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Frontiers of Agriculture in China

ISSN 1673-7334

ISSN 1673-744X(Online)

CN 11-5729/S

Front Agric Chin    2011, Vol. 5 Issue (3) : 291-298     DOI: 10.1007/s11703-011-1067-5
REVIEW |
Molecular characterization, transcriptional regulation and function analysis of nitrate transporters in plants
Chengjin GUO1, Wensuo CHANG1, Juntao GU2, Xiaojuan LI2, Wenjing LU2, Kai XIAO1()
1. College of Agronomy, Agricultural University of Hebei, Baoding 071001, China; 2. College of Life Sciences, Agricultural University of Hebei, Baoding 071001, China
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Abstract  

Nitrogen (N) is one of the most important inorganic nutrients in plants, and its less availability is an important limiting factor for plant growth in most agricultural systems. In this essay, the following aspects on nitrate transporters (NRT) in plants, such as the uptake features of nitrate(NO3-) mediated by roots, molecular characterization of NRTs, expression patterns and transcription regulation mechanisms of NRT genes, and functions of NRTs in plants, have been reviewed. Further studies of the molecular characterization, expression patterns, transcriptional regulation mechanisms, and functions of plant NRTs will provide a more detailed insight to understand the molecular mechanism of nitrate intake and nitrate transportation in plants. In the meantime, the researches on plant NRTs have potential roles for the improvement of nitrogen use efficiency (NUE) in crop production, as well as for the promotion of sustainable development in the agricultural ecosystem.

Keywords nitrate uptake      nitrate transporter      molecular characterization      transcriptional regulation      function     
Corresponding Authors: XIAO Kai,Email:xiaokai@hebau.edu.cn   
Issue Date: 05 September 2011
URL:  
http://academic.hep.com.cn/fag/EN/10.1007/s11703-011-1067-5     OR     http://academic.hep.com.cn/fag/EN/Y2011/V5/I3/291
1 Agüera E, Haba P, Fontes A G, Maldonado J M (1990). Nitrate and nitrite uptake and reduction by intact sunflower plants. Planta , 182: 149–154
doi: 10.1007/BF00239997
2 Alboresi A, Gestin C, Leydecker M T, Bedu M, Meyer C, Truong H N (2005). Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Environ , 28(4): 500–512
doi: 10.1111/j.1365-3040.2005.01292.x pmid:16229082
3 Almagro A, Lin S H, Tsay Y F (2008). Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell , 20(12): 3289–3299
doi: 10.1105/tpc.107.056788 pmid:19050168
4 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(3): 295–302
doi: 10.1270/jsbbs.56.295
5 Behl R, Tischner R, Raschke K (1988). Induction of a high-capacity nitrate-uptake mechanism in barley roots prompted by nitrate uptake through a constitutive low-capacity mechanism. Planta , 176(2): 235–240
doi: 10.1007/BF00392450
6 Chiu C C, Lin C S, Hsia A P, Su R C, Lin H L, Tsay Y F (2004). Mutation of a nitrate transporter, AtNRT1:4, results in a reduced petiole nitrate content and altered leaf development. Plant Cell Physiol , 45(9): 1139–1148
doi: 10.1093/pcp/pch143 pmid:15509836
7 Chopin F, Orsel M, Dorbe M F, Chardon F, Truong H N, Miller A J, Krapp A, Daniel-Vedele F (2007). The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. Plant Cell , 19(5): 1590–1602
doi: 10.1105/tpc.107.050542 pmid:17540716
8 Fan S C, LinC S, Hsu P K, Lin S H, Tsay Y F (2009). Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell ,21: 2750–2761 .
