Strategies of NHX antiporters to deal with salt stress

Authors

DOI:

https://doi.org/10.14719/pst.2442

Keywords:

NHX, Salt stress, homeostasis, antiport, tolerance, SOS

Abstract

The adverse effects of salinity on plant growth are generally associated with the low osmotic potential of the soil solution and the high level of sodium toxicity (and chlorine toxicity for some species) which cause multiple perturbations on plant metabolism, growth, and development at the molecular, biochemical and physiological levels. The vacuolar NHX and plasma membrane SOS antiporters mediate cation and proton exchange across the tonoplast and plasma membrane, respectively. The SOS transporters allow the excretion of Na+ from the cytoplasm to the outside environment and alternatively, NHXs provide Na+ transport from the cytoplasm to the vacuole. Cellular ion homeostasis is an essential phenomenon for all organisms. Most cells manage to maintain a high level of potassium and a low level of sodium in the cytoplasm through the coordination and regulation of different transporters and channels instead of the NHX-type vacuolar antiport. In this article, some important mechanisms in the regulation of ionic ions such as Na+. will be discussed.

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References

FAO, Land. Plant Nutrition Management Service. 2008. [updated 2023 Jun 23; cited 2008 Jun 30]. Available from:http://www.fao.org/ag/agl/agll/spush

FAO, ITPS, GSBI, CBD and EC. 2020. State of knowledge of soil biodiversity - Status, challenges and potentialities, Report 2020. Rome, FAO.

Peleg Z, Blumwald E. Hormone balance and abiotic stress tolerance in crop plants. Current opinion in plant biology. 2011;14:290-295. https://doi.org/10.1016/j.pbi.2011.02.001

Smirnoff N, Stewart G.. Stress metabolites and their role in coastal plants. Ecology of coastal vegetation. Springer, 1985; pp. 273-278. https://doi.org/10.1007/978-94-009-5524-0_30

Patel JA, Vora, AB. Free proline accumulation in drought-stressed plants. Plant Soil 1985;84:427–29. https://doi.org/10.1007/BF02275480

Bartels D., Sunkar, R. Drought and salt tolerance in plants. Crit Rev Plant Sci. 2005; 24, 23-58. https://doi.org/10.1080/07352680590910410

Grote D, Claussen W. 2001. Severity of root rot on tomato plants caused by Phytophthora nicotianae under nutrient?and light?stress conditions. Plant Pathol. 50; 702-707. https://doi.org/10.1046/j.1365-3059.2001.00612.x

Zhu, JK, Liu J, Xiong L. Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 1998; 10:1181-1191. https://doi.org/10.1105/tpc.10.7.1181

Baghour M, Chekroun KB, Rodríguez-Rosales MP, Venema K.. Antiporters: role in salinity tolerance (a review). Moroc J Biol, 2010; 6:16-22

Dajic Z. Salt stress. Physiology and molecular biology of stress tolerance in plants. Springer. 2006:41-99. https://doi.org/10.1007/1-4020-4225-6_3

Mahajan S, Pandey GK, Tuteja N. Calcium- and salt stress signaling in plants: Shedding light on SOS pathway. Arch. Biochem. Biophys, 47:146–58. https://doi:10.1016/j.abb.2008.01. 010. PMID:18241665.

Chinnusamy V, Jagendorf A, Zhu JK. Understanding and improving salt tolerance in plants. Crop Sci. 2005. 45;437–48. https://doi:10.2135/cropsci2005.0437

Leidi EO, Barragán V, Rubio L, El?Hamdaoui A, Ruiz MT, Cubero B, Fernández JA, Bressan RA, Hasegawa PM, Quintero F. The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant Journal. 2010;61:495-06. https://doi.org/10.1111/j.1365-313X.2009.04073.x

Mäser P, Thomine S, Schroeder JI, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 2001;126:1646-67. https://doi.org/10.1104/pp.126.4.1646

Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K. Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt and drought stress tolerance in Arabidopsis thaliana plants. J Exp Bot. 2005;58:301-08. https://doi.org/10.1093/jxb/erl251

Halfter U, Ishitani, M, Zhu, JK. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proceedings of the National Academy of Sciences 2000; 97(7), 3735-40. https://doi.org/10.1073/pnas.97.7.3735

Shi H, Zhu JK. Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol Biol. 2002;50:543-50. https://doi.org/10.1023/A:1019859319617

Barragan V, Leidi EO, Andres Z, Rubio L, De Luca A, Fernandez JA, Pardo, JM. Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. The Plant Cell, 2012; 24(3), 1127-42. https://doi.org/10.1105/tpc.111.095273

Walker DJ Leighv RA, MillervAJ. Potassium homeostasis in vacuolate plant cells. Proc. Natl. Acad. Sci 1996; 93:10510–14. https://doi.org/10.1073/pnas.93.19.10510

Venema K, Belver, A, Marín-Manzano MC, Rodríguez-Rosales MP, Donaire JP. A novel intracellular K+/H+ antiporter related to Na+/H+ antiporters is important for K+ ion homeostasis in plants. J Biol Chem. 2003;278:22453-59. https://doi.org/10.1074/jbc.M210794200

Rahneshan R, Nasibi F, Lakehal A, Bellini C. Unravelling salt stress responses in two pistachio (Pistacia vera L.) genotypes. Acta Physiol Plant 2018;40:172. https://doi.org/10.1007/s11738-018-2745-1

Dong J, Liu C, Wang Y, Zhao Y, Ge D, Yuan Z. Genome-wide identification of the NHX gene family in Punica granatum L. and their expressional patterns under salt stress. Agronomy 2021;11:264 https://doi.org/10.3390/agronomy11020264

