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Plant function and evolutionary biology
RESEARCH ARTICLE

Induction of high-affinity NO3 uptake in grapevine roots is an active process correlated to the expression of specific members of the NRT2 and plasma membrane H+-ATPase gene families

Youry Pii A B , Massimiliano Alessandrini A , Katia Guardini A , Anita Zamboni A C and Zeno Varanini A
+ Author Affiliations
- Author Affiliations

A Biotechnology Department, University of Verona, Strada Le Grazie 15, 37134 Verona, Italy.

B Present address: Faculty of Science and Technology, Free University of Bozen-Bolzano, Piazza Università 5, 39100 Bolzano, Italy.

C Corresponding author. Email: anita.zamboni@univr.it

Functional Plant Biology 41(4) 353-365 https://doi.org/10.1071/FP13227
Submitted: 31 July 2013  Accepted: 17 October 2013   Published: 26 November 2013

Abstract

The phenomenon of NO3 induction in plant roots has been characterised both in herbaceous and woody plants. Grapevine (Vitis vinifera L.) plants, hydroponically grown, showed an increase in NO3 uptake rate in response to anion treatment for different periods in the nutrient solution after 1 week of NO3 deprivation. The expression profile of the two high-affinity NO3 transporters VvNRT2.4A and VvNRT2.4B, and the gene encoding the accessory protein VvNAR2.2 exhibits a similar trend to that of the anion uptake. The induction, also involving the increase in activity and protein levels of plasma membrane H+-ATPase, is correlated with the expression profile of two (VvHA2 and VvHA4) out of eight putative plasma membrane H+-ATPase genes identified in grapevine genome.

Additional keywords: grapevine physiology, nitrate transporters, nitrogen 15 isotope, proton pump, Vitis vinifera L.


References

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFyhu7w%3D&md5=d389894c2f2dfdd4a57a2967cd545b08CAS | 9254694PubMed |

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.
Regulation of GmNRT2 expression and nitrate transport activity in roots of soybean (Glycine max).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvVSiurs%3D&md5=fc5469fa27f0fa637cc9876a41bd14d8CAS | 9715532PubMed |

Araki R, Hasegawa H (2006) Expression of rice (Oryza sativa L.) genes involved in high-affinity nitrate transport during the period of nitrate induction. Breeding Science 56, 295–302.
Expression of rice (Oryza sativa L.) genes involved in high-affinity nitrate transport during the period of nitrate induction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ehs7vM&md5=2dffe9521248df8757d6ff18ec9ea790CAS |

Arango M, Gévaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216, 355–365.

Bavaresco L, Giachino E, Pezzutto S (2003) Grapevine rootstock effects on lime-induced chlorosis, nutrient uptake, and source–sink relationships. Journal of Plant Nutrition 26, 1451–1465.
Grapevine rootstock effects on lime-induced chlorosis, nutrient uptake, and source–sink relationships.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksFeqs7w%3D&md5=01d6d06890bef6882be5f03bc92523f3CAS |

Bell SJ, Henschke PA (2005) Implication of nitrogen nutrition for grapes, fermentation and wine. Australian Journal of Grape and Wine Research 11, 242–295.
Implication of nitrogen nutrition for grapes, fermentation and wine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xks1Ggsg%3D%3D&md5=e3e40f36f0e97150fed7f0c474704cacCAS |

Bouguyon E, Gojon A, Nacry P (2012) Nitrate sensing and signaling in plants. Seminars in Cell & Developmental Biology 23, 648–654.
Nitrate sensing and signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1enurjP&md5=ab9f1bcfdf3d97d4e1dae1df99e2a06fCAS |

Bradford MM (1976) A rapid and sensitive method of quantification of microgram quantities of protein utilizing the principle of protein binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method of quantification of microgram quantities of protein utilizing the principle of protein binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=bead43c1adb6f57157bea3eab849e63cCAS | 942051PubMed |

