NO_3~-转运蛋白在植物适应逆境中的功能研究进展
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摘要
氮是植物生长发育所必需的大量元素,参与植物体内各种代谢活动。硝态氮(NO_3~-)是植物可吸收利用的主要无机氮源。NO_3~-转运蛋白不仅介导植物正常生长发育过程中NO_3~-的吸收、转运和再利用,还参与调控植物对多种逆境的适应过程。结合最新报道,重点总结了近年来关于NO_3~-转运蛋白在植物适应低NO_3~-、低K+、盐、干旱及重金属镉等胁迫中的重要作用的研究进展,以期为今后进一步深入探究植物抗逆机理提供依据和参考。
Nitrogen is an essential macronutrient for plants,and involved in various metabolic events. Nitrogen in nitrate(NO_3~- )is the major form of inorganic nitrogen source for plants. NO_3~- transporters not only play a vital role in nitrate uptake,transport and cyclic utilization during the whole growth and development of plants,but also participate in regulating the adversity adaptation in plants. In this review,we highlight recent progresses in studying the functions of NO_3~- transporters in the adaptation of plants to low NO_3~- ,low K+,salt,drought and cadmium stresses,aiming at providing the reference for further exploring the stress resistance mechanisms in plants.
Nitrogen is an essential macronutrient for plants,and involved in various metabolic events. Nitrogen in nitrate(NO_3~- )is the major form of inorganic nitrogen source for plants. NO_3~- transporters not only play a vital role in nitrate uptake,transport and cyclic utilization during the whole growth and development of plants,but also participate in regulating the adversity adaptation in plants. In this review,we highlight recent progresses in studying the functions of NO_3~- transporters in the adaptation of plants to low NO_3~- ,low K+,salt,drought and cadmium stresses,aiming at providing the reference for further exploring the stress resistance mechanisms in plants.
引文
[1]Amtmann A, Armengaud P. Effects of N, P, K and S on metabolism:new knowledge gained from multi-level analysis[J]. Current Opinion in Plant Biology, 2009, 12(3):275-283.
[2]王宇通,邵新庆,黄欣颖,等.植物根系氮吸收过程的研究进展[J].草业科学, 2010, 27(7):105-111.
[3]李建勇,龚继明.植物硝酸根信号感受与传导途径[J].植物生理学报, 2011, 47:111-118.
[4]Crawford NM, Glass ADM. Molecular and physiological aspects of nitrate uptake in plants[J]. Trends in Plant Science, 1998, 3(10):389-395.
[5]Wang YY, Hsu PK, Tsay YF. Uptake, allocation and signaling of nitrate[J]. Trends in Plant Science, 2012, 17(8):458-467.
[6]Xu G, Fan X, Miller AJ. Plant nitrogen assimilation and use efficiency[J]. Annual Review of Plant Biology, 2012, 63(1):153-182.
[7]Wang YY, Cheng YH, Chen KE, et al. Nitrate transport, signaling,and use efficiency[J]. Annual Review of Plant Biology, 2018, 69(1):85-122.
[8]Dechorgnat J, Nguyen CT, Armengaud P, et al. From the soil to the seeds:the long journey of nitrate in plants[J]. Journal of Experimental Botany, 2011, 62(4):1349-1359.
[9]童依平,蔡超,刘全友,等.植物吸收硝态氮的分子生物学进展[J].植物营养与肥料学报, 2004, 10(4):433-440.
[10]李静,张冰玉,苏晓华,等.植物中的铵根及硝酸根转运蛋白研究进展[J].南京林业大学学报:自然科学版, 2012, 36(4):133-139.
[11]马清,管超,夏曾润,等.高等植物氮素转运蛋白研究进展[J].兰州大学学报:自然科学版, 2015, 51(2):217-227.
[12]张合琼,张汉马,梁永书,等.植物硝酸盐转运蛋白研究进展[J].植物生理学报, 2016(2):141-149.
[13]宋田丽,周建建,徐晨曦,等.植物硝酸盐转运蛋白功能及表达调控研究进展[J].上海师范大学学报:自然科学版,2017, 46(5):740-750.
[14]Léran S, Varala K, Boyer JC, et al. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants[J]. Trends in Plant Science, 2014, 19(1):5-9.
[15]Tsay Y, Schroeder JI, Feldmann KA, et al. The herbcide sensitivity gene CHL1 of Arabidopsis encodes a nitrate inducible nitrate transporter[J]. Cell, 1993, 72(5):705-713.
