Full Text:   <1159>

Summary:  <1081>

CLC number: Q945.78

On-line Access: 2020-06-01

Received: 2019-08-27

Revision Accepted: 2019-12-27

Crosschecked: 2020-05-29

Cited: 0

Clicked: 1930

Citations:  Bibtex RefMan EndNote GB/T7714


Guo-ping Zhang


-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2020 Vol.21 No.6 P.426-441


Advances in studies on ion transporters involved in salt tolerance and breeding crop cultivars with high salt tolerance

Author(s):  Lu Huang, De-zhi Wu, Guo-ping Zhang

Affiliation(s):  Key Laboratory of Crop Germplasm Resource of Zhejiang Province, Department of Agronomy, Zhejiang University, Hangzhou 310058, China

Corresponding email(s):   zhanggp@zju.edu.cn

Key Words:  Salinity, Osmotic stress, Ionic stress, Oxidative stress, Salt tolerance

Lu Huang, De-zhi Wu, Guo-ping Zhang. Advances in studies on ion transporters involved in salt tolerance and breeding crop cultivars with high salt tolerance[J]. Journal of Zhejiang University Science B, 2020, 21(6): 426-441.

@article{title="Advances in studies on ion transporters involved in salt tolerance and breeding crop cultivars with high salt tolerance",
author="Lu Huang, De-zhi Wu, Guo-ping Zhang",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T Advances in studies on ion transporters involved in salt tolerance and breeding crop cultivars with high salt tolerance
%A Lu Huang
%A De-zhi Wu
%A Guo-ping Zhang
%J Journal of Zhejiang University SCIENCE B
%V 21
%N 6
%P 426-441
%@ 1673-1581
%D 2020
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1900510

T1 - Advances in studies on ion transporters involved in salt tolerance and breeding crop cultivars with high salt tolerance
A1 - Lu Huang
A1 - De-zhi Wu
A1 - Guo-ping Zhang
J0 - Journal of Zhejiang University Science B
VL - 21
IS - 6
SP - 426
EP - 441
%@ 1673-1581
Y1 - 2020
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1900510

Soil salinity is a global major abiotic stress threatening crop productivity. In salty conditions, plants may suffer from osmotic, ionic, and oxidative stresses, resulting in inhibition of growth and development. To deal with these stresses, plants have developed a series of tolerance mechanisms, including osmotic adjustment through accumulating compatible solutes in the cytoplasm, reactive oxygen species (ROS) scavenging through enhancing the activity of anti-oxidative enzymes, and Na+/K+ homeostasis regulation through controlling Na+ uptake and transportation. In this review, recent advances in studies of the mechanisms of salt tolerance in plants are described in relation to the ionome, transcriptome, proteome, and metabolome, and the main factor accounting for differences in salt tolerance among plant species or genotypes within a species is presented. We also discuss the application and roles of different breeding methodologies in developing salt-tolerant crop cultivars. In particular, we describe the advantages and perspectives of genome or gene editing in improving the salt tolerance of crops.



Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1]Ali Z, Park HC, Ali A, et al., 2012. TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows K+ specificity in the presence of NaCl. Plant Physiol, 158(3):1463-1474.

[2]Andrés Z, Perez-Hormaeche J, Leidi EO, et al., 2014. Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake. Proc Natl Acad Sci USA, 111(17):E1806-E1814.

[3]Barragán V, Leidi EO, Andrés Z, et al., 2012. Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell, 24(3):1127-1142.

[4]Bassil E, Ohto MA, Esumi T, et al., 2011a. The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell, 23(1):224-239.

[5]Bassil E, Tajima H, Liang YC, et al., 2011b. The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell, 23(9):3482-3497.

[6]Bassil E, Coku A, Blumwald E, 2012. Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot, 63(16):5727-5740.

[7]Butcher K, Wick AF, Desutter T, et al., 2016. Soil salinity: a threat to global food security. Agron J, 108(6):2189-2200.

[8]Byrt CS, Platten JD, Spielmeyer W, et al., 2007. HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol, 143(4):1918-1928.

[9]Byrt CS, Xu B, Krishnan M, et al., 2014. The Na+ transporter, TaHKT1;5-D, limits shoot Na+ accumulation in bread wheat. Plant J, 80(3):516-526.

[10]Chen KL, Gao CX, 2014. Targeted genome modification technologies and their applications in crop improvements. Plant Cell Rep, 33(4):575-583.