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. Journal of Integrative Plant Biology 50, 443–451.
Gene structure and expression of the high-affinity nitrate transport system in rice roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlslahu7k%3D&md5=37189dc1c1154d78198606e201d9ca32CAS | 18713378PubMed |

Cerezo M, Garcia-Agustin P, Serna MD, Primo-Millo E (1997) Kinetics of nitrate uptake by Citrus seedlings and inhibitory effects of salinity. Plant Science 126, 105–112.
Kinetics of nitrate uptake by Citrus seedlings and inhibitory effects of salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslWiurY%3D&md5=d891d633fae740a8d069265f182540b4CAS |

Cerezo M, Flors V, Legaz F, García-Agustín P (2000) Characterization of the low affinity transport system for NO3 – uptake by Citrus roots. Plant Science 160, 95–104.
Characterization of the low affinity transport system for NO3 uptake by Citrus roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsVegsA%3D%3D&md5=8c3fcf2de9b5e1b86073cebefcc4b82dCAS | 11164581PubMed |

Cerezo M, Tillard P, Filleur S, Munos S, Daniel-Vedele F, Gojon A (2001a) Major alterations of the regulation of root NO3 – uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiology 127, 262–271.
Major alterations of the regulation of root NO3 uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvFCrtLg%3D&md5=1978efba50ebe4c0e8e58ef4c61a22c2CAS | 11553754PubMed |

Cerezo M, Tillard P, Gojon A, Primo-Millo E, Garcia-Agustin P (2001b) Characterization and regulation of ammonium transport systems in Citrus plants. Planta 214, 97–105.
Characterization and regulation of ammonium transport systems in Citrus plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXotVylsrw%3D&md5=4fe7487255a61070d32d44787adb716eCAS | 11762176PubMed |

Christou M, Avramides EJ, Jones DL (2006) Dissolved organic nitrogen dynamics in a Mediterranean vineyard soil. Soil Biology & Biochemistry 38, 2265–2277.
Dissolved organic nitrogen dynamics in a Mediterranean vineyard soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotFyku74%3D&md5=7b67308eb64712c5b6d95a35a4c651f3CAS |

Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 3, 389–395.
Molecular and physiological aspects of nitrate uptake in plants.Crossref | GoogleScholarGoogle Scholar |

Daniel-Vedele F, Filleur S, Caboche M (1998) Nitrate transport: a key step in nitrate assimilation. Current Opinion in Plant Biology 1, 235–239.
Nitrate transport: a key step in nitrate assimilation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFaku7o%3D&md5=724ca0b8b112041a6c1f297197617c23CAS | 10066586PubMed |

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. Journal of Experimental Botany 62, 2319–2332.
Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1CltLk%3D&md5=e20c33050305a3e1261c27bfef6737a4CAS | 21220781PubMed |

Filleur S, Daniel-Vedele F (1999) Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 207, 461–469.
Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlOgtrY%3D&md5=a315ffe0395880358dafc3766c38ad63CAS | 9951738PubMed |

Filleur S, Dorbe MF, Cerezo M, Orsel M, Granier F, Gojon A, Daniel-Vedele F (2001) An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Letters 489, 220–224.
An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpsF2nsg%3D%3D&md5=6da6590d8319fb9f479f6c8002f44ed4CAS | 11165253PubMed |

Fisarakis J, Nikolaou N, Tsikalas P, Therios I, Stavrakas D (2005) Effect of salinity and rootstock on concentration of potassium, calcium, magnesium, phosphorus, and nitrate-nitrogen in Thompson Seedless grapevine. Journal of Plant Nutrition 27, 2117–2134.
Effect of salinity and rootstock on concentration of potassium, calcium, magnesium, phosphorus, and nitrate-nitrogen in Thompson Seedless grapevine.Crossref | GoogleScholarGoogle Scholar |

