot 53:825–833CrossRefPubMedGoogle Scholar
  45. Orsel M, Krapp A, Daniel-Vedele F (2002b) Analysis of the NRT2 nitrate transporter family in Arabidopsis. Structure and gene expression. Plant Physiol 129:886–896. doi: 10.1104/pp.005280 PubMedGoogle Scholar
  46. Ouyang J, Cai Z, Xia K, Wang Y, Duan J, Zhang M (2010) Identification and analysis of eight peptide transporter homologs in rice. Plant Sci 179:374–382CrossRefGoogle Scholar
  47. Pellizzaro A, Clochard T, Cukier C, Bourdin C, Juchaux M, Montrichard F, Thany S, Raymond V, Planchet E, Limami AM, Morère-Le Paven MC (2014) The nitrate transporter MtNPF6.8 (MtNRT1.3) transports abscisic acid and mediates nitrate regulation of primary root growth in Medicago truncatula. Plant Physiol 166:2152–2165. doi: 10.1104/pp.114.250811 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Pellizzaro A, Clochard T, Planchet E, Limami AM, Morère-Le Paven MC (2015) Identification and molecular characterization of Medicago truncatula NRT2 and NAR2 families. Physiol Plant 154:256–269. doi: 10.1111/ppl.12314 CrossRefPubMedGoogle Scholar
  49. Planchet E, Rannou O, Ricoult C, Boutet-Mercey S, Maia-Grondard A, Limami AM (2011) Nitrogen metabolism responses to water deficit act through both abscisic acid (ABA)-dependent and independent pathways in Medicago truncatula during post-germination. J Exp Bot 62:605–615. doi: 10.1093/jxb/erq294 CrossRefPubMedGoogle Scholar
  50. Planchet E, Verdu I, Delahaie J, Cukier C, Girard C, Morère-Le Paven MC, Limami AM (2014) Abscisic acid-induced nitric oxide and proline accumulation in independent pathways under water-deficit stress during seedling establishment in Medicago truncatula. J Exp Bot 65:2161–2170. doi: 10.1093/jxb/eru088 CrossRefPubMedGoogle Scholar
  51. Saito A, Tanabata S, Tanabata T, Tajima S, Ueno M, Ishikawa S, Ohtake N, Sueyoshi K, Ohyama T (2014) Effect of nitrate on nodule and root growth of soybean (Glycine max (L.) Merr.). Int J Mol Sci 15:4464–4480. doi: 10.3390/ijms15034464 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Salehin M, Huang YS, Bagchi R, Sherrier DJ, Dickstein R (2013) Allelic differences in Medicago truncatula NIP/LATD mutants correlate with their encoded proteins’ transport activities in planta. Plant Signal Behav 8:e22813. doi: 10.4161/psb.22813 CrossRefPubMedGoogle Scholar
  53. Siddiqi MY, Glass AD, Ruth TJ, Fernando M (1989) Studies of the regulation of nitrate influx by barley seedlings using 13NO3 . Plant Physiol 90:806–813CrossRefPubMedPubMedCentralGoogle Scholar
  54. Siddiqi MY, Glass AD, Ruth TJ, Rufty TW (1990) Studies of the uptake of nitrate in barley: I. Kinetics of 13NO3 Influx. Plant Physiol 93:1426–1432CrossRefPubMedPubMedCentralGoogle Scholar
  55. Signora L, De Smet I, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662CrossRefPubMedGoogle Scholar
  56. Tang H, Krishnakumar V, Bidwell S, Rosen B, Chan A, Zhou S, Gentzbittel L, Childs KL, Yandell M, Gundlach H, Mayer KF, Schwartz DC, Town CD (2014) An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics 15:312. doi: 10.1186/1471-2164-15-312 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Tian Q, Chen F, Liu J, Zhang F, Mi G (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J Plant Physiol 165:942–951. doi: 10.1016/j.jplph.2007.02.011 CrossRefPubMedGoogle Scholar
  58. Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713CrossRefPubMedGoogle Scholar
  59. Veereshlingam H, Haynes JG, Penmetsa RV, Cook DR, Sherrier DJ, Dickstein R (2004) nip, a symbiotic Medicago truncatula mutant that forms root nodules with aberrant infection threads and plant defense-like response. Plant Physiol 136:3692–3702. doi: 10.1104/pp.104.049064 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:4477–4482. doi: 10.1073/pnas.0909571107 CrossRefPubMedPubMedCentralGoogle Scholar
  61. von Wittgenstein NJ, Le CH, Hawkins BJ, Ehlting J (2014) Evolutionary classification of ammonium, nitrate, and peptide transporters in land plants. BMC Evol Biol 14:11. doi: 10.1186/1471-2148-14-11 CrossRefGoogle Scholar
  62. Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot 97:875–881. doi: 10.1093/aob/mcj601 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wang YY, Tsay YF (2011) Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell 23:1945–1957. doi: 10.1105/tpc.111.083618 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wang R, Liu D, Crawford NM (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc Natl Acad Sci USA 95:15134–15139CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–567. doi: 10.1104/pp.103.021253 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–467. doi: 10.1016/j.tplants.2012.04.006 CrossRefPubMedGoogle Scholar
  67. Yendrek CR, Lee YC, Morris V, Liang Y, Pislariu CI, Burkart G, Meckfessel MH, Salehin M, Kessler H, Wessler H, Lloyd M, Lutton H, Teillet A, Sherrier DJ, Journet EP, Harris JM, Dickstein R (2010) A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. Plant J 62:100–112. doi: 10.1111/j.1365-313X.2010.04134.x CrossRefPubMedGoogle Scholar
  68. Yokoyama T, Kodama N, Aoshima H, Izu H, Matsushita K, Yamada M (2001) Cloning of a cDNA for a constitutive NRT1 transporter from soybean and comparison of gene expression of soybean NRT1 transporters. Biochim Biophys Acta 1518:79–86CrossRefPubMedGoogle Scholar
  69. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409CrossRefPubMedGoogle Scholar
  70. Zhang H, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59CrossRefPubMedGoogle Scholar
  71. Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534CrossRefPubMedPubMedCentralGoogle Scholar
  72. Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58:2329–2338. doi: 10.1093/jxb/erm114 CrossRefPubMedGoogle Scholar
  73. Zhang C, Bousquet A, Harris JM (2014) Abscisic acid and LATD/NIP modulate root elongation via reactive oxygen species in Medicago truncatula. Plant Physiol 166:644–658. doi: 10.1104/pp.114.248542 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Anthoni Pellizzaro
    • 1
  • Bénédicte Alibert
    • 1
  • Elisabeth Planchet
    • 1
  • Anis M. Limami
    • 1
  • Marie-Christine Morère-Le Paven
    • 1
    Email author
  1. 1.IRHS, Agrocampus Ouest, INRAUniversité d’AngersBeaucouzé CedexFrance

Personalised recommendations