[11]Chen YS, Lo SF, Sun PK, et al., 2015. A late embryogenesis abundant protein HVA1 regulated by an inducible promoter enhances root growth and abiotic stress tolerance in rice without yield penalty. Plant Biotechnol J, 13(1):105-116.

[12]Chen Z, Newman I, Zhou M, et al., 2005. Screening plants for salt tolerance by measuring K+ flux: a case study for barley. Plant Cell Environ, 28(10):1230-1246.

[13]Chen ZH, Pottosin II, Cuin TA, et al., 2007. Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol, 145(4):1714-1725.

[14]Christian M, Cermak T, Doyle EL, et al., 2010. Targeting DNA double-strand breaks with TAL effector nucleases. Genetics, 186(2):757-761.

[15]Dai F, Wang XL, Zhang XQ, et al., 2018. Assembly and analysis of a qingke reference genome demonstrate its close genetic relation to modern cultivated barley. Plant Biotechnol J, 16(3):760-770.

[16]Davenport RJ, Muñoz-Mayor A, Jha D, et al., 2007. The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant Cell Environ, 30(4):497-507.

[17]Diatloff E, Kumar R, Schachtman DP, 1998. Site directed mutagenesis reduces the Na+ affinity of HKT1, an Na+ energized high affinity K+ transporter. FEBS Lett, 432(1-2):31-36.

[18]Du LQ, Li YX, Li HJ, et al., 1999. Screening of salt tolerant watercress variants on natural seawater contained medium. Acta Bot Sin, 41(6):633-639.

[19]el Mahi H, Pérez-Hormaeche J, de Luca A, et al., 2019. A critical role of sodium flux via the plasma membrane Na+/H+ exchanger SOS1 in the salt tolerance of rice. Plant Physiol, 180(2):1046-1065.

[20]Flowers TJ, Colmer TD, 2008. Salinity tolerance in halophytes. New Phytol, 179(4):945-963.

[21]Forster BP, 2001. Mutation genetics of salt tolerance in barley: an assessment of golden promise and other semi-dwarf mutants. Euphytica, 120(3):317-328.

[22]Fricke W, Peters WS, 2002. The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Plant Physiol, 129(1):374-388.

[23]Fu LB, Shen QF, Kuang LH, et al., 2018. Metabolite profiling and gene expression of Na/K transporter analyses reveal mechanisms of the difference in salt tolerance between barley and rice. Plant Physiol Biochem, 130:248-257.

[24]Fu LB, Shen QF, Kuang LH, et al., 2019. Transcriptomic and alternative splicing analyses reveal mechanisms of the difference in salt tolerance between barley and rice. Environ Exp Bot, 166:103810.

[25]Fukuda A, Nakamura A, Hara N, et al., 2011. Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta, 233(1):175-188.

[26]Gao CX, 2015. Genome editing in crops: from bench to field. Natl Sci Rev, 2(1):13-15.

[27]Gao F, Gao Q, Duan XG, et al., 2006. Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. J Exp Bot, 57(12):3259-3270.

[28]Garciadeblás B, Senn ME, Bañuelos MA, et al., 2003. Sodium transport and HKT transporters: the rice model. Plant J, 34(6):788-801.

[29]Gassmann W, Rubio F, Schroeder JI, 1996. Alkali cation selectivity of the wheat root high-affinity potassium transporter HKT1. Plant J, 10(5):869-882.

[30]Gorham J, Jones RGW, Bristol A, 1990. Partial characterization of the trait for enhanced K+-Na+ discrimination in the D genome of wheat. Planta, 180(4):590-597.

[31]Guo FQ, Li Q, Gu RQ, 1997. Mutation, selection and comparison of several saline-tolerant wheat strains. Acta Agric Nucl Sin, 11(1):1-8 (in Chinese).

[32]Guo R, Shi LX, Yan CR, et al., 2017. Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biol, 17:41.

[33]Hamam AM, Britto DT, Flam-Shepherd R, et al., 2016. Measurement of differential Na+ efflux from apical and bulk root zones of intact barley and Arabidopsis plants. Front Plant Sci, 7:272.

[34]Han Y, Yin SY, Huang L, 2015. Towards plant salinity tolerance-implications from ion transporters and biochemical regulation. Plant Growth Regul, 76(1):13-23.

[35]Han Y, Yin SY, Huang L, et al., 2018. A sodium transporter HvHKT1;1 confers salt tolerance in barley via regulating tissue and cell ion homeostasis. Plant Cell Physiol, 59(10):1976-1989.

