Mechanism of salt stress tolerance in plants: role of cation/proton antiporters

Qurban Ali, Muzammal Mateen Azhar, Arif Malik, Shahbaz Ahmad, Muhammad Zafar Saleem, Muhammad Waseem

Abstract


Salinity is an important adversive environmental problem that caused loss in sense of reducing yield per plant, morphological and physiological functions of crop plants. The plants compete with environmental stress conditions to withstand following normal growth and development. The exchange of cations or protons takes place across the cell membrane to maintain the osmotic pressure of cells under salt stress conditions. There is a huge number of cation/H+ antiporter 1 proteins producing genes by plant cells under salt stress conditions has been identified however, a few has been characterized and sequenced which contributes in ion homeostasis and osmotic adjustment of cells. These cation/H+ antiporters are produced and stored in the vacuoles, endosomal forms and in cytoplasm. The cation/H+ antiporters are involved in the homeostasis of K+, Na+, and pH of the cell under salinity stress conditions. The cation/H+ antiporters help plants cells to regulate all physiological functions under salt stress conditions.


Keywords


salt tolerance, Na+, K+, cation, pH, homeostasis, AtNHX1 gene

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References


Abogadallah, G. M. (2010). Insights into the significance of antioxidative defense under salt stress. Plant signaling & behavior 5, 369-374.

Adams, E., and Shin, R. (2014). Transport, signaling, and homeostasis of potassium and sodium in plants. Journal of integrative plant biology 56, 231-249.

Aharon, G. S., Apse, M. P., Duan, S., Hua, X., and Blumwald, E. (2003). Characterization of a family of vacuolar Na+/H+ antiporters in Arabidopsis thaliana. Plant and Soil 253, 245-256.

Ahmadi, H., Corso, M., Weber, M., Verbruggen, N., and Clemens, S. (2018). CAX1 suppresses Cd‐induced generation of reactive oxygen species in Arabidopsis halleri. Plant, cell & environment 41, 2435-2448.

Almeida, D. M., Oliveira, M. M., and Saibo, N. J. (2017). Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genetics and molecular biology 40, 326-345.

An, R., Chen, Q.-j., Chai, M.-f., Lu, P.-l., Su, Z., Qin, Z.-x., Chen, J., and Wang, X.-c. (2007). atnhx8: proton antiporter-1 family in arabidopsis thaliana, encodes a putative Li+/h+ antiporter, a member of the monovalent cation: proton antiporter-1 family in arabidopsis thaliana, encodes a putative Li+/h+ antiporter. The Plant Journal 49, 718-728.

Apse, M. P., Aharon, G. S., Snedden, W. A., and Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256-1258.

Apse, M. P., and Blumwald, E. (2007). Na+ transport in plants. FEBS letters 581, 2247-2254.

Ashraf, M., Athar, H., Harris, P., and Kwon, T. (2008). Some prospective strategies for improving crop salt tolerance. Advances in agronomy 97, 45-110.

Baghour, M., Gálvez, F. J., Sánchez, M. E., Aranda, M. N., Venema, K., and Rodríguez-Rosales, M. P. (2019). Overexpression of LeNHX2 and SlSOS2 increases salt tolerance and fruit production in double transgenic tomato plants. Plant Physiology and Biochemistry 135, 77-86.

Bartels, D., and Sunkar, R. (2005). Drought and salt tolerance in plants. Critical reviews in plant sciences 24, 23-58.

Bassil, E., and Blumwald, E. (2014). The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters. Current opinion in plant biology 22, 1-6.

Brett, C. L., Donowitz, M., and Rao, R. (2005). Evolutionary origins of eukaryotic sodium/proton exchangers. American Journal of Physiology-Cell Physiology 288, C223-C239.

Cai, X., Zhang, C., Shu, W., Ye, Z., Li, H., and Zhang, Y. (2016). The transcription factor SlDof22 involved in ascorbate accumulation and salinity stress in tomato. Biochemical and biophysical research communications 474, 736-741.

Cao, B., Long, D., Zhang, M., Liu, C., Xiang, Z., and Zhao, A. (2016). Molecular characterization and expression analysis of the mulberry Na+/H+ exchanger gene family. Plant physiology and biochemistry 99, 49-58.

Casey, J. R., Grinstein, S., and Orlowski, J. (2010). Sensors and regulators of intracellular pH. Nature reviews Molecular cell biology 11, 50.

