Abstract
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.
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References
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 206:44–52
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 56:295–302
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
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
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
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
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
Crawford NM, Glass AD (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci 3:389–395
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
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
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
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 53:1711–1721
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
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
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
Harris JM (2015) Abscisic acid: hidden architect of root system structure. Plants 4:548–572. doi:10.3390/plants4030548
Harris JM, Dickstein R (2010) Control of root architecture and nodulation by the LATD/NIP transporter. Plant Signal Behav 5:1365–1369
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
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
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
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
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
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 11:1381–1392
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
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
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
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
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
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
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
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
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
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
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 29:751–760
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 11:865–874
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
López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287
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
Medici A, Krouk G (2014) The Primary Nitrate Response: a multifaceted signalling pathway. J Exp Bot 65:5567–5576. doi:10.1093/jxb/eru245
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
Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29
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
Okamoto M, Vidmar JJ, Glass AD (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol 44:304–317
Orsel M, Filleur S, Fraisier V, Daniel-Vedele F (2002a) Nitrate transport in plants: which gene and which control? J Exp Bot 53:825–833
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
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 179:374–382
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
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
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
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
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
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
Siddiqi MY, Glass AD, Ruth TJ, Fernando M (1989) Studies of the regulation of nitrate influx by barley seedlings using 13NO3 −. Plant Physiol 90:806–813
Siddiqi MY, Glass AD, Ruth TJ, Rufty TW (1990) Studies of the uptake of nitrate in barley: I. Kinetics of 13NO3 − Influx. Plant Physiol 93:1426–1432
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 28:655–662
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
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
Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713
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
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
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
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
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
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 95:15134–15139
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
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
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
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 1518:79–86
Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409
Zhang H, Forde BG (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51:51–59
Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534
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
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
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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).
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Pellizzaro, A., Alibert, B., Planchet, E. et al. Nitrate transporters: an overview in legumes. Planta 246, 585–595 (2017). https://doi.org/10.1007/s00425-017-2724-6
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DOI: https://doi.org/10.1007/s00425-017-2724-6