[16]Huang NC, Chiang CS, Crawford NM, et al. CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots[J]. The Plant Cell, 1996, 8(12):2183-2191.
[17]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-aflinity uptake[J]. The Plant Cell, 1999, 11(8):1381-1392.
[18]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 Physiology, 2004, 45(9):1139-1148.
[19]Lin SH, Kuo HF, Canivenc G, et al. Mutation of the Arabidopsis NRT1. 5 nitrate transporter causes defective root-to-shoot nitrate transport[J]. The Plant Cell, 2008, 20(9):2514-2528.
[20]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]. The Plant Cell, 2010, 22(5):1633-1646.
[21]Wang YY, Tsay YF. Arabidopsis nitrate transporter NRT1. 9 is important in phloem nitrate transport[J]. The Plant Cell, 2011,23(5):1945-1957.
[22]Almagro A, Lin SH, Tsay YF. Characterization of the Arabidopsis nitrate transporter NRT1. 6 reveals a role of nitrate in early embryo development.[J]. The Plant Cell, 2008, 20(12):3289-3299.
[23]Liu W, Sun Q, Wang K, et al. Nitrogen Limitation Adaptation(NLA)is involved in source-to-sink remobilization of nitrate by mediating the degradation of NRT1. 7 in Arabidopsis[J]. New Phytologist,2016, 214(2):734-744.
[24]Hsu PK, Tsay YF. Two phloem nitrate transporters, NRT1. 11 and NRT1. 12, are important for redistributing xylem-borne nitrate to enhance plant growth[J]. Plant Physiology, 2013, 163(2):844-856.
[25]Guiboileau A, Sormani R, Meyer C, et al. Senescence and death of plant organs:nutrient recycling and developmental regulation[J]. Comptes Rendus Biologies, 2010, 333(4):382-391.
[26]Gojon A, Gaymard F. Keeping nitrate in the roots:an unexpected requirement for cadmium tolerance in plants[J]. Journal of Molecular Cell Biology, 2010, 2(6):299-301.
[27]Li W, Wang Y, Okamoto M, et al. Dissection of the AtNRT2.1:AtNRT2. 2 inducible high affinity nitrate transporter gene cluster[J]. Plant Physiology, 2007, 143(1):425-433.
[28]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]. The Plant Cell, 2012, 24(1):245-258.
[29]Lezhneva L, Kiba T, Feria BA, et al. The Arabidopsis nitrate transporter NRT2. 5 plays a role in nitrate acquisition and remobilization in nitrogen-starved plants[J]. The Plant Journal,2014, 60(2):230-241.
[30]Zheng D, Han X, An YI, et al. The nitrate transporter NRT2.1 functions in the ethylene response to nitrate deficiency in Arabidopsis[J]. Plant Cell&Environment, 2013, 36(7):1328-1337.
[31]Liu KH, Tsay YF. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation[J].The EMBO Journal, 2003, 22(5):1005-1013.
[32]Ho CH, Lin SH, Hu HC, et al. CHL1 functions as a nitrate sensor in plants[J]. Cell, 2009, 138(3):1184-1194.
[33]Fan X, Feng H, Tan Y, et al. A putative 6-transmembrane nitrate transporter OsNRT1. 1b plays a key role in rice under low nitrogen[J]. Journal of Integrative Plant Biology, 2016, 58(6):590-599.
[34]Wang W, Hu B, Yuan D, et al. Expression of the nitrate transporter gene OsNRT1. 1A/OsNPF6. 3 confers high yield and early maturation in rice[J]. The Plant Cell, 2018, 30(3):638-651.
[35]Krouk G, Crawford NM, Coruzzi GM, et al. Nitrate signaling:adaptation to fluctuating environments[J]. Current Opinion in Plant Biology, 2010, 13(3):266-273.
[36]Walch LP, Forde BG. Nitrate signaling mediated by the NRT1. 1nitrate transporter antagonises L-glutamate-induced changes in root architecture[J]. The Plant Journal, 2008, 54(5):820-828.
[37]Meng S, Peng JS, He YN, et al. Arabidopsis, NRT1. 5 mediates the suppression of nitrate starvation-induced leaf senescence by modulating foliar potassium level[J]. Molecular Plant, 2016, 9(3):461-470.