Fischer-Schliebs E, Varanini Z, Lüttge U (1994) Isolation of Hf-transport-competent plasma membrane vesicles from corn roots by discontinuous sucrose gradient centrifugation: effect of membrane protectant agents. Journal of Plant Physiology 144, 505–512.
Isolation of Hf-transport-competent plasma membrane vesicles from corn roots by discontinuous sucrose gradient centrifugation: effect of membrane protectant agents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlyqsro%3D&md5=d82a22c702c6a541574fc58cdcbb2634CAS |

Forbush B (1983) Assay of the Na+-, K+-ATPase in plasma membrane preparations: increasing the permeability of membrane vesicles using sodium dodecylsulfate buffered with bovine serum albumine. Analytical Biochemistry 128, 159–163.
Assay of the Na+-, K+-ATPase in plasma membrane preparations: increasing the permeability of membrane vesicles using sodium dodecylsulfate buffered with bovine serum albumine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXmslGqsQ%3D%3D&md5=242af0a2566f1db4db0aad11f4c33db4CAS | 6303151PubMed |

Forde BG, Clarkson DT (1999) Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Advances in Botanical Research 30, 1–90.
Nitrate and ammonium nutrition of plants: physiological and molecular perspectives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltl2rtA%3D%3D&md5=0dad6af0b8ffe2171a1b9e2acd75dcaaCAS |

Forde BG (2000) Nitrate transporters in plants, structure, function and regulation. Biochimica et Biophysica Acta 1465, 219–235.
Nitrate transporters in plants, structure, function and regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Wgt74%3D&md5=fc35bd587be9b97644f0bcb3c61e89d5CAS | 10748256PubMed |

Fraisier V, Gojon A, Tillard P, Daniel-Vedele F (2000) Constitutive expression of a putative high-affinity nitrate transporter in Nicotiana plumbaginifolia: evidence for post-transcriptional regulation by a reduced nitrogen source. The Plant Journal 23, 489–496.
Constitutive expression of a putative high-affinity nitrate transporter in Nicotiana plumbaginifolia: evidence for post-transcriptional regulation by a reduced nitrogen source.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1ehtL8%3D&md5=2d6c931d5e62aa715f56f527aad6b6a6CAS | 10972875PubMed |

García M, Gallego P, Daverede C, Ibrahim H (2001) Effect of three rootstocks on grapevine (Vitis vinifera L) cv. Négrette, grown hydroponically. I. Potassium, calcium and magnesium nutrition. South African Journal of Enology and Viticulture 22, 101–103.

Giannini JL, Ruiz-Christin J, Briskin DP (1988) A small scale procedure for the isolation of transport competent vesicles from plant tissues. Analytical Biochemistry 174, 561–567.
A small scale procedure for the isolation of transport competent vesicles from plant tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXitVKquw%3D%3D&md5=19abb08739a4d1e43b1e5e957be9557cCAS | 3239758PubMed |

Glass ADM, Shaff JE, Kochian LV (1992) Studies on the uptake of nitrate in barley. IV. Electrophysiology. Plant Physiology 99, 456–463.
Studies on the uptake of nitrate in barley. IV. Electrophysiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltlSntLw%3D&md5=1af5629d5898527a5c46021940164617CAS |

Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidamar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. Journal of Experimental Botany 53, 855–864.
The regulation of nitrate and ammonium transport systems in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFSntLc%3D&md5=d1226a2225c103ad083faad076196938CAS |

Gogstad GO, Krutnes MB (1982) Measurement of protein in cell suspensions using the Coomassie brilliant blue die-binding assay. Analytical Biochemistry 126, 355–359.
Measurement of protein in cell suspensions using the Coomassie brilliant blue die-binding assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XmtFWqs7k%3D&md5=799321779552524421cb01e1264e6327CAS | 7158771PubMed |

Grant RS, Matthews MA (1996) The influence of phosphorus availability, scion, and rootstock on grapevine shoot growth, leaf area, and petiole phosphorus concentration. American Journal of Enology and Viticulture 47, 217–224.

