Improving crop salt tolerance using transgenic approaches: an update and physiological analysis
Abstract
Abstract Salinization of land is likely to increase due to climate change with impact on agricultural production. Since most species used as crops are sensitive to salinity, improvement of salt tolerance is needed to maintain global food production. This review summarises successes and failures of transgenic approaches in improving salt tolerance in crop species. A conceptual model of coordinated physiological mechanisms in roots and shoots required for salt tolerance is presented. Transgenic plants overexpressing genes of key proteins contributing to Na + ‘exclusion’ (PM‐ATPases with SOS1 antiporter, and HKT1 transporter) and Na + compartmentation in vacuoles (V‐H + ATPase and V‐H + PPase with NHX antiporter), as well as two proteins potentially involved in alleviating water deficit during salt stress (aquaporins and dehydrins), were evaluated. Of the 51 transformations, with gene(s) involved in Na + ‘exclusion’ or Na + vacuolar compartmentation that contained quantitative data on growth and include a non‐saline control, 48 showed improvements in salt tolerance (less impact on plant mass) of transgenic plants, but with only two tested in field conditions. Of these 51 transformations, 26 involved crop species. Tissue ion concentrations were altered, but not always in the same way. Although glasshouse data are promising, field studies are required to assess crop salinity tolerance.
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Pyramiding multiple genes involved in salt stress responses is important to improve crop salt tolerance.
“Additionally, a study reviewed various transgenic approaches to improve crop salt tolerance, emphasizing the importance of pyramiding multiple genes involved in salt stress responses (Hsu et al., 2020; Kotula et al., 2020; Liu et al., 2021).”
From Emerging applications of gene editing technologies for the development of climate-resilient crops (2025) · cites this paper as Kotula et al., 2020
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Mechanisms of Salinity Tolerance
Munns, R., & Tester, M. (2008) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.59.032607.092911 · Cited by 13,792 · see citing works
Mechanisms of Salt Tolerance in Nonhalophytes
Greenway, H., & Munns, R. (1980) · Annual Review of Plant Physiology · doi:10.1146/annurev.pp.31.060180.001053 · Cited by 4,000 · see citing works
Watson, R., Albritton, D. L., Barker, T., Baskmakov, I., Canziani, O. F., Christ, R., Ulrich Cubasch, B., Davidson, O., Gitay, H., Griggs, D., et al. (2001) · Cited by 3,473 · see citing works
Genes and salt tolerance: bringing them together
Munns, R. (2005) · New Phytologist · doi:10.1111/j.1469-8137.2005.01487.x · Cited by 3,049 · see citing works
Flowers, T. J. (2004) · Journal of Experimental Botany · doi:10.1093/jxb/erh003 · Cited by 2,132 · see citing works
Self-citationSalt Tolerance Conferred by Overexpression of a Vacuolar Na + /H + Antiport in Arabidopsis
Apse, M. P., Aharon, G. S., Snedden, W. A., & Blumwald, E. (1999) · Science · doi:10.1126/science.285.5431.1256 · Cited by 1,964 · see citing works
The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na + /H + antiporter
Shi, H., Ishitani, M., Kim, C.-S., & Zhu, J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.120170197 · Cited by 1,672 · see citing works
A rice quantitative trait locus for salt tolerance encodes a sodium transporter
Ren, Z., Gao, J., Li, L., Cai, X., Huang, W., Chao, D., Zhu, M., Wang, Z., Luan, S., & Lin, H. (2005) · Nature Genetics · doi:10.1038/ng1643 · Cited by 1,503 · see citing works
Shi, H., Quintero, F. J., Pardo, J. M., & Zhu, J. (2002) · The Plant Cell · doi:10.1105/tpc.010371 · Cited by 1,295 · see citing works
Sodium transport in plant cells
Blumwald, E., Aharon, G. S., & Apse, M. P. (2000) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(00)00135-8 · Cited by 994 · see citing works
Breeding for Salinity Resistance in Crop Plants: Where Next?