9 Filleur S, Daniel-Vedele F (1999). Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta , 207(3): 461–469
doi: 10.1007/s004250050505 pmid:9951738
10 Filleur S, Dorbe M F, 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 Lett , 489(2–3): 220–224
doi: 10.1016/S0014-5793(01)02096-8 pmid:11165253
11 Filleur S, Walch-Liu P, Gan Y, Forde B G (2005). Nitrate and glutamate sensing by plant roots. Biochem Soc Trans , 33(1): 283–286
doi: 10.1042/BST0330283 pmid:15667327
12 Forde B G (2000). Nitrate transporters in plants: structure, function and regulation. Biochim Biophys Acta , 1465(1–2): 219–235
doi: 10.1016/S0005-2736(00)00140-1 pmid:10748256
13 Forde B G (2002). Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol , 53(1): 203–224
doi: 10.1146/annurev.arplant.53.100301.135256 pmid:12221973
14 Forde B G, Walch-Liu P (2009). Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant Cell Environ , 32(6): 682–693
doi: 10.1111/j.1365-3040.2008.01927.x pmid:19143987
15 Fritz C, Palacios-Rojas N, Feil R, Stitt M (2006). Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J , 46(4): 533–548
doi: 10.1111/j.1365-313X.2006.02715.x pmid:16640592
16 Galván A, Fernández E (2001). Eukaryotic nitrate and nitrite transporters. Cell Mol Life Sci , 58(2): 225–233 11289304
doi: 10.1007/PL00000850
17 Gan Y, Filleur S, Rahman A, Gotensparre S, Forde B G (2005). Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta , 222(4): 730–742
doi: 10.1007/s00425-005-0020-3 pmid:16021502
18 Glass A D M, Siddiqi M Y (1995). Nitrogen absorption by plants roots. In Srivastava H S, Singh R P, eds. Nitrogen Nutrition in Higher Plants . New Delhi: Associated Publishing, 21–56
19 González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005). PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell , 17(12): 3500–3512
doi: 10.1105/tpc.105.036640 pmid:16284308
20 Good A G, Shrawat A K, Muench D G (2004). Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci , 9(12): 597–605
doi: 10.1016/j.tplants.2004.10.008 pmid:15564127
21 Guo F Q, Wang R, Chen M, Crawford N M (2001). The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell , 13(8): 1761–1777
pmid:11487691
22 Guo F Q, Young J, Crawford N M (2003). The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell , 15(1): 107–117
doi: 10.1105/tpc.006312 pmid:12509525
23 Gutiérrez R A, Gifford M L, Poultney C, Wang R, Shasha D E, Coruzzi G M, Crawford N M (2007a). Insights into the genomic nitrate response using genetics and the Sungear Software System. J Exp Bot , 58(9): 2359–2367
doi: 10.1093/jxb/erm079 pmid:17470441
24 Gutiérrez R A, Lejay L V, Dean A, Chiaromonte F, Shasha D E, Coruzzi G M (2007b). Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol , 8(1): R7.1–7.13
doi: 10.1186/gb-2007-8-1-r7 pmid:17217541
25 Gutiérrez R A, Shasha D E, Coruzzi G M (2005). Systems biology for the virtual plant. Plant Physiol , 138(2): 550–554
doi: 10.1104/pp.104.900150 pmid:15955912
26 Huang N C, Liu K H, Lo H J, Tsay Y F (1999). Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell , 11(8): 1381–1392
pmid:10449574
27 Kawachi T, Sunaga Y, Ebato M, Hatanaka T, Harada H (2006). Repression of nitrate uptake by replacement of Asp105 by asparagine in AtNRT3.1 in Arabidopsis thaliana L. Plant Cell Physiol , 47(10): 1437–1441
doi: 10.1093/pcp/pcl010 pmid:16980702
28 Krapp A, Fraisier V, Scheible W R, Quesada A, Gojon A, Stitt M, Caboche M, Daniel-Vedele F (1998). Expression studies of Nrt2:1Np, a putative high affinity nitrate transporter: evidence for its role in nitrate uptake. Plant J , 14(6): 723–731
doi: 10.1046/j.1365-313x.1998.00181.x