[36]Hare PD, Cress WA, van Staden J, 1998. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ, 21(6):535-553.

[37]Horie T, Costa A, Kim TH, et al., 2007. Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J, 26(12):3003-3014.

[38]Horie T, Hauser F, Schroeder JI, 2009. HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci, 14(12):660-668.

[39]Horie T, Brodsky DE, Costa A, et al., 2011. 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. Plant Physiol, 156(3):1493-1507.

[40]Horie T, Karahara I, Katsuhara M, 2012. Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants. Rice, 5:11.

[41]Huang L, Kuang LH, Li X, et al., 2018. Metabolomic and transcriptomic analyses reveal the reasons why Hordeum marinum has higher salt tolerance than Hordeum vulgare. Environ Exp Bot, 156:48-61.

[42]Huang L, Kuang LH, Wu LY, et al., 2020. The HKT transporter HvHKT1;5 negatively regulates salt tolerance. Plant Physiol, 182(1):584-596.

[43]Huang SB, Spielmeyer W, Lagudah ES, et al., 2008. Comparative mapping of HKT genes in wheat, barley, and rice, key determinants of Na+ transport, and salt tolerance. J Exp Bot, 59(4):927-937.

[44]Huertas R, Olías R, Eljakaoui Z, et al., 2012. Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant Cell Environ, 35(8):1467-1482.

[45]Isayenkov SV, 2012. Physiological and molecular aspects of salt stress in plants. Cytol Genet, 46(5):302-318.

[46]Isayenkov SV, 2019. Genetic sources for the development of salt tolerance in crops. Plant Growth Regul, 89(1):1-17.

[47]Isayenkov SV, Maathuis FJM, 2019. Plant salinity stress: many unanswered questions remain. Front Plant Sci, 10:80.

[48]Ismail AM, Horie T, 2017. Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol, 68:405-434.

[49]Jabnoune M, Espeout S, Mieulet D, et al., 2009. Diversity in expression patterns and functional properties in the rice HKT transporter family. Plant Physiol, 150(4):1955-1971.

[50]James RA, Davenport RJ, Munns R, 2006. Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2. Plant Physiol, 142(4):1537-1547.

[51]James RA, Blake C, Byrt CS, et al., 2011. Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. J Exp Bot, 62(8):2939-2947.

[52]Jinek M, Chylinski K, Fonfara I, et al., 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337(6096):816-821.

[53]Kader MA, Lindberg S, 2008. Cellular traits for sodium tolerance in rice (Oryza sativa L.). Plant Biotechnol, 25(3):247-255.

[54]Kader MA, Seidel T, Golldack D, et al., 2006. Expressions of OsHKT1, OsHKT2, and OsVHA are differentially regulated under NaCl stress in salt-sensitive and salt-tolerant rice (Oryza sativa L.) cultivars. J Exp Bot, 57(15):4257-4268.

[55]Khan MS, Ahmad D, Khan MA, 2015. Trends in genetic engineering of plants with (Na+/H+) antiporters for salt stress tolerance. Biotechnol Biotechnol Equip, 29(5):815-825.

[56]Khatodia S, Bhatotia K, Passricha N, et al., 2016. The CRISPR/ Cas genome-editing tool: application in improvement of crops. Front Plant Sci, 7:506.

[57]Kim YG, Cha J, Chandrasegaran S, 1996. Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA, 93(3):1156-1160.

[58]Kobayashi NI, Yamaji N, Yamamoto H, et al., 2017. OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. Plant J, 91(4):657-670.

[59]Kronzucker HJ, Szczerba MW, Schulze LM, et al., 2008. Non-reciprocal interactions between K+ and Na+ ions in barley (Hordeum vulgare L.). J Exp Bot, 59(10):2793-2801.

[60]Leidi EO, Barragán V, Rubio L, et al., 2010. The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J, 61(3):495-506.

[61]Li B, Wei AY, Song CX, et al., 2008. Heterologous expression of the TsVP gene improves the drought resistance of maize. Plant Biotechnol J, 6(2):146-159.

[62]Li CL, Hou QM, Zeng LH, et al., 1990. Preliminary study on induction of salt-tolerant cell lines in wheat by radiation mutagenesis combined with tissue culture. J Nucl Agric Sci, 1990(01):8-12 (in Chinese).

[63]Li JF, Norville JE, Aach J, et al., 2013. Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol, 31(8):688-691.

[64]Li T, Liu B, Spalding MH, et al., 2012. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol, 30(5):390-392.

