高等植物硝酸盐转运蛋白的功能及其调控机制

摘要/Abstract

摘要： 硝酸盐是植物从土壤中吸收的重要无机氮素形态。植物为适应含有不同浓度NO₃^-的土壤环境，进化出了高亲和硝酸盐转运系统（HATS）和低亲和硝酸盐转运系统（LATS），两个基因家族NRT1和NRT2家族分别参与了LATS和HATS的NO₃^-的吸收和转运。近年来，随着分子生物学技术和植物基因组学的快速发展，研究人员克隆出了大量参与硝酸盐吸收和转运的基因，并对这些基因的功能进行了深入研究，逐渐形成了复杂的硝酸盐调控网络。综述了植物中硝酸盐转运蛋白基因的克隆、表达及调控，并对进一步的研究作了展望，这些结果对于理解植物硝酸盐吸收的调控机制具有重要作用。

关键词: 高等植物, 硝酸盐转运蛋白, 调控机制, 进展

Abstract: Nitrate（NO₃^-）is main nitrogen sources which plants absorb from soil. There are two different uptake systems in plants to cope with low or high NO₃^-concentrations in soil, the high affinity systems（HATS）and low affinity NO₃^-uptake systems（LATS）. It is suggested that NRT1 and NRT2 families contribute to LATS and HATS for both NO₃^-uptake and distribution within the plant. Specific transport systems are essential for the uptake of NO₃^- and for its internal redistribution within plant. Over the past years, a significant advance has been obtained on the gene cloning, expression regulation and functional characterization of NRT1/2 transporters in higher plants. In this article, the research progresses on molecular level of known Nitrate transporters in higher plant in last decade were reviewed.

Key words: Higher plants, Nitrate transporters, Regulation mechanism, Recent advances

贾宏昉, 张洪映, 刘维智, 崔红, 刘国顺. 高等植物硝酸盐转运蛋白的功能及其调控机制[J]. 生物技术通报, 2014, 0(6): 14-21.

Jia Hongfang, Zhang Hongying, Liu Weizhi, Cui Hong, Liu Guoshun. Function and Regulation Mechanisms of Nitrate Transporters in Higher Plants[J]. Biotechnology Bulletin, 2014, 0(6): 14-21.

