Research Progress on the HAK Function of Plant High Affinity Potassium Ion Transporter

doi:10.13560/j.cnki.biotech.bull.1985.2020-0152

Abstract

Abstract: Potassium（K）is an important nutrient element for plant growth and development,and known as the “stress-resistant element” and “quality element”. In low-potassium environments,plants mainly use high-affinity transporters to absorb and transport potassium ions. The KUP/HAK/KT family,the largest high-affinity potassium transport family in the plant,plays a key role in the affinity transport of potassium ions. Here we descripted the basic situation and classification of the KUP/ HAK/KT family of plants,the phylogenetic analysis of the high-affinity potassium ion transporter HAK,the functional studies of the HAK transporter in increasing plant potassium absorption,affecting plant growth and development,and enhancing plant capabilities of resisting biological stress and abiotic stress. Finally,we prospected the to-be-solved issues related to the potassium ion transporter HAK. The deep understanding of the mechanism of plant HAK potassium transporters is of great practical significance in improving the efficiency of potassium fertilizer using,increasing crop yield and quality,and promoting agricultural development.

Key words: potassium ion, high affinity potassium transporter, HAK

SU Wen, LIU Jing, WANG Bing, LI Wei, DAI Liang-ying. Research Progress on the HAK Function of Plant High Affinity Potassium Ion Transporter[J]. Biotechnology Bulletin, 2020, 36(8): 144-152.