[38]Drechsler N, Zheng Y, Bohner A, et al. Nitrate-dependent control of shoot K homeostasis by NPF7. 3/NRT1. 5 and SKOR in Arabidopsis[J]. Plant Physiology, 2015, 169(4):2832-2847.
[39]Maathuis FJM. Physiological functions of mineral macronutrients[J]. Current Opinion in Plant Biology, 2009, 12(3):250-258.
[40]Sharma T, Dreyer I, Riedelsberger J. The role of K+channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana[J]. Frontiers in Plant Science, 2013, 4(2):224.
[41]Forde B, Lorenzo H. The nutritional control of root development[J]. Plant&Soil, 2001, 232(1/2):51-68.
[42]LoPez-Bucio J, Cruz-Ram?Rez A, Herrera-Estrella L. The role of nutrient availability in regulating root architecture[J]. Current Opinion in Plant Biology, 2003, 6(3):280-287.
[43]Li H, Yu M, Du XQ, et al. NRT1. 5/NPF7. 3 functions as a proton-coupled H+/K+antiporterforK+loadingintothexylemin Arabidopsis[J]. The Plant Cell, 2017, 29(8):2016-2026.
[44]Zheng Y, Drechsler N, Rausch C, et al. The Arabidopsis nitrate transporter NPF7. 3/NRT1. 5 is involved in lateral root development under potassium deprivation[J]. Plant Signaling&Behavior,2016, 11(5):2832-2847.
[45]Wilkinson S, Davies WJ. ABA-based chemical signaling:the coordination of responses to stress in plants[J]. Plant Cell and Environment, 2002, 25(2):195-210.
[46]Dodd IC, Tan LP, He J. Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation?[J]. Journal of Experimental Botany, 2003, 54:1281-1288.
[47]Schahram B, Sharyar B, Peter W, et al. Improvement of water use and N fertilizer efficiency by subsoil irrigation of winter wheat[J]. European Journal of Agronomy, 2008, 28(1):1-7.
[48]Guo FQ, Young J, Crawford NM. The nitrate transporter AtNRT1. 1(CHL1)functions in stomatal opening and contributes to drought susceptibility in Arabidopsis[J]. The Plant Cell, 2003, 15(1):107-117.
[49]Chen CZ, Lv XF, Li JY, et al. Arabidopsis NRT1. 5 is another essential component in the regulation of nitrate reallocation and stress tolerance[J]. Plant Physiology, 2012, 159:1582-1590.
[50]Taochy C, Gaillard I, Ipotesi E, et al. The Arabidopsis root stele transporter NPF2. 3 contributes to nitrate translocation to shoots under salt stress[J]. Plant Journal for Cell&Molecular Biology,2015, 83(3):466-479.
[51]荆红梅,郑海雷,赵中秋,等.植物对镉胁迫响应的研究进展[J].生态学报, 2001, 21(12):2125-2130.
[52]Zhang GB, Yi HY, Gong JM. The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation[J]. The Plant Cell, 2014, 26(10):3984-3998.
[53]ZimmermannP,Hirsch-HoffmannM,HennigL,etal.GENEVESTIGATOR:Arabidopsis microarray database and analysis toolbox[J]. Plant Physiology, 2004, 136(1):2621-2632.
[2]王宇通,邵新庆,黄欣颖,等.植物根系氮吸收过程的研究进展[J].草业科学, 2010, 27(7):105-111.
[3]李建勇,龚继明.植物硝酸根信号感受与传导途径[J].植物生理学报, 2011, 47:111-118.
[4]Crawford NM, Glass ADM. Molecular and physiological aspects of nitrate uptake in plants[J]. Trends in Plant Science, 1998, 3(10):389-395.
[5]Wang YY, Hsu PK, Tsay YF. Uptake, allocation and signaling of nitrate[J]. Trends in Plant Science, 2012, 17(8):458-467.
[6]Xu G, Fan X, Miller AJ. Plant nitrogen assimilation and use efficiency[J]. Annual Review of Plant Biology, 2012, 63(1):153-182.
[7]Wang YY, Cheng YH, Chen KE, et al. Nitrate transport, signaling,and use efficiency[J]. Annual Review of Plant Biology, 2018, 69(1):85-122.
[8]Dechorgnat J, Nguyen CT, Armengaud P, et al. From the soil to the seeds:the long journey of nitrate in plants[J]. Journal of Experimental Botany, 2011, 62(4):1349-1359.