Flowers, T. J., & Yeo, A. (1995) · Australian Journal of Plant Physiology · doi:10.1071/pp9950875 · Cited by 994 · see citing works
Self-citationROS homeostasis in halophytes in the context of salinity stress tolerance
Bose, J., Rodrigo-Moreno, A., & Shabala, S. N. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert430 · Cited by 967 · see citing works
Shi, H., Lee, B., Wu, S.-J., & Zhu, J. (2002) · Nature Biotechnology · doi:10.1038/nbt766 · Cited by 949 · see citing works
Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene
Munns, R., James, R. A., Xu, B., Athman, A., Conn, S. J., Jordans, C., Byrt, C. S., Hare, R. A., Tyerman, S. D., Tester, M. A., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2120 · Cited by 854 · see citing works
Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes
Flowers, T. J., Munns, R., & Colmer, T. D. (2014) · Annals of Botany · doi:10.1093/aob/mcu217 · Cited by 752 · see citing works
Self-citationGhoulam, C., Foursy, A., & Farès, K. (2002) · Environmental and Experimental Botany · doi:10.1016/s0098-8472(01)00109-5 · Cited by 748 · see citing works
Sunarpi, Horie, T., Motoda, J., Kubo, M., Yang, H., Yoda, K., Horie, R., Chan, W., Leung, H., Hattori, K., et al. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02595.x · Cited by 645 · see citing works
Barragán‐Borrero, V., Leidi, E. O., Andrés, Z., Rubio, L., Luca, A. D., Fernández, J. A., Cubero, B., & Pardo, J. M. (2012) · The Plant Cell · doi:10.1105/tpc.111.095273 · Cited by 631 · see citing works
The Chemistry and Fertility of Sea Waters
(1955) · AIBS Bulletin · doi:10.1093/aibsbulletin/5.5.12-c · Cited by 571 · see citing works
Møller, I. S., Gilliham, M., Jha, D., Mayo, G. M., Roy, S. J., Coates, J. C., Haseloff, J. P., & Tester, M. A. (2009) · The Plant Cell · doi:10.1105/tpc.108.064568 · Cited by 563 · see citing works
Gaxiola, R. A., Palmgren, M. B., & Schumacher, K. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.03.050 · Cited by 559 · see citing works
Use of wild relatives to improve salt tolerance in wheat
Colmer, T. D., Flowers, T. J., & Munns, R. (2006) · Journal of Experimental Botany · doi:10.1093/jxb/erj124 · Cited by 534 · see citing works
Self-citationPlasma Membrane H + -ATPase Regulation in the Center of Plant Physiology
Falhof, J., Pedersen, J. T., Fuglsang, A. T., & Palmgren, M. B. (2015) · Molecular Plant · doi:10.1016/j.molp.2015.11.002 · Cited by 533 · see citing works
Hauser, F., & Horie, T. (2009) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2009.02056.x · Cited by 529 · see citing works
Energy costs of salt tolerance in crop plants
Munns, R., Day, D. A., Fricke, W., Watt, M., Arsova, B., Barkla, B. J., Bose, J., Byrt, C. S., Chen, Z., Foster, K. J., et al. (2019) · New Phytologist · doi:10.1111/nph.15864 · Cited by 523 · see citing works
HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants
Horie, T., Hauser, F., & Schroeder, J. I. (2009) · Trends in Plant Science · doi:10.1016/j.tplants.2009.08.009 · Cited by 519 · see citing works
Osmotic adjustment and energy limitations to plant growth in saline soil
Munns, R., Passioura, J. B., Colmer, T. D., & Byrt, C. S. (2019) · New Phytologist · doi:10.1111/nph.15862 · Cited by 483 · see citing works
Self-citationAlkali cation exchangers: roles in cellular homeostasis and stress tolerance
Pardo, J. M., Cubero, B., Leidi, E. O., & Quintero, F. J. (2006) · Journal of Experimental Botany · doi:10.1093/jxb/erj114 · Cited by 453 · see citing works
Yang, Q., Chen, Z., Zhou, X., Yin, H., Li, X., Xin, X., Hong, X., Zhu, J., & Gong, Z. (2008) · Molecular Plant · doi:10.1093/mp/ssn058 · Cited by 449 · see citing works
Maeshima, M. (2000) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(00)00130-9 · Cited by 439 · see citing works
Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs
Galau, G. A., Hughes, D. W., & Dure, L. S. (1986) · Plant Molecular Biology · doi:10.1007/bf00021327 · Cited by 436 · see citing works
Xue, Z., Zhi, D., Xue, G., Zhang, H., Zhao, Y., & Xia, G. (2004) · Plant Science · doi:10.1016/j.plantsci.2004.05.034 · Cited by 429 · see citing works
Arabidopsis H + -PPase AVP1 Regulates Auxin-Mediated Organ Development
Li, J., Yang, H., Peer, W. A., Richter, G. L., Blakeslee, J. J., Bandyopadhyay, A., Titapiwantakun, B., Undurraga, S. F., Khodakovskaya, M. V., Richards, E. L., et al. (2005) · Science · doi:10.1126/science.1115711 · Cited by 412 · see citing works
Salt tolerance mechanisms in quinoa (Chenopodium quinoa Willd.)