Hole DJ, Emran AM, Fares Y, Drew MC (1990) Induction of nitrate transport in maize roots, and kinetics of influx, measured with nitrogen-13. Plant Physiology 93, 642–647.
Induction of nitrate transport in maize roots, and kinetics of influx, measured with nitrogen-13.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslCqu74%3D&md5=9cf66db25c5f3b7aca444644fff96fc7CAS | 16667516PubMed |

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. The Plant Cell 11, 1381–1392.

Keller M, Kummer M, Carmo-Vasconcelos M (2001) Reproductive growth of grapevines in response to nitrogen supply and rootstock. Australian Journal of Grape and Wine Research 7, 12–18.
Reproductive growth of grapevines in response to nitrogen supply and rootstock.Crossref | GoogleScholarGoogle Scholar |

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. The Plant Cell 24, 245–258.
The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOksrc%3D&md5=8cd67f97dd080bc23697160e63e79c3aCAS | 22227893PubMed |

Kronzucker HJ, Siddiqi MY, Glass ADM (1995) Kinetics of NO3 influx in spruce. Plant Physiology 109, 319–326.

Lejay L, Gansel X, Cerezo M, Tillard P, Müller C, Krapp A, von Wirén N, Daniel-Vedele F, Gojon A (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. The Plant Cell 15, 2218–2232.
Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsV2gu78%3D&md5=b1708993218876040813b0c37f2b65e5CAS | 12953122PubMed |

Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass AD (2007) Dissection of the AtNRT2.1 : AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiology 143, 425–433.
Dissection of the AtNRT2.1 : AtNRT2.2 inducible high-affinity nitrate transporter gene cluster.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Olsg%3D%3D&md5=88a54fc19d3a0e36dfd6139e599a1a4eCAS | 17085507PubMed |

Marschner P (2011) ‘Marschner’s mineral nutrition of higher plants.’ 3rd edn. (Academic Press: London)

Mata C, van Vemde N, Clarkson DT, Martins-Loucao MA, Lambers H (2000) Influx, efflux and net uptake of nitrate in Quercus suber seedlings. Plant and Soil 221, 25–32.
Influx, efflux and net uptake of nitrate in Quercus suber seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslynsrk%3D&md5=3b11a502cdb2de13ce063616ba95698dCAS |

McClure PR, Kochian LV, Spanswick RM, Shaff JE (1990a) Evidence for cotransport of nitrate and protons in maize roots. I. Effect of nitrate on the membrane potential. Plant Physiology 93, 281–289.
Evidence for cotransport of nitrate and protons in maize roots. I. Effect of nitrate on the membrane potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXktlOrtb0%3D&md5=1ce98ace9ae4eeca4c5f71441a9eb3f2CAS | 16667448PubMed |

McClure PR, Kochian LV, Spanswick RM, Shaff JE (1990b) Evidence for cotransport of nitrate and protons in maize roots. II. Measurements of NO3 – and H+ fluxes with ion-selective microelectrodes. Plant Physiology 93, 290–294.
Evidence for cotransport of nitrate and protons in maize roots. II. Measurements of NO3 and H+ fluxes with ion-selective microelectrodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXktlOku70%3D&md5=03ca11ffd97f2134c82fb39558fb12cdCAS | 16667449PubMed |

Moriau L, Bogaerts P, Jonniaux JL, Boutry M (1993) Identification and characterization of a second plasma membrane H(+)-ATPase gene subfamily in Nicotiana plumbaginifolia. Plant Molecular Biology 21, 955–963.
Identification and characterization of a second plasma membrane H(+)-ATPase gene subfamily in Nicotiana plumbaginifolia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlalt7c%3D&md5=cd7a96de3bc328ef7ee84d8dee0358f7CAS | 8490141PubMed |

Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant and Soil
Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource.Crossref | GoogleScholarGoogle Scholar |

Nakamura Y, Umemiya Y, Masuda K, Inoue H, Fukumoto M (2007) Molecular cloning and expression analysis of cDNAs encoding a putative Nrt2 nitrate transporter from peach. Tree Physiology 27, 503–510.
Molecular cloning and expression analysis of cDNAs encoding a putative Nrt2 nitrate transporter from peach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsVCgsLg%3D&md5=855dbaf8954c32bb0d22024cd92ea576CAS | 17241992PubMed |