Cerevisiae, S., Bowers, K., Levi, B. P., Patel, F. I., and Stevens, T. H. (2000). The Sodium/Proton Exchanger Nhx1p Is Required for Endosomal Protein Trafficking in the Yeast.

Chanroj, S., Wang, G., Venema, K., Zhang, M. W., Delwiche, C. F., and Sze, H. (2012). Conserved and diversified gene families of monovalent cation/H+ antiporters from algae to flowering plants. Frontiers in plant science 3, 25.

Chauhan, S., Forsthoefel, N., Ran, Y., Quigley, F., Nelson, D. E., and Bohnert, H. J. (2000). Na+/myo‐inositol symporters and Na+/H+‐antiport in Mesembryanthemum crystallinum. The Plant Journal 24, 511-522.

Chien, P.-S., Nam, H. G., and Chen, Y.-R. (2015). A salt-regulated peptide derived from the CAP superfamily protein negatively regulates salt-stress tolerance in Arabidopsis. Journal of experimental botany 66, 5301-5313.

Deinlein, U., Stephan, A. B., Horie, T., Luo, W., Xu, G., and Schroeder, J. I. (2014). Plant salt-tolerance mechanisms. Trends in plant science 19, 371-379.

Dhar, R., Sägesser, R., Weikert, C., Yuan, J., and Wagner, A. (2011). Adaptation of Saccharomyces cerevisiae to saline stress through laboratory evolution. Journal of evolutionary biology 24, 1135-1153.

Djanaguiraman, M., and Prasad, P. V. (2013). Effects of salinity on ion transport, water relations and oxidative damage. In "Ecophysiology and Responses of Plants under Salt Stress", pp. 89-114. Springer.

Feki, K., Quintero, F. J., Khoudi, H., Leidi, E. O., Masmoudi, K., Pardo, J. M., and Brini, F. (2014). A constitutively active form of a durum wheat Na+/H+ antiporter SOS1 confers high salt tolerance to transgenic Arabidopsis. Plant cell reports 33, 277-288.

Fukuda, A., Nakamura, A., Tagiri, A., Tanaka, H., Miyao, A., Hirochika, H., and Tanaka, Y. (2004). Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant and cell physiology 45, 146-159.

Gao, X., Ren, Z., Zhao, Y., and Zhang, H. (2003). Overexpression of SOD2 increases salt tolerance of Arabidopsis. Plant physiology 133, 1873-1881.

Gaxiola, R. A., Rao, R., Sherman, A., Grisafi, P., Alper, S. L., and Fink, G. R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proceedings of the National Academy of Sciences 96, 1480-1485.

Gharsallah, C., Fakhfakh, H., Grubb, D., and Gorsane, F. (2016). Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants 8.

Hamaji, K., Nagira, M., Yoshida, K., Ohnishi, M., Oda, Y., Uemura, T., Goh, T., Sato, M. H., Morita, M. T., and Tasaka, M. (2009). Dynamic aspects of ion accumulation by vesicle traffic under salt stress in Arabidopsis. Plant and cell physiology 50, 2023-2033.

Hasanuzzaman, M., Nahar, K., Alam, M., Roychowdhury, R., and Fujita, M. (2013). Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. International journal of molecular sciences 14, 9643-9684.

Hasegawa, P. M., Bressan, R. A., Zhu, J.-K., and Bohnert, H. J. (2000). Plant cellular and molecular responses to high salinity. Annual review of plant biology 51, 463-499.

He, C., Yan, J., Shen, G., Fu, L., Holaday, A. S., Auld, D., Blumwald, E., and Zhang, H. (2005). Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant and cell physiology 46, 1848-1854.

Hedrich, R. (2012). Ion channels in plants. Physiological reviews 92, 1777-1811.

Horie, T., Karahara, I., and Katsuhara, M. (2012). Salinity tolerance mechanisms in glycophytes: An overview with the central focus on rice plants. Rice 5, 11.

Hrabak, E. M., Chan, C. W., Gribskov, M., Harper, J. F., Choi, J. H., Halford, N., Kudla, J., Luan, S., Nimmo, H. G., and Sussman, M. R. (2003). The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant physiology 132, 666-680.