Adolf, V. I., Jacobsen, S., & Shabala, S. N. (2012) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2012.07.004 · Cited by 400 · see citing works
HKT1;5-Like Cation Transporters Linked to Na + Exclusion Loci in Wheat, Nax2 and Kna1
Byrt, C. S., Platten, J. D., Spielmeyer, W., James, R. A., Lagudah, E. S., Dennis, E. S., Tester, M. A., & Munns, R. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.093476 · Cited by 398 · see citing works
Sea-level rise caused by climate change and its implications for society
Mimura, N. (2013) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.89.281 · Cited by 391 · see citing works
Nomenclature for HKT transporters, key determinants of plant salinity tolerance
Platten, J. D., Cotsaftis, O., Berthomieu, P., Bohnert, H. J., Davenport, R. J., Fairbairn, D. J., Horie, T., Leigh, R. A., Lin, H.-X., Sheng, L., et al. (2006) · Trends in Plant Science · doi:10.1016/j.tplants.2006.06.001 · Cited by 371 · see citing works
Na+/H+ Antiport in Isolated Tonoplast Vesicles from Storage Tissue of Beta vulgaris
Blumwald, E., & Poole, R. J. (1985) · PLANT PHYSIOLOGY · doi:10.1104/pp.78.1.163 · Cited by 340 · see citing works
Disorder and function: a review of the dehydrin protein family
Graether, S. P., & Boddington, K. F. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00576 · Cited by 326 · see citing works
Yeo, A., & Flowers, T. J. (1986) · Australian Journal of Plant Physiology · doi:10.1071/pp9860161 · Cited by 318 · see citing works
Self-citationBassil, E., Coku, A., & Blumwald, E. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers250 · Cited by 311 · see citing works
The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato
Leidi, E. O., Barragán‐Borrero, V., Rubio, L., El‐Hamdaoui, A., Ruiz, M. T. G., Cubero, B., Fernández, J. A., Bressan, R. A., Hasegawa, P. M., Quintero, F. J., et al. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2009.04073.x · Cited by 303 · see citing works
The ins and outs of intracellular ion homeostasis: NHX-type cation/H + transporters
Bassil, E., & Blumwald, E. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.08.002 · Cited by 300 · see citing works
Pasapula, V., Shen, G., Kuppu, S., Paéz-Valencia, J., Mendoza, M., Hou, P., Chen, J., Qiu, X., Zhu, L., Zhang, X., et al. (2010) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2010.00535.x · Cited by 297 · see citing works
Wang, B., Lüttge, U. E., & Ratajczak, R. (2001) · Journal of Experimental Botany · doi:10.1093/jexbot/52.365.2355 · Cited by 291 · see citing works
Bao, A., Wang, S., Wu, G., Xi, J., Zhang, J., & Wang, C. (2008) · Plant Science · doi:10.1016/j.plantsci.2008.10.009 · Cited by 257 · see citing works
Brini, F., Hanin, M., Lumbreras, V., Amara, I., Khoudi, H., Hassairi, A., Pagès, M., & Masmoudi, K. (2007) · Plant Cell Reports · doi:10.1007/s00299-007-0412-x · Cited by 248 · see citing works
Engineering salinity tolerance in plants: progress and prospects
Wani, S. H., Kumar, V., Khare, T., Guddimalli, R., Parveda, M., Solymosi, K., Suprasanna, P., & Kavi Kishor, P. B. (2020) · Planta · doi:10.1007/s00425-020-03366-6 · Cited by 233 · see citing works
HKT transporters mediate salt stress resistance in plants: from structure and function to the field
Hamamoto, S., Horie, T., Hauser, F., Deinlein, U., Schroeder, J. I., & Uozumi, N. (2014) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2014.11.025 · Cited by 227 · see citing works