Nazoa P, Vidmar JJ, Tranbarger TJ, Mouline K, Damiani I, Tillard P, Zhuo D, Glass ADM, Touraine B (2003) Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: Responses to nitrate, amino acids and developmental stage. Plant Molecular Biology 52, 689–703.
Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: Responses to nitrate, amino acids and developmental stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFymtrg%3D&md5=6f1299367c62cb4a72a6e97573c825d0CAS | 12956537PubMed |

Nikolaou N, Koukourikou MA, Karagiannidis N (2000) Effects of various rootstocks on xylem exudates cytokinin content, nutrient uptake and growth patterns of grapevine Vitis vinifera L. cv. Thompson Seedless. Agronomie 20, 363–373.
Effects of various rootstocks on xylem exudates cytokinin content, nutrient uptake and growth patterns of grapevine Vitis vinifera L. cv. Thompson Seedless.Crossref | GoogleScholarGoogle Scholar |

Nikolic M, Cesco S, Monte R, Tomasi N, Gottardi S, Zamboni A, Pinton R, Varanini Z (2012) Nitrate transport in cucumber leaves is an inducible process involving an increase in plasma membrane H+-ATPase activity and abundance. BMC Plant Biology 12, 66
Nitrate transport in cucumber leaves is an inducible process involving an increase in plasma membrane H+-ATPase activity and abundance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCgu7bE&md5=6b2a7c652b02645374c6cd04fd3bc297CAS | 22571503PubMed |

Okamoto M, Vidmar JJ, Glass ADM (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant & Cell Physiology 44, 304–317.
Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivVWit7w%3D&md5=f72c124680be18a1c501289d1b857afdCAS |

Okamoto M, Kumar A, Li W, Wang Y, Siddiqi MY, Crawford NM, Glass AD (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiology 140, 1036–1046.
High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xislygs74%3D&md5=8ebc463b15a947ab228b0adf8a3079e1CAS | 16415212PubMed |

Ookura T, Wada M, Sakakibara Y, Jeong KH, Maruta I, Kawamura Y, Kasamo K (1994) Identification and characterization of a family of genes for the plasma membrane H(+)-ATPase of Oryza sativa L. Plant & Cell Physiology 35, 1251–1256.

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 Physiology 142, 1304–1317.
Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein-protein interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1eju7%2FI&md5=1b5533037a15693268362ca001333e4aCAS | 17012411PubMed |

Oufattole M, Arango M, Boutry M (2000) Identification and expression analysis of three new Nicotiana plumbaginifolia genes encoding isoforms of a plasma membrane H+-ATPase, one of which is induced by mechanical stress. Planta 210, 715–722.
Identification and expression analysis of three new Nicotiana plumbaginifolia genes encoding isoforms of a plasma membrane H+-ATPase, one of which is induced by mechanical stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1GjtL8%3D&md5=265607925cfae43ba768cf0de43a63b3CAS | 10805442PubMed |

Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52, 817–845.
Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgtrs%3D&md5=4e091fb047dff12922012645a9867ddbCAS | 11337417PubMed |

Perez C, Michelet B, Ferrant V, Bogaerts P, Boutry M (1992) Differential expression within a three-gene subfamily encoding a plasma membrane H+-ATPase in Nicotiana plumbaginifolia. The Journal of Biological Chemistry 267, 1204–1211.

Peuke AD, Kaiser WM (1996) Nitrate or ammonium uptake and transport, and rapid regulation of nitrate reduction in higher plants. Progress in Botany 57, 93–113.