References

[1] Leigh RA, Wyn Jones RG.A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell[J]. New Phytologist, 1984, 97(1):1-13.
[2] 徐赫韩, 侯国媛, 李洋, 等. 植物钾离子通道 AKT1 的研究进展[J]. 生物技术, 2018, 28(2):200-204.
Xu HH, Hou GY, Li Y, et al.Research progress of plant potassium channel AKT1[J]. Biotechnology, 2018, 8(2):200-204, 150.
[3] Zörb C, Senbayram M, Peiter E.Potassium in agriculture-status and perspectives[J]. Journal of Plant Physiology, 2014, 171(9):656-669.
[4] Kollist H, Nuhkat M, Roelfsema MR.Closing gaps:linking elements that control stomatal movement[J]. New Phytologist, 2014, 203(1):44-62.
[5] Wang Y, Wu WH.Potassium transport and signaling in higher plants[J]. Annual Review of Plant Biology, 2013, 64:451-476.
[6] Wang Y, Lü J, Chen D, et al.Genome-wide identification, evolution, and expression analysis of the KT/HAK/KUP family in pear[J]. Genome, 2018, 61(10):755-765.
[7] Rubio F, Nieves-Cordones M, Horie T, et al.Doing ‘business as usual’comes with a cost:evaluating energy cost of maintaining plant intracellular K+ homeostasis under saline conditions[J]. New Phytologist, 2020, 225(3):1097-1104.
[8] Véry AA, Nieves-Cordones M, Daly M, et al.Molecular biology of K+ transport across the plant cell membrane:what do we learn from comparison between plant species?[J]. Journal of Plant Physiology, 2014, 171(9):748-769.
[9] Yang T, Zhang S, Hu Y, et al.The role of a potassium transporter OsHAK5 in potassium acquisition and transport from roots to shoots in rice at low potassium supply levels[J]. Plant Physiology, 2014, 166(2):945-959.
[10] He C, Cui K, Duan A, et al.Genome-wide and molecular evolution analysis of the Poplar KT/HAK/KUP potassium transporter gene family[J]. Ecology and Evolution, 2012, 2(8):1996-2004.
[11] Song Z, Wu X, Gao Y, et al.Genome-wide analysis of the HAK potassium transporter gene family reveals asymmetrical evolution in tobacco(Nicotiana tabacum)[J]. Genome, 2019, 62(4):267-278.
[12] Ahn SJ, Shin R, Schachtman DP.Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake[J]. Plant Physiology, 2004, 134(3):1135-1145.
[13] Chen G, Hu Q, Luo LE, et al.Rice potassium transporter OsHAK1 is essential for maintaining potassium-mediated growth and functions in salt tolerance over low and high potassium concentration ranges[J]. Plant, Cell & Environment, 2015, 38(12):2747-2765.
[14] Nieves-Cordones M, Ródenas R, Chavanieu A, et al.Uneven HAK/KUP/KT protein diversity among angiosperms:species distribution and perspectives[J]. Frontiers in Plant Science, 2016, 7:127.
[15] Ou W, Mao X, Huang C, et al.Genome-wide identification and expression analysis of the KUP family under abiotic stress in cassava(Manihot esculenta Crantz)[J]. Frontiers in Physiology, 2018, 9:17.
[16] Horie T, Brodsky DE, Costa A, et al.K+ transport by the OsHKT2;4 transporter from rice with atypical Na+ transport properties and competition in permeation of K+ over Mg²+ and Ca²+ ions[J]. Plant Physiology, 2011, 156(3):1493-1507.
[17] Takahashi R, Nishio T, Ichizen N, et al.High-affinity K+ transporter PhaHAK5 is expressed only in salt-sensitive reed plants and shows Na+ permeability under NaCl stress[J]. Plant Cell Reports, 2007, 26(9):1673-1679.
[18] Cheng X, Liu X, Mao W, et al.Genome-wide identification and analysis of HAK/KUP/KT potassium transporters gene family in wheat(Triticum aestivum L.)[J]. International Journal of Molecular Sciences, 2018, 19(12):3969.
[19] Desbrosses G, Josefsson C, Rigas S, et al.AKT1 and TRH1 are required during root hair elongation in Arabidopsis[J]. Journal of Experimental Botany, 2003, 54(383):781-788.
[20] Vicente-Agullo F, Rigas S, Desbrosses G, et al.Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots[J]. The Plant Journal, 2004, 40(4):523-535.
[21] Santa-María GE, Rubio F, Dubcovsky J, et al.The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter[J]. The Plant Cell, 1997, 9(12):2281-2289.
[22] Very AA, Sentenac H.Molecular mechanisms and regulation of K+ transport in higher plants[J]. Annual Review of Plant Biology, 2003, 54(1):575-603.
[23] Kim EJ, Kwak JM, Uozumi N, et al.AtKUP1:an Arabidopsis gene encoding high-affinity potassium transport activity[J]. The Plant Cell, 1998, 10(1):51-62.
[24] Li W, Xu G, Alli A, et al.Plant HAK/KUP/KT K+ transporters:function and regulation[C]//Seminars in Cell & Developmental Biology. Academic Press, 2018, 74:133-141.