Hu, W., Yuan, Q., Wang, Y., et al. (2012) · Plant and Cell Physiology · doi:10.1093/pcp/pcs154 · Cited by 225 · see citing works
Shen, Y., Shen, L., Shen, Z., Jing, W., Ge, H., Zhao, J., & Zhang, W. (2015) · Plant Cell & Environment · doi:10.1111/pce.12586 · Cited by 221 · see citing works
Tissue tolerance: an essential but elusive trait for salt-tolerant crops
Munns, R., James, R. A., Gilliham, M., Flowers, T. J., & Colmer, T. D. (2016) · Functional Plant Biology · doi:10.1071/fp16187 · Cited by 218 · see citing works
Self-citationA banana aquaporin gene, MaPIP1;1, is involved in tolerance to drought and salt stresses
Xu, Y., Hu, W., Liu, J., Zhang, J., Jia, C., Miao, H., Xu, B., & Jin, Z. (2014) · BMC Plant Biology · doi:10.1186/1471-2229-14-59 · Cited by 212 · see citing works
Structure, function and regulation of the plant vacuolar H+-translocating ATPase
Ratajczak, R. (2000) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(00)00129-2 · Cited by 209 · see citing works
Yue, Y., Zhang, M., Zhang, J., Duan, L., & Li, Z. (2011) · Journal of Plant Physiology · doi:10.1016/j.jplph.2011.10.007 · Cited by 205 · see citing works
Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination
Liu, C., Fukumoto, T., Matsumoto, T., et al. (2012) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2012.11.018 · Cited by 197 · see citing works
Gévaudant, F., Duby, G., von Stedingk, E., Zhao, R., Morsomme, P., & Boutry, M. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.103762 · Cited by 196 · see citing works
Metabolic Engineering for Increased Salt Tolerance – the Next Step
Bohnert, H. J., & Jensen, R. (1996) · Australian Journal of Plant Physiology · doi:10.1071/pp9960661 · Cited by 193 · see citing works
Banerjee, A., & Roychoudhury, A. (2015) · Plant Growth Regulation · doi:10.1007/s10725-015-0113-3 · Cited by 190 · see citing works
Roychoudhury, A., Roy, C., & Sengupta, D. N. (2007) · Plant Cell Reports · doi:10.1007/s00299-007-0371-2 · Cited by 188 · see citing works
Non‐selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca 2+ and pH
Byrt, C. S., Zhao, M., Kourghi, M., et al. (2016) · Plant Cell & Environment · doi:10.1111/pce.12832 · Cited by 185 · see citing works
Katsuhara, M., Koshio, K., Shibasaka, M., et al. (2003) · Plant and Cell Physiology · doi:10.1093/pcp/pcg167 · Cited by 179 · see citing works
Lv, S., Zhang, K., Gao, Q., Lian, L., Song, Y., & Zhang, J. (2008) · Plant and Cell Physiology · doi:10.1093/pcp/pcn090 · Cited by 178 · see citing works
Li, Z., Baldwin, C. M., Hu, Q., LIU, H., & Luo, H. (2009) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2009.02080.x · Cited by 174 · see citing works
Rodríguez‐Rosales, M. P., Jiang, X., Gálvez, F. J., Aranda, M. N., Cubero, B., & Venema, K. (2008) · New Phytologist · doi:10.1111/j.1469-8137.2008.02461.x · Cited by 166 · see citing works
Shekhawat, U. K. S., Srinivas, L., & Ganapathi, T. R. (2011) · Planta · doi:10.1007/s00425-011-1455-3 · Cited by 162 · see citing works
Improved Salinity Tolerance of Rice Through Cell Type-Specific Expression of AtHKT1;1
Plett, D., Safwat, G., Gilliham, M., Møller, I. S., Roy, S. J., Shirley, N. J., Jacobs, A. K., Johnson, A. A. T., & Tester, M. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012571 · Cited by 162 · see citing works