Huertas, R., Rubio, L., Cagnac, O., GARCÍA‐SÁNCHEZ, M. J., ALCHÉ, J. D. D., Venema, K., FERNÁNDEZ, J. A., and RODRÍGUEZ‐ROSALES, M. P. (2013). The K+/H+ antiporter LeNHX2 increases salt tolerance by improving K+ homeostasis in transgenic tomato. Plant, cell & environment 36, 2135-2149.

Ismail, A., Riemann, M., and Nick, P. (2012). The jasmonate pathway mediates salt tolerance in grapevines. Journal of Experimental Botany 63, 2127-2139.

Janz, D., Behnke, K., Schnitzler, J.-P., Kanawati, B., Schmitt-Kopplin, P., and Polle, A. (2010). Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biology 10, 150.

Jha, B., Mishra, A., Jha, A., and Joshi, M. (2013). Developing transgenic Jatropha using the SbNHX1 gene from an extreme halophyte for cultivation in saline wasteland. PLoS One 8, e71136.

Jia, Q., Zheng, C., Sun, S., Amjad, H., Liang, K., and Lin, W. (2018). The role of plant cation/proton antiporter gene family in salt tolerance. Biologia Plantarum, 1-13.

Jiang, W., Sun, L., Yang, X., Wang, M., Esmaeili, N., Pehlivan, N., Zhao, R., Zhang, H., and Zhao, Y. (2017). The Effects of Transcription Directions of Transgenes and the gypsy Insulators on the Transcript Levels of Transgenes in Transgenic Arabidopsis. Scientific reports 7, 14757.

Jiang, X., Leidi, E. O., and Pardo, J. M. (2010). How do vacuolar NHX exchangers function in plant salt tolerance? Plant signaling & behavior 5, 792-795.

Krebs, M., Beyhl, D., Görlich, E., Al-Rasheid, K. A., Marten, I., Stierhof, Y.-D., Hedrich, R., and Schumacher, K. (2010). Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proceedings of the National Academy of Sciences 107, 3251-3256.

Krulwich, T. A., Sachs, G., and Padan, E. (2011). Molecular aspects of bacterial pH sensing and homeostasis. Nature Reviews Microbiology 9, 330.

Kumar, K., Kumar, M., Kim, S.-R., Ryu, H., and Cho, Y.-G. (2013). Insights into genomics of salt stress response in rice. Rice 6, 27.

Latef, A. A. H. A., and Ahmad, P. (2015). Legumes and breeding under abiotic stress: an overview. Legumes under Environmental Stress: Yield, Improvement and Adaptations, 315.

Leidi, E. O., Barragán, V., Rubio, L., El‐Hamdaoui, A., Ruiz, M. T., Cubero, B., Fernández, J. A., Bressan, R. A., Hasegawa, P. M., and Quintero, F. J. (2010). The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. The Plant Journal 61, 495-506.

Li, M., Li, Y., Li, H., and Wu, G. (2011). Overexpression of AtNHX5 improves tolerance to both salt and drought stress in Broussonetia papyrifera (L.) Vent. Tree physiology 31, 349-357.

Li, N., Wang, X., Ma, B., Du, C., Zheng, L., and Wang, Y. (2017). Expression of a Na+/H+ antiporter RtNHX1 from a recretohalophyte Reaumuria trigyna improved salt tolerance of transgenic Arabidopsis thaliana. Journal of plant physiology 218, 109-120.

Ma, D.-M., Xu, W.-R., Li, H.-W., Jin, F.-X., Guo, L.-N., Wang, J., Dai, H.-J., and Xu, X. (2014). Co-expression of the Arabidopsis SOS genes enhances salt tolerance in transgenic tall fescue (Festuca arundinacea Schreb.). Protoplasma 251, 219-231.

Ma, S., and Bohnert, H. J. (2007). Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome biology 8, R49.

Ma, Y. C., Augé, R. M., Dong, C., and Cheng, Z. M. (2017). Increased salt tolerance with overexpression of cation/proton antiporter 1 genes: a meta‐analysis. Plant biotechnology journal 15, 162-173.

Mahajan, S., and Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Archives of biochemistry and biophysics 444, 139-158.

Manohar, M., Shigaki, T., and Hirschi, K. (2011). Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biology 13, 561-569.

Martínez-Atienza, J., Jiang, X., Garciadeblas, B., Mendoza, I., Zhu, J.-K., Pardo, J. M., and Quintero, F. J. (2007). Conservation of the salt overly sensitive pathway in rice. Plant physiology 143, 1001-1012.