[25] Okada T, Yamane S, Yamaguchi M, et al.Characterization of rice KT/HAK/KUP potassium transporters and K+ uptake by HAK1 from Oryza sativa[J]. Plant Biotechnology, 2018, 35:101-111.
[26] Feng H, Tang Q, Cai J, et al.Rice OsHAK16 functions in potassium uptake and translocation in shoot, maintaining potassium homeostasis and salt tolerance[J]. Planta, 2019, 250(2):549-561.
[27] Banuelos MA, Garciadeblas B, Cubero B, et al.Inventory and functional characterization of the HAK potassium transporters of rice[J]. Plant Physiology, 2002, 130(2):784-795.
[28] Shen Y, Shen L, Shen Z, et al.The potassium transporter OsHAK21 functions in the maintenance of ion homeostasis and tolerance to salt stress in rice[J]. Plant, Cell & Environment, 2015, 38(12):2766-2779.
[29] Gierth M, Mäser P, Schroeder JI.The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots[J]. Plant Physiology, 2005, 137(3):1105-1114.
[30] Shin R, Schachtman DP.Hydrogen peroxide mediates plant root cell response to nutrient deprivation[J]. Proceedings of the National Academy of Sciences, 2004, 101(23):8827-8832.
[31] Martínez-Cordero MA, Martínez V, Rubio F.Cloning and functional characterization of the high-affinity K+ transporter HAK1 of pepper[J]. Plant Molecular Biology, 2004, 56(3):413-421.
[32] Nieves-Cordones M, Miller AJ, Alemán F, et al.A putative role for the plasma membrane potential in the control of the expression of the gene encoding the tomato high-affinity potassium transporter HAK5[J]. Plant Molecular Biology, 2008, 68(6):521.
[33] Alemán F, Nieves-Cordones M, Martínez V, et al.Differential regulation of the HAK5 genes encoding the high-affinity K+ transporters of Thellungiella halophila and Arabidopsis thaliana[J]. Environmental and Experimental Botany, 2009, 65(2-3):263-269.
[34] Santa-María GE, Rubio F, Dubcovsky J, et al.The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter[J]. The Plant Cell, 1997, 9(12):2281-2289.
[35] Boscari A, Clement M, Volkov V, et al.Potassium channels in barley:cloning, functional characterization and expression analyses in relation to leaf growth and development[J]. Plant, Cell & Environment, 2009, 32(12):1761-1777.
[36] Su H, Golldack D, Zhao C, et al.The expression of HAK-type K+ transporters is regulated in response to salinity stress in common ice plant[J]. Plant Physiology, 2002, 129(4):1482-1493.
[37] Su Q, Feng S, An L, et al.Cloning and functional expression in Saccharomyces cereviae of a K+ transporter, AlHAK, from the graminaceous halophyte, Aeluropus littoralis[J]. Biotechnology Letters, 2007, 29(12):1959-1963.
[38] Takahashi R, Nishio T, Ichizen N, et al.Cloning and functional analysis of the K+ transporter, PhaHAK2, from salt-sensitive and salt-tolerant reed plants[J]. Biotechnology Letters, 2007, 29(3):501-506.
[39] Garciadeblas B, Benito B, Rodríguez-Navarro A.Molecular cloning and functional expression in bacteria of the potassium transporters CnHAK1 and CnHAK2 of the seagrass Cymodocea nodosa[J]. Plant Molecular Biology, 2002, 50(4-5):623-633.
[40] Guo Z, Yang Q, Wan X, et al.Functional characterization of a potassium transporter gene NrHAK1 in Nicotiana rustica[J]. Journal of Zhejiang University Science B, 2008, 9(12):944-952.
[41] Chen G, Zhang Y, Ruan B, et al.OsHAK1 controls the vegetative growth and panicle fertility of rice by its effect on potassium-mediated sugar metabolism[J]. Plant Science, 2018, 274:261-270.
[42] Zhang H, Xiao W, Yu W, et al.Foxtail millet SiHAK1 excites extreme high-affinity K+ uptake to maintain K+ homeostasis under low K+ or salt stress[J]. Plant Cell Reports, 2018, 37(11):1533-1546.
[43] Qin YJ, Wu WH, Wang Y.ZmHAK5 and ZmHAK1 function in K+ uptake and distribution in maize under low K+ conditions[J]. Journal of Integrative Plant Biology, 2019, 61(6):691-705.
[44] Feng X, Wang Y, Zhang N, et al.Genome-wide systematic characterization of the HAK/KUP/KT gene family and its expression profile during plant growth and in response to low-K+ stress in Saccharum[J]. BMC Plant Biology, 2020, 20:20.
[45] 张松. 钾离子转运蛋白 OsHAK5 调控水稻株型机理的探究[D]. 南京:南京农业大学, 2015.
Zhang S.How does a potassium transporter OsHAK5 affect rice plant architecture[D]. Nanjing:Nanjing Agricultural Univer-sity, 2015.
[46] Qin LJ, Zhao D, Zhang Y, et al.Selectable marker-free co-expression of Nicotiana rustica CN and Nicotiana tabacum HAK1 genes improves resistance to tobacco mosaic virus in tobacco[J]. Functional Plant Biology, 2015, 42(8):802-815.