Muñoz‐Mayor, A., Pineda, B., García‐Abellán, J. O., Antón, T., García‐Sogo, B., Sánchez‐Bel, P., Pardo, F., Atarés, A., Angosto, T., Pintor‐Toro, J. A., et al. (2012) · Journal of Plant Physiology · doi:10.1016/j.jplph.2011.11.018 · Cited by 159 · see citing works
Venema, K., Belver, A., Marín‐Manzano, M. C., Rodríguez‐Rosales, M. P., & Donaire, J. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210794200 · Cited by 157 · see citing works
Bublitz, M., Morth, J. P., & Nissen, P. (2011) · Journal of Cell Science · doi:10.1242/jcs.088716 · Cited by 153 · see citing works
Schilling, R. K., Marschner, P., Shavrukov, Y. N., Berger, B., Tester, M. A., Roy, S. J., & Plett, D. (2013) · Plant Biotechnology Journal · doi:10.1111/pbi.12145 · Cited by 149 · see citing works
Kumar, M., Lee, S., Kim, J., Kim, S., Aye, S. S., & Kim, S. (2014) · Journal of Plant Biology · doi:10.1007/s12374-014-0487-1 · Cited by 144 · see citing works
Structural and Functional Dynamics of Dehydrins: A Plant Protector Protein under Abiotic Stress
Yu, Z., Wang, X., & Zhang, L. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113420 · Cited by 144 · see citing works
Expression of yeast SOD2 in transgenic rice results in increased salt tolerance
Zhao, F., Guo, S., Zhang, H., et al. (2005) · Plant Science · doi:10.1016/j.plantsci.2005.08.017 · Cited by 121 · see citing works
Overexpression of SOD2 Increases Salt Tolerance of Arabidopsis
Gao, X., Ren, Z., Zhao, Y., et al. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.026062 · Cited by 109 · see citing works
Oh, D., Dassanayake, M., Haas, J. S., Kropornika, A., Wright, C. L., D’Urzo, M. P., Hong, H., Ali, S., Hernandez, A. G., Lambert, G. M., et al. (2010) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.163923 · Cited by 101 · see citing works
Pehlivan, N., Sun, L., Jarrett, P. C., Yang, X., Mishra, N., Chen, L., Kadıoğlu, A., Shen, G., & Zhang, H. (2016) · Plant and Cell Physiology · doi:10.1093/pcp/pcw055 · Cited by 101 · see citing works
Gaxiola, R. A., Sanchez, C. A., Paéz-Valencia, J., Ayre, B. G., & Elser, J. J. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.195701 · Cited by 99 · see citing works
Overexpression of OsVP1 and OsNHX1 Increases Tolerance to Drought and Salinity in Rice
Liu, S., Zheng, L., Xue, Y., Zhang, Q., Wang, L., & Shou, H. (2010) · Journal of Plant Biology · doi:10.1007/s12374-010-9135-6 · Cited by 97 · see citing works
Aquaporins and Root Water Uptake
(2017) · doi:10.1007/978-3-319-49395-4_6 · Cited by 89 · see citing works
Han, Y., Yin, S., Huang, L., Wu, X., Zeng, J., Liu, X., Qiu, L., Munns, R., Chen, Z.-H., & Zhang, G. (2018) · Plant and Cell Physiology · doi:10.1093/pcp/pcy116 · Cited by 85 · see citing works
Fan, W., Deng, G., Wang, H., et al. (2014) · Physiologia Plantarum · doi:10.1111/ppl.12301 · Cited by 83 · see citing works
Sodium or potassium efflux ATPase
Rodríguez‐Navarro, A., & Benito, B. (2010) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2010.07.009 · Cited by 83 · see citing works
Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis
He, C., Yang, A., Zhang, W., Gao, Q., & Zhang, J. (2010) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-009-9665-0 · Cited by 81 · see citing works
Zhang, Y.-M., Zhang, H.-M., Liu, Z., Li, H.-C., Guo, X., & Li, G. (2014) · Plant Molecular Biology · doi:10.1007/s11103-014-0278-6 · Cited by 80 · see citing works