[65]Ligaba A, Katsuhara M, 2010. Insights into the salt tolerance mechanism in barley (Hordeum vulgare) from comparisons of cultivars that differ in salt sensitivity. J Plant Res, 123(1):105-118.

[66]Lindsay MP, Lagudah ES, Hare RA, et al., 2004. A locus for sodium exclusion (Nax1), a trait for salt tolerance, mapped in durum wheat. Funct Plant Biol, 31(11):1105-1114.

[67]Linh LH, Linh TH, Xuan TD, et al., 2012. Molecular breeding to improve salt tolerance of rice (Oryza sativa L.) in the Red River Delta of Vietnam. Int J Plant Genomics, 2012(66):949038.

[68]Lv SL, Zhang KW, Gao Q, et al., 2008. Overexpression of an H+-PPase gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol, 49(8):1150-1164.

[69]Lv SL, Lian LJ, Tao PL, et al., 2009. Overexpression of Thellungiella halophila H+-PPase (TsVP) in cotton enhances drought stress resistance of plants. Planta, 229(4):899-910.

[70]Martínez-Atienza J, Jiang XY, Garciadeblas B, et al., 2007. Conservation of the salt overly sensitive pathway in rice. Plant Physiol, 143(2):1001-1012.

[71]Mäser P, Eckelman B, Vaidyanathan R, et al., 2002a. Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett, 531(2):157-161.

[72]Mäser P, Hosoo Y, Goshima S, et al., 2002b. Glycine residues in potassium channel-like selectivity filters determine potassium selectivity in four-loop-per-subunit HKT transporters from plants. Proc Natl Acad Sci USA, 99(9):6428-6433.

[73]Meena KK, Sorty AM, Bitla UM, et al., 2017. Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci, 8:172.

[74]Mian A, Oomen RJFJ, Isayenkov S, et al., 2011. Over-expression of an Na+- and K+-permeable HKT transporter in barley improves salt tolerance. Plant J, 68(3):468-479.

[75]Miller G, Suzuki N, Ciftci-Yilmaz S, et al., 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ, 33(4):453-467.

[76]Møller IS, Gilliham M, Jha D, et al., 2009. Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell, 21(7):2163-2178.

[77]Moya JL, Gómez-Cadenas A, Primo-Millo E, et al., 2003. Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use. J Exp Bot, 54(383):825-833.

[78]Munns R, 2002. Comparative physiology of salt and water stress. Plant Cell Environ, 25(2):239-250.

[79]Munns R, 2005. Genes and salt tolerance: bringing them together. New Phytol, 167(3):645-663.

[80]Munns R, Rawson HM, 1999. Effect of salinity on salt accumulation and reproductive development in the apical meristem of wheat and barley. Aust J Plant Physiol, 26(5):459-464.

[81]Munns R, Tester M, 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol, 59:651-681.

[82]Munns R, Gilliham M, 2015. Salinity tolerance of crops— what is the cost? New Phytol, 208(3):668-673.

[83]Munns R, James RA, Xu B, et al., 2012. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol, 30(4):360-364.

[84]Nabors MW, Gibbs SE, Bernstein CS, 1980. NaCl-tolerant tobacco plants from cultured cells. Z Pflanzenphysiol, 97(1):13-17.

[85]Nawrot R, Barylski J, Lippmann R, et al., 2016. Combination of transcriptomic and proteomic approaches helps to unravel the protein composition of Chelidonium majus L. milky sap. Planta, 244(5):1055-1064.

[86]Nekrasov V, Wang CM, Win J, et al., 2017. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep, 7:482.

[87]Nevo E, Chen GX, 2010. Drought and salt tolerances in wild relatives for wheat and barley improvement. Plant Cell Environ, 33(4):670-685.

[88]Oomen RJFJ, Benito B, Sentenac H, et al., 2012. HKT2;2/1, a K+-permeable transporter identified in a salt-tolerant rice cultivar through surveys of natural genetic polymorphism. Plant J, 71(5):750-762.

[89]Passioura JB, Munns R, 2000. Rapid environmental changes that affect leaf water status induce transient surges or pauses in leaf expansion rate. Aust J Plant Physiol, 27(10):941-948.

[90]Platten JD, Cotsaftis O, Berthomieu P, et al., 2006. Nomenclature for HKT transporters, key determinants of plant salinity tolerance. Trends Plant Sci, 11(8):372-374.