[47] Qi Z, Hampton CR, Shin R, et al.The high affinity K+ transporter AtHAK5 plays a physiological role in planta at very low K+ concentrations and provides a caesium uptake pathway in Arabidopsis[J]. Journal of Experimental Botany, 2008, 59(3):595-607.
[48] Zhao S, Zhang ML, Ma TL, et al.Phosphorylation of ARF2 relieves its repression of transcription of the K+ transporter gene HAK5 in response to low potassium stress[J]. The Plant Cell, 2016, 28(12):3005-3019.
[49] Zhu JK.Salt and drought stress signal transduction in plants[J]. Annual Review of Plant Biology, 2002, 53(1):247-273.
[50] Chen G, Liu C, Gao Z, et al.OsHAK1, a high-affinity potassium transporter, positively regulates responses to drought stress in rice[J]. Frontiers in Plant Science, 2017, 8:1885.
[51] 张祎, 秦利军, 赵丹, 赵德刚. 超量表达NtHAK1 基因提高烟草干旱胁迫能力[J]. 植物生理学报, 2017, 53(8):1444-1452.
Zhang Y, Qin LJ, Zhso D, Zhao DG.Improvement of drought-stress in NtHAK1-overexpressing Nicotiana tabacum[J]. Plant Physiology Communications, 2017, 53(8):1444-1452.
[52] Jiang Y, Qiu Y, Hu Y, et al.Heterologous expression of AtWRKY57 confers drought tolerance in Oryza sativa[J]. Frontiers in Plant Science, 2016, 7:145.
[53] Zhang Z, Zhang J, Chen Y, et al.Genome-wide analysis and identification of HAK potassium transporter gene family in maize(Zeamays L.)[J]. Molecular Biology Reports, 2012, 39(8):8465-8473.
[54] Assaha DV, Ueda A, Saneoka H, et al.The role of Na+ and K+ transporters in salt stress adaptation in glycophytes[J]. Frontiers in Physiology, 2017, 8:509.
[55] Horie T, Sugawara M, Okada T, et al.Rice sodium-insensitive potassium transporter, OsHAK5, confers increased salt tolerance in tobacco BY2 cells[J]. Journal of Bioscience and Bioengineering, 2011, 111(3):346-356.
[56] Alemán F, Caballero F, Ródenas R, et al.The F130S point mutation in the Arabidopsis high-affinity K transporter AtHAK5 increases K over Na and Cs selectivity and confers Na and Cs tolerance to yeast under heterologous expression[J]. Frontiers in Plant Science, 2014, 5:430.
[57] Maathuis FJ.The role of monovalent cation transporters in plant responses to salinity[J]. Journal of Experimental Botany, 2005, 57(5):1137-1147.
[58] Yang H, Zhang W, Chai W, et al.PtHAK5, a candidate for mediating high-affinity K+ uptake in the halophytic grass, Puccinellia tenuiflora[J]. Frontiers of Agricultural Science and Engineering, 2018, 5(1):108-117.
[59] 车文利, 张书玲, 吴立柱, 等. 转 AlHAK1 基因棉花耐盐能力分析[J]. 中国农业科技导报, 2015, 17(1):49-56.
Che WL, Zhang SL, Wu LZ, et al.Analysis of salt-tolerant ability in transgenic cotton(Gossypium hirsutum L.)with AlHAK1[J]. Journal of Agricultural Science and Technology, 2015, 17(1):49-56.
[60] Walters DR, Bingham IJ.Influence of nutrition on disease development caused by fungal pathogens:implications for plant disease control[J]. Annals of Applied Biology, 2007, 151(3):307-324.
[61] Römheld V, Kirkby EA.Research on potassium in agriculture:needs and prospects[J]. Plant and Soil, 2010, 335(1-2):155-180.
[62] Fuchs WH, Grossmann F.Nutrition and resistance of crop plants against pathogens and pests[J]. Handbuch Der Pflanzenernahrung Und Dungung, 1972, 1(Part 2):1008-1107.
[63] Jeworutzki E, Roelfsema MR, Anschütz U, et al.Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca²+-associated opening of plasma membrane anion channels[J]. The Plant Journal, 2010, 62(3):367-378.
[64] Atkinson MM, Baker CJ.Alteration of plasmalemma sucrose transport in Phaseolus vulgaris by Pseudomonas syringae pv. syringae and its association with K+ /H+ exchange[J]. Phytopathology, 1987, 77(11):1573-1578.
[65] Magnan F, Ranty B, Charpenteau M, et al.Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid[J]. The Plant Journal, 2008, 56(4):575-589.
[66] Leba LJ, Cheval C, Ortiz-Martín I, et al.CML9, an Arabidopsis calmodulin-like protein, contributes to plant innate immunity through a flagellin-dependent signalling pathway[J]. The Plant Journal, 2012, 71(6):976-989.
[67] Leba LJ, Perochon A, Cheval C, et al.CML9, a multifunctional Arabidopsis thaliana calmodulin-like protein involved in stress responses and plant growth?[J]. Plant Signaling & Behavior, 2012, 7(9):1121-1124.
[68] Brauer EK, Ahsan N, Dale R, et al.The Raf-like kinase ILK1 and the high affinity K+ transporter HAK5 are required for innate immunity and abiotic stress response[J]. Plant Physiology, 2016, 171(2):1470-1484.