Khan, K., Agarwal, P., Shanware, A., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0128866 · Cited by 75 · see citing works
Multifaceted roles of aquaporins as molecular conduits in plant responses to abiotic stresses
Srivastava, A. K., Suprasanna, P., Nguyen, D. V., et al. (2014) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2014.973367 · Cited by 72 · see citing works
Zhao, J., Zhi, D., Xue, Z., et al. (2007) · Journal of Plant Physiology · doi:10.1016/j.jplph.2007.04.001 · Cited by 71 · see citing works
Chen, H., Chen, X., Gu, H., et al. (2014) · Plant Growth Regulation · doi:10.1007/s10725-014-9890-3 · Cited by 70 · see citing works
SpAHA1 and SpSOS1 Coordinate in Transgenic Yeast to Improve Salt Tolerance
Zhou, Y., Yin, X., Duan, R., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137447 · Cited by 68 · see citing works
Porcel, R., Bustamante, A., Ros, R., et al. (2018) · Plant Cell & Environment · doi:10.1111/pce.13416 · Cited by 67 · see citing works
Expression of OsNHX1 gene in maize confers salt tolerance and promotes plant growth in the field
Chen, M., Chen, Q.-J., Niu, X.-G., et al. (2007) · Plant Soil and Environment · doi:10.17221/2302-pse · Cited by 63 · see citing works
LEA Proteins and the Evolution of the WHy Domain
Mertens, J., Aliyu, H., & Cowan, D. A. (2018) · Applied and Environmental Microbiology · doi:10.1128/aem.00539-18 · Cited by 61 · see citing works
Gao, J., Sun, J. Y., Cao, P., Ren, L., Liu, C., Chen, S., Chen, F., & Jiang, J. (2016) · BMC Plant Biology · doi:10.1186/s12870-016-0781-9 · Cited by 60 · see citing works
Zhang, J., Duan, Z., Zhang, D., et al. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.02.067 · Cited by 57 · see citing works
Sun, J., Cao, H., Cheng, J., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092648 · Cited by 52 · see citing works
Improving salt tolerance in potato through overexpression of AtHKT1 gene
Wang, L., Liu, Y., Li, D., et al. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1963-z · Cited by 51 · see citing works
Yang, Y., Tang, R., Li, B., Wang, H. H., Jin, Y., Jiang, C., Bao, Y., Su, H., Zhao, N., J., X., et al. (2015) · Tree Physiology · doi:10.1093/treephys/tpv027 · Cited by 49 · see citing works
Li, W., Qiang, X., Han, X., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082229 · Cited by 49 · see citing works
Overexpression of PeHA1 enhances hydrogen peroxide signaling in salt-stressed Arabidopsis
Wang, M., Wang, Y., Sun, J., et al. (2013) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2013.06.020 · Cited by 44 · see citing works
Hu, D., Sun, M., Sun, C., et al. (2015) · Scientia Horticulturae · doi:10.1016/j.scienta.2015.09.019 · Cited by 44 · see citing works
Oda, Y., Kobayashi, N. I., Tanoi, K., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19010235 · Cited by 44 · see citing works
Jacobs, A. K., Ford, K. L., Kretschmer, J. M., & Tester, M. A. (2011) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2011.00594.x · Cited by 43 · see citing works
Li, J., He, X., Li, X., Zhou, J., Wu, P., Shou, H., & Zhang, F. (2008) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b0710445 · Cited by 42 · see citing works
Lv, S., Jiang, P., Nie, L., et al. (2015) · Plant Cell & Environment · doi:10.1111/pce.12557 · Cited by 42 · see citing works