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=aa80c9eea3a1151f965b4bfe903672daCAS | 11328886PubMed |

Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36
Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Crossref | GoogleScholarGoogle Scholar | 11972351PubMed |

Plett D, Toubia J, Garnett T, Tester M, Kaiser BN, Baumann U (2010) Dichotomy in the NRT gene families of dicots and grass species. PLoS ONE 5, e15289
Dichotomy in the NRT gene families of dicots and grass species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFKlur%2FP&md5=1b6a39d80aef0bb7d1cf495c1d2fe175CAS | 21151904PubMed |

Quaggiotti S, Ruperti B, Borsa P, Destro T, Malagoli M (2003) Expression of a putative high-affinity NO3 – transporter and of a H+-ATPase in relation to whole plant nitrate transport physiology in two maize genotypes differently responsive to low nitrogen availability. Journal of Experimental Botany 54, 1023–1031.
Expression of a putative high-affinity NO3 transporter and of a H+-ATPase in relation to whole plant nitrate transport physiology in two maize genotypes differently responsive to low nitrogen availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFWmsLg%3D&md5=1a7350c4e578f0d0c62eca402d42fdbbCAS | 12598572PubMed |

Quesada A, Krapp A, Trueman LJ, Daniel-Vedele F, Fernandez E, Forde BG, Caboche M (1997) PCR identification of a Nicotiana plumbaginifolia cDNA homologous to the high-affinity nitrate transporters of the crnA family. Plant Molecular Biology 34, 265–274.
PCR identification of a Nicotiana plumbaginifolia cDNA homologous to the high-affinity nitrate transporters of the crnA family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktlWls7s%3D&md5=aa734dda2d5cc7b85dc18f111cd905c1CAS | 9207842PubMed |

Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339, 62–66.
Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhs1Kks70%3D&md5=fc5cb6dd0164c74819dcf67e6757ad3eCAS | 12618301PubMed |

Santi S, Locci G, Pinton R, Cesco S, Varanini Z (1995) Plasma membrane H+-ATPase in maize roots induced for NO3 uptake. Plant Physiology 109, 1277–1283.

Santi S, Locci G, Monte R, Pinton R, Varanini Z (2003) Induction of nitrate uptake in maize roots: expression of a putative high-affinity nitrate transporter and plasma membrane H+-ATPase. Journal of Experimental Botany 54, 1851–1864.
Induction of nitrate uptake in maize roots: expression of a putative high-affinity nitrate transporter and plasma membrane H+-ATPase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsl2ktro%3D&md5=f796beec07efd61250068d1ce2c9f0ccCAS | 12869520PubMed |

Schimel JP, Chapin FS (1996) Tundra plant uptake of amino acid and NH4 + nitrogen in situ: plants compete well for amino acid N1. Ecology 77, 2142–2147.
Tundra plant uptake of amino acid and NH4 + nitrogen in situ: plants compete well for amino acid N1.Crossref | GoogleScholarGoogle Scholar |

Schreiner RP, Scagel CF, Baham J (2006) Nutrient uptake and distribution in a mature “Pinot noir” vineyard. HortScience 41, 336–345.

Serna MD, Borras R, Legaz F, Primo-Millo E (1992) The influence of nitrogen concentration and ammonium/nitrate ratio on N-uptake, mineral composition and yield of citrus. Plant and Soil 147, 13–23.
The influence of nitrogen concentration and ammonium/nitrate ratio on N-uptake, mineral composition and yield of citrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXht1elt7k%3D&md5=5638b425cf247f73952d2d9cf7aea0f9CAS |

Siddiqi MY, Glass ADM, Ruth TJ, Rufty TW (1990) Studies of the uptake of nitrate in barley. I. Kinetics of 13NO3 – influx. Plant Physiology 93, 1426–1432.
Studies of the uptake of nitrate in barley. I. Kinetics of 13NO3 influx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXls12jtLc%3D&md5=a61821b16dcbc89546833018aa0b7042CAS | 16667635PubMed |

Sorgonà A, Abenavoli MR, Cacco G (2005) A comparative study between two citrus rootstocks: effect of nitrate on the root morpho-topology and net nitrate uptake. Plant and Soil 270, 257–267.
A comparative study between two citrus rootstocks: effect of nitrate on the root morpho-topology and net nitrate uptake.Crossref | GoogleScholarGoogle Scholar |