[91]Qiu L, Wu DZ, Ali S, et al., 2011. Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley. Theor Appl Genet, 122(4):695-703.

[92]Qiu QS, Guo Y, Dietrich MA, et al., 2002. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA, 99(12):8436-8441.

[93]Quintero FJ, Ohta M, Shi HZ, et al., 2002. Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA, 99(13):9061-9066.

[94]Rajendran K, Tester M, Roy SJ, 2009. Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ, 32(3):237-249.

[95]Ren ZH, Gao JP, Li LG, et al., 2005. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet, 37(10):1141-1146.

[96]Reynolds MP, Mujeeb-Kazi A, Sawkins M, 2005. Prospects for utilising plant-adaptive mechanisms to improve wheat and other crops in drought- and salinity-prone environments. Ann Appl Biol, 146(2):239-259.

[97]Reynolds M, Dreccer F, Trethowan R, 2007. Drought-adaptive traits derived from wheat wild relatives and landraces. J Exp Bot, 58(2):177-186.

[98]Rodríguez-Navarro A, 2000. Potassium transport in fungi and plants. Biochim Biophys Acta, 1469(1):1-30.

[99]Rodríguez-Navarro A, Rubio F, 2006. High-affinity potassium and sodium transport systems in plants. J Exp Bot, 57(5):1149-1160.

[100]Rodríguez-Rosales MP, Jiang XY, Gálvez FJ, et al., 2008. Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol, 179(2):366-377.

[101]Roorkiwal M, Nayak SN, Thudi M, et al., 2014. Allele diversity for abiotic stress responsive candidate genes in chickpea reference set using gene based SNP markers. Front Plant Sci, 5:248.

[102]Roy SJ, Negrão S, Tester M, 2014. Salt resistant crop plants. Curr Opin Biotechnol, 26:115-124.

[103]Rubio F, Gassmann W, Schroeder JI, 1995. Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science, 270(5242):1660-1663.

[104]Rubio F, Schwarz M, Gassmann W, et al., 1999. Genetic selection of mutations in the high affinity K+ transporter HKT1 that define functions of a loop site for reduced Na+ permeability and increased Na+ tolerance. J Biol Chem, 274(11):6839-6847.

[105]Sassi A, Mieulet D, Khan I, et al., 2012. The rice monovalent cation transporter OsHKT2;4: revisited ionic selectivity. Plant Physiol, 160(1):498-510.

[106]Schachtman DP, Schroeder JI, 1994. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature, 370(6491):655-658.

[107]Schachtman DP, Schroeder JI, Lucas WJ, et al., 1992. Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA. Science, 258(5088):1654-1658.

[108]Shabala S, 2013. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot, 112(7):1209-1221.

[109]Shabala S, Shabala S, Cuin TA, et al., 2010. Xylem ionic relations and salinity tolerance in barley. Plant J, 61(5):839-853.

[110]Shabala S, Bose J, Hedrich R, 2014. Salt bladders: do they matter? Trends Plant Sci, 19(11):687-691.

[111]Shen QF, Fu LB, Dai F, et al., 2016. Multi-omics analysis reveals molecular mechanisms of shoot adaption to salt stress in Tibetan wild barley. BMC Genomics, 17:889.

[112]Shen QF, Fu LB, Qiu L, et al., 2017. Time-course of ionic responses and proteomic analysis of a Tibetan wild barley at early stage under salt stress. Plant Growth Regul, 81(1):11-21.

[113]Shen QF, Yu JH, Fu LB, et al., 2018. Ionomic, metabolomic and proteomic analyses reveal molecular mechanisms of root adaption to salt stress in Tibetan wild barley. Plant Physiol Biochem, 123:319-330.

[114]Shi HZ, Ishitani M, Kim C, et al., 2000. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA, 97(12):6896-6901.

[115]Shi HZ, Quintero FJ, Pardo JM, et al., 2002. The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell, 14(2):465-477.

[116]Singh RK, Redoña E, Refuerzo L, 2009. Varietal improvement for abiotic stress tolerance in crop plants: special reference to salinity in rice. In: Pareek A, Sopory SK, Bohnert BH, et al. (Eds.), Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation. Springer, Dordrecht, p.387-415.

[117]Suzuki K, Yamaji N, Costa A, et al., 2016. OsHKT1;4-mediated Na+ transport in stems contributes to Na+ exclusion from leaf blades of rice at the reproductive growth stage upon salt stress. BMC Plant Biol, 16:22.