Zhou, Y., Yin, X., Wan, S., et al. (2018) · Plant Molecular Biology Reporter · doi:10.1007/s11105-018-1099-6 · Cited by 41 · see citing works
Xu, C., Zheng, L., Gao, C., Wang, C., Liu, G., Jiang, J., & Wang, Y. (2010) · Plant Molecular Biology Reporter · doi:10.1007/s11105-010-0247-4 · Cited by 39 · see citing works
Fan, Y., Wan, S., Jiang, Y., Xia, Y., Chen, X., Gao, M., Cao, Y., Luo, Y., Zhou, Y., & Jiang, X. (2018) · PROTOPLASMA · doi:10.1007/s00709-018-1275-4 · Cited by 39 · see citing works
Hu, Y., Zeng, Y., Guan, B., & Zhang, F. (2011) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-011-0013-9 · Cited by 37 · see citing works
Dabbous, A., Saad, R. B., Brini, F., Farhat, A., Zorrig, W., Abdely, C., & Hamed, K. B. (2017) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2017.01.013 · Cited by 37 · see citing works
Zhang, Y., Wang, Y., Sa, G., et al. (2017) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-017-1263-y · Cited by 36 · see citing works
Kang, P., Bao, A., Kumar, T., et al. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01598 · Cited by 35 · see citing works
Li, N., Du, C., Ma, B., et al. (2018) · Plant and Cell Physiology · doi:10.1093/pcp/pcy187 · Cited by 34 · see citing works
Chen, G., Yan, W., Yang, L., Gai, J., & Zhu, Y. (2014) · Horticulture Environment and Biotechnology · doi:10.1007/s13580-014-0003-z · Cited by 33 · see citing works
Involvement of SlSOS2 in tomato salt tolerance
Belver, A., Olías, R., Huertas, R., et al. (2012) · Bioengineered · doi:10.4161/bioe.20796 · Cited by 32 · see citing works
Plant H+-PPases: Reversible Enzymes with Contrasting Functions Dependent on Membrane Environment
Gaxiola, R. A., Regmi, K. C., Paéz-Valencia, J., Pizzio, G. A., & Zhang, S. (2015) · Molecular Plant · doi:10.1016/j.molp.2015.09.008 · Cited by 31 · see citing works
Nakayama, H., Yoshida, K., & Shinmyō, A. (2004) · Biotechnology and Bioengineering · doi:10.1002/bit.20021 · Cited by 30 · see citing works
Two alternative splicing variants of maize HKT1;1 confer salt tolerance in transgenic tobacco plants
Ren, Z., Liú, Y., Liu, Y., et al. (2015) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-015-0861-9 · Cited by 29 · see citing works
Huang, L., Kuang, L., Wu, L., et al. (2019) · Plant Growth Regulation · doi:10.1007/s10725-019-00538-7 · Cited by 29 · see citing works
Zhang, K., Song, J., Chen, X., et al. (2016) · Euphytica · doi:10.1007/s10681-016-1733-z · Cited by 27 · see citing works
Gao, L.-W., Yang, S., Wei, S., et al. (2020) · Plant Molecular Biology · doi:10.1007/s11103-020-01011-0 · Cited by 25 · see citing works
Adem, G. D., Roy, S. J., Huang, Y., et al. (2017) · Functional Plant Biology · doi:10.1071/fp17133 · Cited by 24 · see citing works
Islam, S. M. T., Tammi, R. S., Singla-Pareek, S. L., et al. (2010) · Acta Physiologiae Plantarum · doi:10.1007/s11738-009-0443-8 · Cited by 19 · see citing works
Hill, W., Jin, X., & Zhang, X. (2016) · Plant Growth Regulation · doi:10.1007/s10725-016-0169-8 · Cited by 19 · see citing works
Molecular cloning and functional characterisation of an H+-pyrophosphatase from Iris lactea
Meng, L., Li, S., Guo, J., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-18032-3 · Cited by 16 · see citing works
Roles of membrane transporters: connecting the dots from sequence to phenotype
David, R., Byrt, C. S., Tyerman, S. D., et al. (2019) · Annals of Botany · doi:10.1093/aob/mcz066 · Cited by 15 · see citing works