29 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(3): 1075–1086
doi: 10.1104/pp.106.087510 pmid:16998085
30 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. Plant Cell , 15(9): 2218–2232
doi: 10.1105/tpc.013516 pmid:12953122
31 Leydecker M T, Camus I, Daniel-Vedele F, Truong H N (2000). Screening for Arabidopsis mutants affected in the Nii gene expression using the Gus reporter gene. Physiologia Plantarum , 108(2): 161–170
doi: 10.1034/j.1399-3054.2000.108002161.x
32 Li W, Wang Y, Okamoto M, Crawford N M, Siddiqi M Y, Glass A D M (2006). Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol , 143(1): 425–433
doi: 10.1104/pp.106.091223 pmid:17085507
33 Liu K H, Tsay Y F (2003). Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J , 22(5): 1005–1013
doi: 10.1093/emboj/cdg118 pmid:12606566
34 Mu?os S, Cazettes C, Fizames C, Gaymard F, Tillard P, Lepetit M, Lejay L, Gojon A (2004). Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. Plant Cell , 16(9): 2433–2447
doi: 10.1105/tpc.104.024380 pmid:15319483
35 Navarro F J, Machín F, Martín Y, Siverio J M (2006). Down-regulation of eukaryotic nitrate transporter by nitrogen-dependent ubiquitinylation. J Biol Chem , 281(19): 13268–13274
doi: 10.1074/jbc.M601253200 pmid:16543229
36 Nazoa P, Vidmar J J, Tranbarger T J, Mouline K, Damiani I, Tillard P, Zhuo D, Glass A D M, Touraine B (2003). Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: responses to nitrate, amino acids and developmental stage. Plant Mol Biol , 52(3): 689–703
doi: 10.1023/A:1024899808018 pmid:12956537
37 Okamoto M, Kumar A, Li W, Wang Y, Siddiqi M Y, Crawford N M, Glass A D M (2006). High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiol , 140(3): 1036–1046
doi: 10.1104/pp.105.074385 pmid:16415212
38 Okamoto M, Vidmar J J, Glass A D M (2003). Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol , 44(3): 304–317
doi: 10.1093/pcp/pcg036 pmid:12668777
39 Orsel M, Chopin F, Leleu O, Smith S J, Krapp A, Daniel-Vedele F, Miller A J (2006). Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein-protein interaction. Plant Physiol , 142(3): 1304–1317
doi: 10.1104/pp.106.085209 pmid:17012411
40 Orsel M, Chopin F, Leleu O, Smith S J, Krapp A, Daniel-Vedele F, Miller A J (2007). Nitrate signaling and the two component high affinity uptake system in Arabidopsis. Plant Signal Behav , 2(4): 260–262
pmid:19704673
41 Orsel M, Eulenburg K, Krapp A, Daniel-Vedele F (2004). Disruption of the nitrate transporter genes AtNRT2.1 and AtNRT2.2 restricts growth at low external nitrate concentration. Planta , 219(4): 714–721
doi: 10.1007/s00425-004-1266-x pmid:15107992
42 Pao S S, Paulsen I T, Saier M H Jr (1998). Major facilitator superfamily. Microbiol Mol Biol Rev , 62(1): 1–34
pmid:9529885
43 Paulsen I T, Skurray R A (1994). The POT family of transport proteins. Trends Biochem Sci , 19(10): 404
doi: 10.1016/0968-0004(94)90087-6 pmid:7817396
44 Peoples M B, Freney J R, Mosier A R (1995). Minimizing gaseous losses of nitrogen. In Bacon P E, ed. Nitrogen Fertilizer in the Environment . New York: Marcel Dekker, 565–606
45 Quesada A, Galván A, Fernández E (1994). Identification of nitrate transporter genes in Chlamydomonas reinhardtii. Plant J , 5(3): 407–419
doi: 10.1111/j.1365-313X.1994.00407.x pmid:8180624
46 Scheible W R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi M K, Stitt M (2004). Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol , 136(1): 2483–2499
doi: 10.1104/pp.104.047019 pmid:15375205
47 Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible W R, Krapp A (2002). Steps towards an integrated view of nitrogen metabolism. J Exp Bot , 53(370): 959–970