[9]童依平,蔡超,刘全友,等.植物吸收硝态氮的分子生物学进展[J].植物营养与肥料学报, 2004, 10(4):433-440.
[10]李静,张冰玉,苏晓华,等.植物中的铵根及硝酸根转运蛋白研究进展[J].南京林业大学学报:自然科学版, 2012, 36(4):133-139.
[11]马清,管超,夏曾润,等.高等植物氮素转运蛋白研究进展[J].兰州大学学报:自然科学版, 2015, 51(2):217-227.
[12]张合琼,张汉马,梁永书,等.植物硝酸盐转运蛋白研究进展[J].植物生理学报, 2016(2):141-149.
[13]宋田丽,周建建,徐晨曦,等.植物硝酸盐转运蛋白功能及表达调控研究进展[J].上海师范大学学报:自然科学版,2017, 46(5):740-750.
[14]Léran S, Varala K, Boyer JC, et al. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants[J]. Trends in Plant Science, 2014, 19(1):5-9.
[15]Tsay Y, Schroeder JI, Feldmann KA, et al. The herbcide sensitivity gene CHL1 of Arabidopsis encodes a nitrate inducible nitrate transporter[J]. Cell, 1993, 72(5):705-713.
[16]Huang NC, Chiang CS, Crawford NM, et al. CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots[J]. The Plant Cell, 1996, 8(12):2183-2191.
[17]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-aflinity uptake[J]. The Plant Cell, 1999, 11(8):1381-1392.
[18]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 Physiology, 2004, 45(9):1139-1148.
[19]Lin SH, Kuo HF, Canivenc G, et al. Mutation of the Arabidopsis NRT1. 5 nitrate transporter causes defective root-to-shoot nitrate transport[J]. The Plant Cell, 2008, 20(9):2514-2528.
[20]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]. The Plant Cell, 2010, 22(5):1633-1646.
[21]Wang YY, Tsay YF. Arabidopsis nitrate transporter NRT1. 9 is important in phloem nitrate transport[J]. The Plant Cell, 2011,23(5):1945-1957.
[22]Almagro A, Lin SH, Tsay YF. Characterization of the Arabidopsis nitrate transporter NRT1. 6 reveals a role of nitrate in early embryo development.[J]. The Plant Cell, 2008, 20(12):3289-3299.
[23]Liu W, Sun Q, Wang K, et al. Nitrogen Limitation Adaptation(NLA)is involved in source-to-sink remobilization of nitrate by mediating the degradation of NRT1. 7 in Arabidopsis[J]. New Phytologist,2016, 214(2):734-744.
[24]Hsu PK, Tsay YF. Two phloem nitrate transporters, NRT1. 11 and NRT1. 12, are important for redistributing xylem-borne nitrate to enhance plant growth[J]. Plant Physiology, 2013, 163(2):844-856.
[25]Guiboileau A, Sormani R, Meyer C, et al. Senescence and death of plant organs:nutrient recycling and developmental regulation[J]. Comptes Rendus Biologies, 2010, 333(4):382-391.
[26]Gojon A, Gaymard F. Keeping nitrate in the roots:an unexpected requirement for cadmium tolerance in plants[J]. Journal of Molecular Cell Biology, 2010, 2(6):299-301.
[27]Li W, Wang Y, Okamoto M, et al. Dissection of the AtNRT2.1:AtNRT2. 2 inducible high affinity nitrate transporter gene cluster[J]. Plant Physiology, 2007, 143(1):425-433.
[28]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]. The Plant Cell, 2012, 24(1):245-258.
[29]Lezhneva L, Kiba T, Feria BA, et al. The Arabidopsis nitrate transporter NRT2. 5 plays a role in nitrate acquisition and remobilization in nitrogen-starved plants[J]. The Plant Journal,2014, 60(2):230-241.
[30]Zheng D, Han X, An YI, et al. The nitrate transporter NRT2.1 functions in the ethylene response to nitrate deficiency in Arabidopsis[J]. Plant Cell&Environment, 2013, 36(7):1328-1337.
[31]Liu KH, Tsay YF. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation[J].The EMBO Journal, 2003, 22(5):1005-1013.
[32]Ho CH, Lin SH, Hu HC, et al. CHL1 functions as a nitrate sensor in plants[J]. Cell, 2009, 138(3):1184-1194.