Martinière, A., Bassil, E., Jublanc, E., Alcon, C., Reguera, M., Sentenac, H., Blumwald, E., and Paris, N. (2013). In vivo intracellular pH measurements in tobacco and Arabidopsis reveal an unexpected pH gradient in the endomembrane system. The Plant Cell 25, 4028-4043.

Mäser, P., Thomine, S., Schroeder, J. I., Ward, J. M., Hirschi, K., Sze, H., Talke, I. N., Amtmann, A., Maathuis, F. J., and Sanders, D. (2001). Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiology 126, 1646-1667.

Mazel, A., Leshem, Y., Tiwari, B. S., and Levine, A. (2004). Induction of salt and osmotic stress tolerance by overexpression of an intracellular vesicle trafficking protein AtRab7 (AtRabG3e). Plant physiology 134, 118-128.

McCubbin, T., Bassil, E., Zhang, S., and Blumwald, E. (2014). Vacuolar Na+/H+ NHX-type antiporters are required for cellular K+ homeostasis, microtubule organization and directional root growth. Plants 3, 409-426.

Mei, H., Cheng, N. H., Zhao, J., Park, S., Escareno, R. A., Pittman, J. K., and Hirschi, K. D. (2009). Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytologist 183, 95-105.

Mickelbart, M. V., Hasegawa, P. M., and Bailey-Serres, J. (2015). Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nature Reviews Genetics 16, 237.

Miller, G., Suzuki, N., Ciftci‐Yilmaz, S., and Mittler, R. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, cell & environment 33, 453-467.

Morgan, A. J., Platt, F. M., Lloyd-Evans, E., and Galione, A. (2011). Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease. Biochemical Journal 439, 349-378.

Munns, R., and Gilliham, M. (2015). Salinity tolerance of crops–what is the cost? New phytologist 208, 668-673.

Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651-681.

Noreen, S., Siddiq, A., Hussain, K., Ahmad, S., and Hasanuzzaman, M. (2017). Foliar application of salicylic acid with salinity stress on physiological and biochemical attributes of sunflower (Helianthus annuus L.) crop. Acta Scientiarum Polonorum-Hortorum Cultus 16, 57-74.

Ohnishi, M., Fukada-Tanaka, S., Hoshino, A., Takada, J., Inagaki, Y., and Iida, S. (2005). Characterization of a novel Na+/H+ antiporter gene InNHX2 and comparison of InNHX2 with InNHX1, which is responsible for blue flower coloration by increasing the vacuolar pH in the Japanese morning glory. Plant and cell physiology 46, 259-267.

Ohta, M., Hayashi, Y., Nakashima, A., Hamada, A., Tanaka, A., Nakamura, T., and Hayakawa, T. (2002). Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS letters 532, 279-282.

Olías, R., Eljakaoui, Z., Li, J., DE MORALES, P. A., MARÍN‐MANZANO, M. C., Pardo, J. M., and Belver, A. (2009). The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant, cell & environment 32, 904-916.

Orij, R., Brul, S., and Smits, G. J. (2011). Intracellular pH is a tightly controlled signal in yeast. Biochimica et Biophysica Acta (BBA)-General Subjects 1810, 933-944.

Padmanaban, S., Chanroj, S., Kwak, J. M., Li, X., Ward, J. M., and Sze, H. (2007). Participation of endomembrane cation/H+ exchanger AtCHX20 in osmoregulation of guard cells. Plant Physiology 144, 82-93.

Pardo, J. M., Cubero, B., Leidi, E. O., and Quintero, F. J. (2006). Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. Journal of experimental botany 57, 1181-1199.

Pardo, J. M., and Rubio, F. (2011). Na+ and K+ transporters in plant signaling. In "Transporters and pumps in plant signaling", pp. 65-98. Springer.

Park, H. J., Kim, W.-Y., and Yun, D.-J. (2016). A new insight of salt stress signaling in plant. Molecules and cells 39, 447.

Paroutis, P., Touret, N., and Grinstein, S. (2004). The pH of the secretory pathway: measurement, determinants, and regulation. Physiology 19, 207-215.

