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

Functional Plant Biology

Volumn 41, Issue 4, 2014, Pages 353-365

  Pii, Youry ^a,b   Alessandrini, Massimiliano ^a   Guardini, Katia ^a   Zamboni, Anita ^a   Varanini, Zeno ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b FREE UNIVERSITY OF BOZEN BOLZANO   (Italy)

Author keywords

grapevine physiology; nitrate transporters; nitrogen 15 isotope; proton pump; Vitis vinifera L.

Indexed keywords

ANION; GENE; GENOME; MEMBRANE; NITRATE; NITROGEN ISOTOPE; NUTRIENT; PHYSIOLOGY; PLANT; PLASMA; ROOT SYSTEM;

EID: 84896332777     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP13227     Document Type: Article

References (81)

1. 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. doi:10.1093/nar/25.17.3389
2. 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. doi:10.1007/s004250050372
3. 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. doi:10.1270/jsbbs.56.295
4. Arango M, Gévaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216, 355-365.
5. 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. doi:10.1081/PLN-120021054
6. Bell SJ, Henschke PA (2005) Implication of nitrogen nutrition for grapes, fermentation and wine. Australian Journal of Grape and Wine Research 11, 242-295. doi:10.1111/j.1755-0238.2005.tb00028.x
7. Bouguyon E, Gojon A, Nacry P (2012) Nitrate sensing and signaling in plants. Seminars in Cell & Developmental Biology 23, 648-654. doi:10.1016/j.semcdb.2012.01.004
8. 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. doi:10.1016/0003-2697 (76)90527-3
9. 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. doi:10.1111/j.1744- 7909.2008.00642.x
10. 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. doi:10.1016/S0168-9452(97)00095-2
11. 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. doi:10.1016/S0168-9452(00)00363-0
12. Cerezo M, Tillard P, Filleur S, Munos S, Daniel-Vedele F, Gojon A (2001a) Major alterations of the regulation of rootNO3-uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiology 127, 262-271. doi:10.1104/pp.127.1.262
13. Cerezo M, Tillard P, Gojon A, Primo-Millo E, Garcia-Agustin P (2001b) Characterization and regulation of ammoniumtransport systems in Citrus plants. Planta 214, 97-105. doi:10.1007/s004250100590
14. Christou M, Avramides EJ, Jones DL (2006) Dissolved organic nitrogen dynamics in a Mediterranean vineyard soil. Soil Biology & Biochemistry 38, 2265-2277. doi:10.1016/j.soilbio.2006.01.025
15. Crawford NM, Glass ADM (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 3, 389-395. doi:10.1016/S1360-1385(98)01311-9
16. Daniel-Vedele F, Filleur S, Caboche M (1998) Nitrate transport: a key step in nitrate assimilation. Current Opinion in Plant Biology 1, 235-239. doi:10.1016/S1369-5266(98)80110-6
17. 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. doi:10.1093/jxb/erq403
18. Filleur S, Daniel-VedeleF(1999) Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 207, 461-469. doi:10.1007/s004250050505
19. Filleur S, DorbeMF,CerezoM,OrselM,Granier F, GojonA, Daniel-VedeleF (2001) An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Letters 489, 220-224. doi:10.1016/S0014-5793 (01)02096-8
20. 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. doi:10.1081/PLN-200034662
21. Fischer-Schliebs E, Varanini Z, Lüttge U (1994) Isolation of Hf-transportcompetent plasma membrane vesicles from corn roots by discontinuous sucrose gradient centrifugation: effect of membrane protectant agents. Journal of Plant Physiology 144, 505-512. doi:10.1016/S0176-1617(11) 82130-9
22. 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. doi:10.1016/0003-2697(83)90356-1
23. Forde BG, Clarkson DT (1999) Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Advances in Botanical Research 30, 1-90. doi:10.1016/S0065-2296(08)60226-8
24. Forde BG (2000) Nitrate transporters in plants, structure, function and regulation. Biochimica et Biophysica Acta 1465, 219-235. doi:10.1016/S0005- 2736(00)00140-1
25. 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. doi:10.1046/j.1365-313x.2000. 00813.x
26. García M, Gallego P, Daverede C, IbrahimH(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.
27. 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. doi:10.1016/0003-2697(88) 90056-5
28. Glass ADM, Shaff JE, Kochian LV (1992) Studies on the uptake of nitrate in barley. IV. Electrophysiology. Plant Physiology 99, 456-463. doi:10.1104/pp.99.2.456
29. 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. doi:10.1093/jexbot/53.370.855
30. Gogstad GO, KrutnesMB(1982) Measurement of protein in cell suspensions using the Coomassie brilliant blue die-binding assay. Analytical Biochemistry 126, 355-359. doi:10.1016/0003-2697(82)90527-9
31. 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.
32. Hole DJ, Emran AM, Fares Y, DrewMC(1990) Induction of nitrate transport in maize roots, and kinetics of influx, measured with nitrogen-13. Plant Physiology 93, 642-647. doi:10.1104/pp.93.2.642
33. 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.