doi: 10.1093/jexbot/53.370.959 pmid:11912238
48 Tillard P, Passama L, Gojon A (1998). Are phloem amino acids involved in the shoot to root control of NO3- uptake in Ricinus communis plants? J Exp Bot , 49(325): 1371–1379
doi: 10.1093/jexbot/49.325.1371
49 Tong Y, Zhou J J, Li Z, Miller A J (2005). A two-component high-affinity nitrate uptake system in barley. Plant J , 41(3): 442–450
doi: 10.1111/j.1365-313X.2004.02310.x pmid:15659102
50 Touraine B, Glass A D M (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 Physiol , 114(1): 137–144
doi: 10.1104/pp.114.1.137 pmid:9159946
51 Trueman L J, Richardson A, Forde B.G (1996). Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene , 175(1–2): 223–231
doi: 10.1016/0378-1119(96)00154-0 pmid:8917103
52 Tsay Y F, Chiu C C, Tsai C B, Ho C H, Hsu P K (2007). Nitrate transporters and peptide transporters. FEBS Lett , 581(12): 2290–2300
doi: 10.1016/j.febslet.2007.04.047 pmid:17481610
53 Tsay Y F, Schroeder J I, Feldmann K A, Crawford N M (1993). The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell , 72(5): 705–713
doi: 10.1016/0092-8674(93)90399-B pmid:8453665
54 Unkles S E, Hawker K L, Grieve C, Campbell E I, Montague P, Kinghorn J R (1991). crnA encodes a nitrate transporter in Aspergillus nidulans. Proc Natl Acad Sci USA , 88(1): 204–208
doi: 10.1073/pnas.88.1.204 pmid:1986367
55 Vidmar J J, Zhuo D, Siddiqi M Y, Schjoerring J K, Touraine B, Glass A D M (2000). Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiol , 123(1): 307–318
doi: 10.1104/pp.123.1.307 pmid:10806247
56 Walch-Liu P, Filleur S, Gan Y, Forde B G (2005). Signaling mechanisms integrating root and shoot responses to changes in the nitrogen supply. Photosynth Res , 83: 239–250 .
57 Walch-Liu P, Ivanov I I, Filleur S, Gan Y, Remans T, Forde B G (2006). Nitrogen regulation of root branching. Ann Bot (Lond) , 97(5): 875–881
doi: 10.1093/aob/mcj601 pmid:16339770
58 Wang R, Guegler K, LaBrie S T, Crawford N M (2000). Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell , 12(8): 1491–1509
pmid:10948265
59 Wang R, Okamoto M, Xing X, Crawford N M (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(2): 556–567
doi: 10.1104/pp.103.021253 pmid:12805587
60 Wang R, Tischner R, Gutiérrez R A, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford N M (2004). Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol , 136(1): 2512–2522
doi: 10.1104/pp.104.044610 pmid:15333754
61 Wang R, Xing X, Crawford N (2007). Nitrite acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiol , 145(4): 1735–1745
doi: 10.1104/pp.107.108944 pmid:17951451
62 Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004). Metabolic engineering with Dof1 transcription factor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA , 101(20): 7833–7838
doi: 10.1073/pnas.0402267101 pmid:15136740
63 Zhang H M, Forde B G (1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science , 279(5349): 407–409
doi: 10.1126/science.279.5349.407 pmid:9430595
64 Zhang H, Forde B G (2000). Regulation of Arabidopsis root development by nitrate availability. J Exp Bot , 51(342): 51–59
doi: 10.1093/jexbot/51.342.51 pmid:10938795
65 Zhou J J, Fernández E, Galván A, Miller A J (2000a). A high affinity nitrate transport system from Chlamydomonas requires two gene products. FEBS Lett , 466(2–3): 225–227
doi: 10.1016/S0014-5793(00)01085-1 pmid:10682832
66 Zhuo D, Okamoto M, Vidmar J J, Glass A D M (1999). Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. Plant J , 17(5): 563–568
doi: 10.1046/j.1365-313X.1999.00396.x pmid:10205909
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