Pehlivan, N., Sun, L., Jarrett, P., Yang, X., Mishra, N., Chen, L., Kadioglu, A., Shen, G., and Zhang, H. (2016). Co-overexpressing a plasma membrane and a vacuolar membrane sodium/proton antiporter significantly improves salt tolerance in transgenic Arabidopsis plants. Plant and Cell Physiology 57, 1069-1084.

Pinedo, I., Ledger, T., Greve, M., and Poupin, M. J. (2015). Burkholderia phytofirmans PsJN induces long-term metabolic and transcriptional changes involved in Arabidopsis thaliana salt tolerance. Frontiers in plant science 6, 466.

Pitman, M. G., and Läuchli, A. (2002). Global impact of salinity and agricultural ecosystems. In "Salinity: environment-plants-molecules", pp. 3-20. Springer.

Pittman, J. (2012). Multiple transport pathways for mediating intracellular pH homeostasis: the contribution of H+/ion exchangers. Frontiers in plant science 3, 11.

Qiu, Q.-S., Guo, Y., Dietrich, M. A., Schumaker, K. S., and Zhu, J.-K. (2002). Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proceedings of the National Academy of Sciences 99, 8436-8441.

Qiu, Q.-S., Guo, Y., Quintero, F. J., Pardo, J. M., Schumaker, K. S., and Zhu, J.-K. (2004). Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly-sensitive (SOS) pathway. Journal of Biological Chemistry 279, 207-215.

Quintero, F. J., Blatt, M. R., and Pardo, J. M. (2000). Functional conservation between yeast and plant endosomal Na+/H+ antiporters 1. FEBS letters 471, 224-228.

Quintero, F. J., Ohta, M., Shi, H., Zhu, J.-K., and Pardo, J. M. (2002). Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proceedings of the National Academy of Sciences 99, 9061-9066.

Rajagopal, D., Agarwal, P., Tyagi, W., Singla-Pareek, S. L., Reddy, M. K., and Sopory, S. (2007). Pennisetum glaucum Na+/H+ antiporter confers high level of salinity tolerance in transgenic Brassica juncea. Molecular Breeding 19, 137-151.

Reddy, I. N. B. L., Kim, B.-K., Yoon, I.-S., Kim, K.-H., and Kwon, T.-R. (2017). Salt tolerance in rice: focus on mechanisms and approaches. Rice Science 24, 123-144.

Reguera, M., Bassil, E., and Blumwald, E. (2014). Intracellular NHX-type cation/H+ antiporters in plants. Molecular plant 7, 261-263.

Rodríguez-Rosales, M. P., Gálvez, F. J., Huertas, R., Aranda, M. N., Baghour, M., Cagnac, O., and Venema, K. (2009). Plant NHX cation/proton antiporters. Plant signaling & behavior 4, 265-276.

Roy, S. J., Negrão, S., and Tester, M. (2014). Salt resistant crop plants. Current opinion in Biotechnology 26, 115-124.

Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B.-h., Matsumoto, T. K., Koiwa, H., Zhu, J.-K., Bressan, R. A., and Hasegawa, P. M. (2001). AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proceedings of the national academy of sciences 98, 14150-14155.

Sajid, M., Rashid, B., and Ali, Q. (2018). Mechanisms of heat sensing and responses in plants. It is not all about Ca 2+ ions. Biologia plantarum, 1-12.

Senadheera, P., Singh, R., and Maathuis, F. J. (2009). Differentially expressed membrane transporters in rice roots may contribute to cultivar dependent salt tolerance. Journal of experimental botany 60, 2553-2563.

Serrano, R., and Rodriguez-Navarro, A. (2001). Ion homeostasis during salt stress in plants. Current opinion in cell biology 13, 399-404.

Shabala, S., and Munns, R. (2012). Salinity stress: physiological constraints and adaptive mechanisms. Plant stress physiology 1, 59-93.

Shen, J., Zeng, Y., Zhuang, X., Sun, L., Yao, X., Pimpl, P., and Jiang, L. (2013). Organelle pH in the Arabidopsis endomembrane system. Molecular plant 6, 1419-1437.

Shi, Y., and Massagué, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. cell 113, 685-700.

Shin, R. (2014). Strategies for improving potassium use efficiency in plants. Molecules and cells 37, 575.

Suzuki, N., Rivero, R. M., Shulaev, V., Blumwald, E., and Mittler, R. (2014). Abiotic and biotic stress combinations. New Phytologist 203, 32-43.