Tong Y, Zhou JJ, Li Z, Miller AJ (2005) A two-component high-affinity nitrate uptake system in barley. The Plant Journal 41, 442–450.
A two-component high-affinity nitrate uptake system in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVKns7c%3D&md5=3df86ab42278fcbffd632d3153bf391aCAS | 15659102PubMed |

Touraine B, Glass AD (1997) NO3 – and ClO3 – fluxes in the chl1–5 mutant of Arabidopsis thaliana. Does the CHL1–5 gene encode a low-affinity NO3 – transporter? Plant Physiology 114, 137–144.
NO3 and ClO3 fluxes in the chl1–5 mutant of Arabidopsis thaliana. Does the CHL1–5 gene encode a low-affinity NO3 transporter?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtlamsb0%3D&md5=c2755afc93efe1135001c7c4eecf03f7CAS | 9159946PubMed |

Trueman LJ, Richardson A, Forde BG (1996) Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene 175, 223–231.
Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtlehtLk%3D&md5=33baa992542a91b7243d4d9499181c85CAS | 8917103PubMed |

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.
The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Oit7k%3D&md5=30f1fd55182936e97987388022dfaeabCAS | 8453665PubMed |

Vidmar JJ, Zhuo D, Siddiqi MY, Schjoerring JK, Touraine B, Glass AD (2000) Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiology 123, 307–318.
Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFems7s%3D&md5=374a3908aeb07047cbdcf1cdce09f417CAS | 10806247PubMed |

Wada M, Takano M, Kasamo K (1992) Nucleotide sequence of a complementary DNA encoding plasma membrane H+-ATPase from rice (Oryza sativa L.). Plant Physiology 99, 794–795.
Nucleotide sequence of a complementary DNA encoding plasma membrane H+-ATPase from rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit12js7o%3D&md5=c2b3927d8dd2930cf0cd8485c381f60bCAS | 16668962PubMed |

Williams LE, Miller AJ (2001) Transporters responsible for the uptake and partitioning of nitrogenous solutes. Annual Review of Plant Physiology and Plant Molecular Biology 52, 659–688.
Transporters responsible for the uptake and partitioning of nitrogenous solutes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWgtr4%3D&md5=82077f595c1ef3e24ef528c7c3894a78CAS | 11337412PubMed |

Yan M, Fan X, Feng H, Miller AJ, Shen Q, Xu G (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 & Environment 34, 1360–1372.
Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOntbvN&md5=57a4edebf6220098dd5027a45b0c6de0CAS |

Yang T, Zhu L, Wang S, Gu W, Huang D, Xu W, Jiang A, Li S (2007) Nitrate uptake kinetics of grapevine under root restriction. Scientia Horticulturae 111, 358–364.
Nitrate uptake kinetics of grapevine under root restriction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqu70%3D&md5=d6b86279b34e2cec59c2c72879764d5aCAS |

Zhang JS, Xie C, Li ZY, Chen SY (1999) Expression of the plasma membrane H+-ATPase gene in response to salt stress in a rice salt-tolerant mutant and its original variety. Theoretical and Applied Genetics 99, 1006–1011.
Expression of the plasma membrane H+-ATPase gene in response to salt stress in a rice salt-tolerant mutant and its original variety.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotVCis7k%3D&md5=d2e4be94436802f460c481c7f3a3b8deCAS |

Zhou JJ, Fernandez E, Galvan A, Miller AJ (2000) A high affinity nitrate transport system from Chlamydomonas requires two gene products. FEBS Letters 466, 225–227.
A high affinity nitrate transport system from Chlamydomonas requires two gene products.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtlCitLo%3D&md5=37329896d2d4b7a3531eb69648ec0973CAS | 10682832PubMed |

Zhuo DG, Okamoto M, Vidmar JJ, Glass ADM (1999) Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. The Plant Journal 17, 563–568.
Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisVKmtr8%3D&md5=d5eefc761830fd222d3bf03f2168d23cCAS |