[33]Fan X, Feng H, Tan Y, et al. A putative 6-transmembrane nitrate transporter OsNRT1. 1b plays a key role in rice under low nitrogen[J]. Journal of Integrative Plant Biology, 2016, 58(6):590-599.
[34]Wang W, Hu B, Yuan D, et al. Expression of the nitrate transporter gene OsNRT1. 1A/OsNPF6. 3 confers high yield and early maturation in rice[J]. The Plant Cell, 2018, 30(3):638-651.
[35]Krouk G, Crawford NM, Coruzzi GM, et al. Nitrate signaling:adaptation to fluctuating environments[J]. Current Opinion in Plant Biology, 2010, 13(3):266-273.
[36]Walch LP, Forde BG. Nitrate signaling mediated by the NRT1. 1nitrate transporter antagonises L-glutamate-induced changes in root architecture[J]. The Plant Journal, 2008, 54(5):820-828.
[37]Meng S, Peng JS, He YN, et al. Arabidopsis, NRT1. 5 mediates the suppression of nitrate starvation-induced leaf senescence by modulating foliar potassium level[J]. Molecular Plant, 2016, 9(3):461-470.
[38]Drechsler N, Zheng Y, Bohner A, et al. Nitrate-dependent control of shoot K homeostasis by NPF7. 3/NRT1. 5 and SKOR in Arabidopsis[J]. Plant Physiology, 2015, 169(4):2832-2847.
[39]Maathuis FJM. Physiological functions of mineral macronutrients[J]. Current Opinion in Plant Biology, 2009, 12(3):250-258.
[40]Sharma T, Dreyer I, Riedelsberger J. The role of K+channels in uptake and redistribution of potassium in the model plant Arabidopsis thaliana[J]. Frontiers in Plant Science, 2013, 4(2):224.
[41]Forde B, Lorenzo H. The nutritional control of root development[J]. Plant&Soil, 2001, 232(1/2):51-68.
[42]LoPez-Bucio J, Cruz-Ram?Rez A, Herrera-Estrella L. The role of nutrient availability in regulating root architecture[J]. Current Opinion in Plant Biology, 2003, 6(3):280-287.
[43]Li H, Yu M, Du XQ, et al. NRT1. 5/NPF7. 3 functions as a proton-coupled H+/K+antiporterforK+loadingintothexylemin Arabidopsis[J]. The Plant Cell, 2017, 29(8):2016-2026.
[44]Zheng Y, Drechsler N, Rausch C, et al. The Arabidopsis nitrate transporter NPF7. 3/NRT1. 5 is involved in lateral root development under potassium deprivation[J]. Plant Signaling&Behavior,2016, 11(5):2832-2847.
[45]Wilkinson S, Davies WJ. ABA-based chemical signaling:the coordination of responses to stress in plants[J]. Plant Cell and Environment, 2002, 25(2):195-210.
[46]Dodd IC, Tan LP, He J. Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation?[J]. Journal of Experimental Botany, 2003, 54:1281-1288.
[47]Schahram B, Sharyar B, Peter W, et al. Improvement of water use and N fertilizer efficiency by subsoil irrigation of winter wheat[J]. European Journal of Agronomy, 2008, 28(1):1-7.
[48]Guo FQ, Young J, Crawford NM. The nitrate transporter AtNRT1. 1(CHL1)functions in stomatal opening and contributes to drought susceptibility in Arabidopsis[J]. The Plant Cell, 2003, 15(1):107-117.
[49]Chen CZ, Lv XF, Li JY, et al. Arabidopsis NRT1. 5 is another essential component in the regulation of nitrate reallocation and stress tolerance[J]. Plant Physiology, 2012, 159:1582-1590.
[50]Taochy C, Gaillard I, Ipotesi E, et al. The Arabidopsis root stele transporter NPF2. 3 contributes to nitrate translocation to shoots under salt stress[J]. Plant Journal for Cell&Molecular Biology,2015, 83(3):466-479.
[51]荆红梅,郑海雷,赵中秋,等.植物对镉胁迫响应的研究进展[J].生态学报, 2001, 21(12):2125-2130.
[52]Zhang GB, Yi HY, Gong JM. The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation[J]. The Plant Cell, 2014, 26(10):3984-3998.
[53]ZimmermannP,Hirsch-HoffmannM,HennigL,etal.GENEVESTIGATOR:Arabidopsis microarray database and analysis toolbox[J]. Plant Physiology, 2004, 136(1):2621-2632.