Kishimoto, M., Shimajiri, Y., Oshima, A., et al. (2013) · Plant Biotechnology · doi:10.5511/plantbiotechnology.13.0517a · Cited by 14 · see citing works
Overexpression ofENA1 from yeast increases salt tolerance inArabidopsis
Kong, X., Gao, X., Li, W., Zhao, J., Zhao, Y., & Zhang, H. (2008) · Journal of Plant Biology · doi:10.1007/bf03030726 · Cited by 12 · see citing works
Bublitz, M., Morth, J. P., & Nissen, P. (2011) · Journal of Cell Science · doi:10.1242/jcs.102921 · Cited by 11 · see citing works
Li, X., Wang, F., Sun, D., et al. (2018) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-018-1430-9 · Cited by 8 · see citing works
Overexpressing Vitis vinifera YSK2 dehydrin in tobacco improves plant performance
Jardak, R., Zarrouk, O., Salem, A. B., Zoghlami, N., Mejri, S., Gandoura, S., Khiari, B., Mliki, A., Chaves, M. M., Ghorbel, A., et al. (2015) · Agricultural Water Management · doi:10.1016/j.agwat.2015.09.023 · Cited by 7 · see citing works
Dong, Q., Liu, D. D., Wang, Q., Fang, M.-J., Hao, Y., & Yao, Y. (2015) · Russian Journal of Plant Physiology · doi:10.1134/s1021443715050064 · Cited by 6 · see citing works
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Integrated approaches for increasing plant yield under salt stress
Ahmad, I., Zhu, G., Zhou, G., Younas, M. U., Suliman, M. S. E., Liu, J., Zhu, Y. M., & Salih, E. G. I. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2023.1215343 · Cited by 48 · see citing works
“Despite much research documented in understanding the response of plants to salt stress, the breeding of salt-resistant genotypes remains slow, with limited progress in plants (Asif et al., 2018; Kotula et al., 2020).”
BackgroundEmerging applications of gene editing technologies for the development of climate-resilient crops
Chavhan, R. L., Jaybhaye, S. G., Hinge, V. R., Deshmukh, A. S., Shaikh, U. S., Jadhav, P. K., Kadam, U. S., & Hong, J. C. (2025) · Frontiers in Genome Editing · doi:10.3389/fgeed.2025.1524767 · Cited by 43 · see citing works
- Authors
- Kotula, L., Garcia Caparros, P., Zörb, C., Colmer, T. D., & Flowers, T. J.
- Affiliations
- The University of Western Australia (AU)
- Agronomy Department of Superior School Engineering University of Almeria, CIAIMBITAL, Agrifood Campus of International Excellence ceiA3 Almería Spain
- University of Hohenheim (DE)
- University of Sussex (GB)
- Corresponding author
- Colmer, Timothy D.
- Venue
- Plant, Cell & Environment
- Publisher
- Wiley
- Published
- 2020-09-15
- Volume
- 43
- Issue
- 12
- Pages
- 2932-2956
- ISSN
- 0140-7791 (ISSN-L)
- 1365-3040
- OpenAlex
- W3047450346
- Cited by
- 125
- References
- 133
- Citations by year
- 2026: 12 · 2025: 20 · 2024: 23 · 2023: 17 · 2022: 28 · 2021: 19 · 2020: 6
- FWCI
- 1.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Plant Cell & Environment (publishedVersion)
- PubMed (publishedVersion)
- UWA Profiles and Research Repository (UWA) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
- Keywords
- salt tolerance, salt stress, genetically modified crops, Na+ exclusion, vacuolar H+-ATPase, aquaporins, dehydrins, drought stress, ion homeostasis, land salinization
- MeSH terms
- Crop Production, Crops, Agricultural, Plants, Genetically Modified, Salt Tolerance, Salt-Tolerant Plants
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