34. 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. doi:10.1111/j.1755-0238.2001.tb00188.x
35. 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. doi:10.1105/tpc.111.092221
36. Kronzucker HJ, Siddiqi MY, Glass ADM (1995) Kinetics of NO3-influx in spruce. Plant Physiology 109, 319-326.
37. 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. doi:10.1105/tpc.013516
38. 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. doi:10.1104/pp.106. 091223
39. Marschner P (2011) 'Marschner's mineral nutrition of higher plants.' 3rd edn. (Academic Press: London)
40. Mata C, van Vemde N, Clarkson DT, Martins-LoucaoMA,LambersH(2000) Influx, efflux and net uptake of nitrate in Quercus suber seedlings. Plant and Soil 221, 25-32. doi:10.1023/A:1004785331462
41. 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. doi:10.1104/pp.93.1.281
42. 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. doi:10.1104/pp.93.1.290
43. 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. doi:10.1007/BF00023594
44. 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 doi:10.1007/s11104-013-1645-9
45. 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. doi:10.1093/treephys/27.4. 503
46. 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. doi:10.1023/A: 1024899808018
47. 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. doi:10.1051/agro:2000133
48. 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. doi:10.1186/1471-2229-12-66
49. 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. doi:10.1093/pcp/pcg036
50. Okamoto M, Kumar A, Li W, Wang Y, SiddiqiMY, Crawford NM,GlassAD (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiology 140, 1036-1046. doi:10.1104/pp.105.074385
51. 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.
52. 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. doi:10.1104/pp.106.085209
53. Oufattole M, Arango M, Boutry M (2000) Identification and expression analysis of three new Nicotiana plumbaginifolia genes encoding isoforms of a plasma membraneH+-ATPase, one of which is induced by mechanical stress. Planta 210, 715-722. doi:10.1007/s004250050672
54. Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annual Review of Plant Physiology and Plant Molecular Biology 52, 817-845. doi:10.1146/annurev.arplant.52.1.817
55. 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.
56. 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.
57. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45. doi:10.1093/nar/29.9.e45
58. 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. doi:10.1093/nar/30.9. e36
59. 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. doi:10.1371/journal.pone.0015289
60. 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. doi:10.1093/jxb/erg106
61. 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. doi:10.1023/A:100587 2816881
62. Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumptionfree analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339, 62-66. doi:10.1016/S0304-3940(02) 01423-4
63. 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.
64. 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. doi:10.1093/jxb/erg208
65. 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. doi:10.2307/2265708
66. Schreiner RP, Scagel CF, Baham J (2006) Nutrient uptake and distribution in a mature "Pinot noir" vineyard. HortScience 41, 336-345.
67. 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. doi:10.1007/ BF00009366
68. 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. doi:10.1104/pp.93.4.1426
69. Sorgonà A, AbenavoliMR,CaccoG(2005)Acomparative study between two citrus rootstocks: effect of nitrate on the root morpho-topology and net nitrate uptake. Plant and Soil 270, 257-267. doi:10.1007/s11104-004-1607-3
70. 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. doi:10.1111/j.1365-313X.2004.02310.x
71. 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. doi:10.1104/pp.114.1.137
72. 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. doi:10.1016/0378- 1119(96)00154-0
73. 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. doi:10.1016/0092-8674(93)90399-B
74. Vidmar JJ, Zhuo D, Siddiqi MY, Schjoerring JK, Touraine B, Glass AD (2000) Regulation of high-affinity nitrate transporter genes and highaffinity nitrate influx by nitrogen pools in roots of barley. Plant Physiology 123, 307-318. doi:10.1104/pp.123.1.307
75. 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. doi:10.1104/pp.99.2.794
76. 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. doi:10.1146/annurev. arplant.52.1.659
77. 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. doi:10.1111/j.1365-3040.2011.02335.x
78. 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. doi:10.1016/j.scienta.2006.11.005
79. 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. doi:10.1007/s001220051408
80. 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. doi:10.1016/S0014-5793(00)01085-1
81. 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. doi:10.1046/j.1365-313X. 1999.00396.x