参考文献

[1] Singh B, Sekhon GS. Agriculture and enviroment[M] . New York：Marcel Dekker, 1990：357-398.
[2] Wang YY, Hsu PK, Tsay YF. Uptake, allocation and signaling of nitrate[J] . Trends in Plant Science, 2012, 17（8）：458-467.
[3] Guo FQ, Yong J, Crawford NM. The nitrate transporter AtNRT1.1（CHL1）functions in stomatal opening and contributes to drought susceptibility in Arabidopsis[J] . Plant Cell, 2003, 15（1）：107-118.
[4] Ho CH, Lin SH, Hu H, et al. CHL1 functions as a nitrate sensor in plants[J] . Cell, 2009, 138（11）：1184-1194.
[5] Forde BG. Nitrate transporters in plants：structure, function and regulation[J] . Biochimica Biophysica Acta, 2000, 1465（12）：219-235.
[6] Williams LE, Miller AJ. Transporters responsible for the uptake and partitioning of nitrogenous solutes[J] . Annu Rev Plant Physiol Plant Mol Biol, 2001, 52（1）：659-688.
[7] Wang YY, Hsu PK, Tsay YF. Uptake, allocation and signaling of nitrate[J] . Trends Plant Sci, 2012, 17（8）：458-467.
[8] Liu KH, Huang CY, Tsay YF. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake[J] . Plant Cell, 1999, 11（5）：865-874.
[9] Huang NC, Liu KH, Lo HJ, et al. Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake[J] . Plant Cell, 1999, 11（8）：1381-1392.
[10] Chiu CC, LIN CS, Hsia AP, et al. Mutation of a nitrate transporter, AtNRT1：4, results in a reduced petiole nitrate content and altered leaf development[J] . Plant Cell and Physiology, 2004, 45（9）：1139-1148.
[11] Lin SH, Kuo HF, Canivenc G, et al. Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport[J] . Plant Cell, 2008, 20（9）：2514-2528.
[12] Li JY, Fu YL, Pike SM, et al. The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance[J] . Plant Cell, 2010, 22（3）：1633-1646.
[13] Almagro A, Lin SH, Tsay YF. Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development[J] . Plant Cell, 2008, 20（12）：3289-3299.
[14] Fan SC, Lin CS, Hsu PK, et al. The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate[J] . Plant Cell, 2009, 21（5）：2750-2761.
[15] Wang YY, Tsay YF. Arabidopsis nitrate transporter NRT 1.9 is important in phloem nitrate transport[J] . Plant Cell, 2011, 23（5）：1945-1957.
[16] Araki R, Hasegawa H. Expression of rice（Oryza sativa L.）genes involved in high-affinity nitrate transport during the period of nitrate induction[J] . Breeding Science, 2006, 56（1）：295-302.
[17] Liu KH, Huang CY, Tsay YF. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake[J] . Plant Cell, 1999, 11（5）：865-874.
[18] Liu KH, Tsay YF. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation[J] . EMBO J, 2003, 22（5）：1005-1013.
[19] Morère-Le, Paven MC, Viau L, Hamon A, et al. Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula[J] . J Exp Bot, 2011, 62（15）：5595-5605.
[20] Unkles SE, Hawker KL, Grieve C, et al. CrnAencodes a nitrate transporter in Aspergillus nidulans[J] . Proc Natl Acad Sci USA, 1991, 88（1）：204-208.
[21] McClure PE, Kochian LV, Spanswick RM, et al. Evidence for cotransport of nitrate and protons in maize roots[J] . Plant Physiology, 1990, 93（1）：281-289.
[22] Zhou JJ, Trueman LJ, Boorer KJ, et al. A high-affinity fungal nitrate carrier with two transport mechanisms[J] . J Biol Chem, 2000, 275（51）：39894-39899.
[23] Quesada A, Galvan A, Fernandez E. Identification of nitrate transporter genes in Chlamydomonas reinhardtii[J] . Plant Journal, 1994, 5（3）：407-419.
[24] Sakamoto T, Inoue SK, Bryant DA. A novel nitrate/nitrite permease in the marine Cyanobacterium synechococcus sp. strain PCC7002 [J] . Journal Bacteriol, 1999, 181（23）：7363-7372.
[25] Trueman LJ, Richardson A, Forde BG. Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlam-ydomonas reinhardtii[J] . Gene, 1996, 175（1-2）：223-231.
[26] Yan M, Fan XR, Feng HM, et al. Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges[J] . Plant Cell and Environment, 2011, 34（8）：1360-1372.
[27] Xu G, Fan X, Miller AJ. Plant nitrogen assimilation and use efficiency[J] . Annu Rev Plant Biol, 2012, 63（1）：153-82.
[28] Tang Z, Fan XR, Li Q, et al. Knock down of a rice stellar nitrate transporter alters long distance translocation but not root influx[J] . Plant Physiology, 2012, 160（4）：2052-2063.
[29] Zhou JJ, Fernandez E, Galvan A, et al. A high affinity nitrate transport system from Chlamydomonas requires two gene products[J] . FEBS Letter, 2000, 466（2-3）：225-227.
[30] Tong YP, Zhou JJ, Li ZS, et al. A two-component high-affinity nitrate uptake system in barley[J] . Plant J, 2005, 41（3）：442-450.
[31] Orsel M, Chopin F, Leleu O, et al. Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein-protein interaction[J] . Plant Physiology, 2006, 142（3）：1304-1317.
[32] Ishikawa S, Ito Y, Sato Y, et al. Two-component high-affinity nitrate transport system in barley：membrane localization, protein expression in roots and a direct protein-protein interaction[J] . Plant Biotech, 2009, 26（2）：197-205.