[118]Tester M, Davenport R, 2003. Na+ tolerance and Na+ transport in higher plants. Ann Bot, 91(5):503-527.

[119]Thomson MJ, de Ocampo M, Egdane J, et al., 2010. Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice, 3(2):148-160.

[120]Wang FB, Liu JC, Zhou LJ, et al., 2016. Senescence-specific change in ROS scavenging enzyme activities and regulation of various SOD isozymes to ROS levels in psf mutant rice leaves. Plant Physiol Biochem, 109:248-261.

[121]Wang H, Zhang MS, Guo R, et al., 2012. Effects of salt stress on ion balance and nitrogen metabolism of old and young leaves in rice (Oryza sativa L.). BMC Plant Biol, 12:194.

[122]Wang Y, Jia JF, 1999. Selection and characteristics analysis of NaCl-tolerant cell line from Astragalus adsurgens callus cultures. Chin J Appl Environ Biol, 5(6):547-550 (in Chinese).

[123]Wang YP, Cheng X, Shan QW, et al., 2014. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol, 32(9):947-951.

[124]Waters S, Gilliham M, Hrmova M, 2013. Plant high-affinity potassium (HKT) transporters involved in salinity tolerance: structural insights to probe differences in ion selectivity. Int J Mol Sci, 14(4):7660-7680.

[125]Wu DZ, Shen QF, Cai SG, et al., 2013a. Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol, 54(12):1976-1988.

[126]Wu DZ, Cai SG, Chen MX, et al., 2013b. Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS ONE, 8(1):e55431.

[127]Wu DZ, Shen QF, Qiu L, et al., 2014. Identification of proteins associated with ion homeostasis and salt tolerance in barley. Proteomics, 14(11):1381-1392.

[128]Xu D, Duan X, Xue QZ, et al., 2008b. Transformation of rice with agronomically useful genes toward production of insect-resistant and water stress-tolerant plants. Proceedings of the 3rd International Rice Genetics Symposium, Manila, Philippines, p.796-803.

[129]Xu HX, Jiang XY, Zhan KH, et al., 2008a. Functional characterization of a wheat plasma membrane Na+/H+ antiporter in yeast. Arch Biochem Biophys, 473(1):8-15.

[130]Yang Q, Chen ZZ, Zhou XF, et al., 2009. Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant, 2(1):22-31.

[131]Yao X, Horie T, Xue SW, et al., 2010. Differential sodium and potassium transport selectivities of the rice OsHKT2;1 and OsHKT2;2 transporters in plant cells. Plant Physiol, 152(1):341-355.

[132]Ye JM, Kao KN, Harvey BL, et al., 1987. Screening salt-tolerant barley genotypes via F1 anther culture in salt stress media. Theor Apple Genet, 74(4):426-429.

[133]Yu LJ, Nie JN, Cao CY, et al., 2010. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol, 188(3):762-773.

[134]Zahra J, Nazim H, Cai SG, et al., 2014. The influence of salinity on cell ultrastructures and photosynthetic apparatus of barley genotypes differing in salt stress tolerance. Acta Physiol Plant, 36(5):1261-1269.

[135]Zhang C, Li HJ, Wang JY, et al., 2017. The rice high-affinity K+ transporter OsHKT2;4 mediates Mg2+ homeostasis under high-Mg2+ conditions in transgenic Arabidopsis. Front Plant Sci, 8:1823.

[136]Zhang Y, Massel K, Godwin ID, et al., 2018. Applications and potential of genome editing in crop improvement. Genome Biol, 19:210.

[137]Zhang YM, Zhang HM, Liu ZH, et al., 2015. The wheat NHX antiporter gene TaNHX2 confers salt tolerance in transgenic alfalfa by increasing the retention capacity of intracellular potassium. Plant Mol Biol, 87(3):317-327.

[138]Zhao RT, Gao SG, Qiao YK, et al., 1995. Studies on the application of anther culture in salt-tolerance breeding in wheat (Triticum aestivum L.). Acta Agron Sin, 21(2):230-234 (in Chinese).

[139]Zhou JP, Deng KJ, Cheng Y, et al., 2017. CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci, 8:1598.

[140]Zhu JK, 2001. Plant salt tolerance. Trends Plant Sci, 6(2):66-71.

[141]Zhu JK, 2003. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol, 6(5):441-445.

Open peer comments: Debate/Discuss/Question/Opinion


Please provide your name, email address and a comment

Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2022 Journal of Zhejiang University-SCIENCE