Tester, M., and Davenport, R. (2003). Na+ tolerance and Na+ transport in higher plants. Annals of botany 91, 503-527.

Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M., and Stockinger, B. (2006). TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24, 179-189.

Venema, K., Belver, A., Marín-Manzano, M. C., Rodríguez-Rosales, M. P., and Donaire, J. P. (2003). A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants. Journal of Biological Chemistry 278, 22453-22459.

Vinocur, B., and Altman, A. (2005). Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Current opinion in biotechnology 16, 123-132.

Wang, B., Zhai, H., He, S., Zhang, H., Ren, Z., Zhang, D., and Liu, Q. (2016). A vacuolar Na+/H+ antiporter gene, IbNHX2, enhances salt and drought tolerance in transgenic sweetpotato. Scientia horticulturae 201, 153-166.

Wang, L., Wu, X., Liu, Y., and Qiu, Q.-S. (2015). AtNHX5 and AtNHX6 control cellular K+ and pH homeostasis in Arabidopsis: three conserved acidic residues are essential for K+ transport. PloS one 10, e0144716.

Wu, X., Ebine, K., Ueda, T., and Qiu, Q.-S. (2016a). AtNHX5 and AtNHX6 are required for the subcellular localization of the SNARE complex that mediates the trafficking of seed storage proteins in Arabidopsis. PLoS One 11, e0151658.

Wu, X., Li, J., Wu, X., Liu, Q., Wang, Z., Liu, S., Li, S., Ma, Y., Sun, J., and Zhao, L. (2016b). Ectopic expression of Arabidopsis thaliana Na+(K+)/H+ antiporter gene, AtNHX5, enhances soybean salt tolerance. Genet. Mol. Res 15, 1-12.

Xiong, L., Schumaker, K. S., and Zhu, J.-K. (2002). Cell signaling during cold, drought, and salt stress. The plant cell 14, S165-S183.

Yadav, N. S., Shukla, P. S., Jha, A., Agarwal, P. K., and Jha, B. (2012). The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC plant biology 12, 188.

Yamaguchi, T., and Blumwald, E. (2005). Developing salt-tolerant crop plants: challenges and opportunities. Trends in plant science 10, 615-620.

Yokoi, S., Quintero, F. J., Cubero, B., Ruiz, M. T., Bressan, R. A., Hasegawa, P. M., and Pardo, J. M. (2002). Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. The Plant Journal 30, 529-539.

Yoshida, K., Kawachi, M., Mori, M., Maeshima, M., Kondo, M., Nishimura, M., and Kondo, T. (2005). The involvement of tonoplast proton pumps and Na+ (K+)/H+ exchangers in the change of petal color during flower opening of morning glory, Ipomoea tricolor cv. Heavenly Blue. Plant and Cell Physiology 46, 407-415.

Yue, Y., Zhang, M., Zhang, J., Duan, L., and Li, Z. (2012). SOS1 gene overexpression increased salt tolerance in transgenic tobacco by maintaining a higher K+/Na+ ratio. Journal of Plant Physiology 169, 255-261.

Zhang, Z., Yao, X., and Zhu, H. (2010). Potential application of geopolymers as protection coatings for marine concrete: II. Microstructure and anticorrosion mechanism. Applied clay science 49, 7-12.

Zhao, J., Barkla, B. J., Marshall, J., Pittman, J. K., and Hirschi, K. D. (2008). The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227, 659-669.

Zheng, S., Pan, T., Fan, L., and Qiu, Q.-S. (2013). A novel AtKEA gene family, homolog of bacterial K+/H+ antiporters, plays potential roles in K+ homeostasis and osmotic adjustment in Arabidopsis. PLoS One 8, e81463.

Zhou, Y., Yin, X., Wan, S., Hu, Y., Xie, Q., Li, R., Zhu, B., Fu, S., Guo, J., and Jiang, X. (2018). The Sesuvium portulacastrum Plasma Membrane Na+/H+ Antiporter SpSOS1 Complemented the Salt Sensitivity of Transgenic Arabidopsis sos1 Mutant Plants. Plant Molecular Biology Reporter 36, 553-563.

Zhu, J.-K. (2003). Regulation of ion homeostasis under salt stress. Current opinion in plant biology 6, 441-445.




DOI: http://doi.org/10.17503/agrivita.v42i3.2242

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