[33] Yong Z, Kotur Z, Glass ADM. Two-component high-affinity nitrate transport system in barley：membrane localization, protein expression in roots and a direct protein-protein interaction[J] . Plant Journal, 2010, 63（2）：739-748.
[34] Kotur Z, Mackenzie N, Ramesh S, et al. Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1[J] . New Phytologist, 2012, 194（3）：724-31.
[35] Guo FQ, Wang RC, Chen MS, et al. The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1（CHL1）is activated and functions in nascent organ development during vegetative and reproductive growth[J] . Plant Cell, 2001, 13（8）：1761-1778.
[36] Mu?os S, Cazettes C, Fizames C, et al. 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[J] . Plant Cell, 2004, 16（9）：2433-2447.
[37] Li JY, Fu YL, Pike SM, et al. The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance[J] . Plant Cell, 2010, 22（5）：1633-1646.
[38] Zhang HM, Forde BG. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture[J] . Science, 1998, 279（5349）：407-409.
[39] Little DY, Rao H, Oliva S, et al. The putative high-affinity nitate transporter NRT2.1 represses lateral root initiation in response to nutritional cues[J] . Proc Natl Acad Sci USA, 2005, 102（38）：13693-13698.
[40] Remans T, Nacry P, Pervent M, et al. A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis[J] . Plant Physiology, 2006, 140（3）：909-921.
[41] Filleur S, Daniel VF. Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display[J] . Planta, 1999, 207（3）：461-469.
[42] Vidmar JJ, Zhuo D, Siddiqi MY, et al. Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley[J] . Plant Physiology, 2000, 123（1）：307-318.
[43] Laugier E, Bouguyon E, Mauries A, et al. Regulation of high-affinity nitrate uptake in roots of Arabidopsis depends predominantly on posttranscriptional control of the NRT2.1/NAR2.1 transport system[J] . Plant Physiology, 2012, 158（2）：1067-1078.
[44] Zhou JJ, Theodoulou FL, Muldin I, et al. Cloning and functional characterization of a Brassica napus transporter which is able to transport nitrate and histidine[J] . Journal of Biological Chemistry, 1998, 273（20）：12017-12023.
[45] Lejay L, Tillard P, Lepetit M, et al. Molecular and functional regulation of two NO₃^- uptake systems by N and C status of Arabidopsis plants[J] . Plant Journal, 1999, 18（5）：509-519.
[46] Liu KH, Tsay YF. Switching between the two actions modes of the dual-affinity nitrate transporter CHL1 by phosphorylation[J] . EMBO Journal, 2003, 22（5）：1005-1013.
[47] Huang NC, Chiang CS, Crawford, et al. CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots[J] . Plant Cell, 1996, 8（12）：2183-2191.
[48] Lejay L, Wirth J, Pervent M, et al. Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis[J] . Plant Physiology, 2008, 146（4）：2036-2053.
[49] Okamoto M, Vidmar JJ, Glass ADM. Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana：Responses to nitrate provision[J] . Plant Cell Physiology, 2003, 44（3）：304-317.
[50] Girin T, Lejay L, Wirth J, et al. Identification of a 150 bp cis-acting element of the AtNRT2.1 promoter involved in the regulation of gene expression by the N and C status of the plant[J] . Plant Cell and Environment, 2007, 30（11）：1366-1380.
[51] Wirth J, Chopin F, Santoni V, et al. Regulation of root nitrate uptake at the NRT2.1 protein level in Arabidopsis thaliana[J] . J Biol Chem, 2007, 282（1）：23541-23552.
[52] Orsel M, Krapp A, Daniel-Vedele F. Analysis of the NRT2 nitrate transporter family in Arabidopsis. Structure and gene expression[J] . Plant Physiology, 2002, 129（2）：886-896.
[53] Kiba T, Feria-Bourrellier A, Lafouge F, et al. The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants[J] . Plant Cell, 2012, 24（1）：245-258.
[54] Pourtau N, Jennings R, Pelzer E, et al. Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis[J] . Planta, 2006, 224（3）：556-568.
[55] Trevisan S, Borsa P, Botton A, et al. Expression of two maize putative nitrate transporters in response to nitrate and sugar availability[J] . Plant Biology, 2008, 10（4）：462-475.
[56] Feng HM, Yan M, Fan XR, et al. Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status[J] . J Exp Bot, 2011, 62（7）：2319-2332.
[57] Rastogi R, Bate NJ, Sivasankar S, et al. Foot printing of the spinach nitrite reductase gene promoter reveals the preservation of nitrate regulatory elements between fungi and higher plants[J] . Plant Molecular Biology, 1997, 34（3）：465-476.
[58] Konishi M, Yanagisawa S. Identification of a nitrate-responsive cis-element in the Arabidopsis NIR1 promoter defines the presence of multiple cis-regulatory elements for nitrogen response[J] . Plant Journal, 2010, 63（2）：269-282.
[59] Marzluf GA. Genetic regulation of nitrogen metabolism in the fungi[J] . Microbiology and Molecular Biology Reviews, 1997, 61（1）：17-32.