Fan W, Denga G, Wang H, Zhang H, Zhang P. Elevated compartmentalization of Na+ into vacuoles improves salt and cold stress tolerance in sweet potato (Ipomoea batatas). Physiol Plant 2015;154:560–71. https://doi.org/10.1111/ppl.12301

Mäser P, Thomine S, Schroeder J.I, Ward JM, Hirschi K, Sze H, Talke IN, Amtmann A, Maathuis FJ, Sanders D. Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 2001;26:1646-67. https://doi.org/10.1104%2Fpp.126.4.1646

Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM.. Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant cell. 2012;24:1127-42. https://doi.org/10.1105/tpc.111.095273

Brett CL, Donowitz M, Rao R. Evolutionary origins of eukaryotic sodium/proton exchangers. Am. J. Physiol. Cell Physiol. 2005;288:C223-39. https://doi.org/10.1152/ajpcell.00360.2004

Porat R, Daus A, Weiss B, Cohen L, Droby S. Biotechnology. Effects of combining hot water, sodium bicarbonate, and biocontrol on postharvest decay of citrus fruit. J Hortic Sci. Biotechnol. 2002;77:441-45. https://doi.org/10.1080/14620316.2002.11511519

Apse MP, Sottosanto JB, Blumwald E. Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T?DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J. 2003;36:229-39

Yamaguchi T, Apse MP Shi H, Blumwald E. Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity. Proc Natl Acad. 2003;100:12510-15. https://doi.org/10.1073/pnas.2034966100

Hasegawa PM, Bressan RA, Zhu J-K, Bohnert H. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Biol. 2000;51:463-99. https://doi.org/10.1146/annurev.arplant.51.1.463

Shi H., Zhu JK. Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol Biol. 2002; 50:543-50. https://doi.org/10.1023/A:1019859319617

Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y. Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant. Cell. Physiol. 2004;45:146-59. https://doi.org/10.1093/pcp/pch014

Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E. Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+-and pH-dependent manner. Proc. Natl. Acad 2005;102:16107-12. https://doi.org/10.1073/pnas.0504437102

Wu CA, Yang GD, Meng QW, Zheng CC. The cotton GhNHX1 gene encoding a novel putative tonoplast Na+/H+ antiporter plays an important role in salt stress. Plant Cell Physiol. 2004;45:600-07. https://doi.org/10.1093/pcp/pch071

Walker DJ, Leigh RA, Miller AJ. Potassium homeostasis in vacuolate plant cells. Proc. Natl. Acad. Sci.U.S.A. 1996;93:10510–14. https://doi.org/10.1073/pnas.93.19.10510

Barkla BJ, Zingarelli L, Blumwald E, Smith JAC. Tonoplast Na+/H+ antiport activity and its energization by the vacuolar H+-ATPase in the halophytic plant Mesembryanthemum crystallinum L. Plant Physiol. 1995;109:549–56. https://doi.org/10.1104/pp.109.2.549

Staal M, Maathuis FJ, Elzenga JTM, Overbeek JHM, Prins HBA. Na+/H+ antiport activity in tonoplast vesicles from roots of the salt?tolerant Plantago maritima and the salt?sensitive Plantago media. Physiol. Plant. 1991;82:179-84. https://doi.org/10.1111/j.1399-3054.1991.tb00078.x

Ballesteros E, Blumwald E, Donaire JP, Belver A. Na+/H+ antiport activity in tonoplast vesicles isolated from sunflower roots induced by NaCl stress. Physiol. Plant. 1997;99:328-334. https://doi.org/10.1111/j.1399-3054.1997.tb05420.x

Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K. Overexpression of wheat Na+/H+ antiporter TNHX1 and H+-pyrophosphatase TVP1 improve salt and drought stress tolerance in Arabidopsis thaliana plants. J Exp Bot. 2007;58:301-08. https://doi.org/10.1093/jxb/erl251

Apse MP, Aharon GS, Snedden WA, Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis.Science 1999;285:1256-58. https://doi.org/10.1126/science.285.5431.1256

Sakano K. Revision of biochemical pH?Stat: Involvement of alternative pathway metabolisms. Plant Cell Physiol. 1998;39:467?73. https://doi.org/10.1093/oxfordjournals.pcp.a029393

Zhao J, Davis LC, Verpoorte R. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv. 2005;23:283?33. https://doi.org/10.1016/j.biotechadv.2005.01.003

Yoshida K, Kawachi M, Mori M, Maeshima M, Kondo M, Nishimura M, Kondo T. The involvement of tonoplast proton pumps and Na+(K+)/H+ exchangers in the change of petal colour during flower opening of Morning Glory, Ipomea tricolor cv. Heavenly Blue. Plant Cell Physiol. 2005;46: 407-15. https://doi.org/10.1093/pcp/pci057

Leigh RA, Wyn Jones RG. A hypothesis relating critical potassium concentrations for growth to the distributions and functions of this ion in the plant cell. New Phytol. 1984;97: 1–13. https://doi.org/10.1111/j.1469-8137.1984.tb04103.x

Pardo JM, Cubero B, Leidi EO, Quintero F. Alkali cation exchangers: roles in cellular homeostasis and stress tolerance. J Exp Bot. 2006;57:1181-99. https://doi.org/10.1093/jxb/erj114

Glenn E, Brown JJ, Blumwald E. Salt-tolerant mechanisms and crop potential of halophytes. Crit Rev Plant Sci. 1999;18:227–255. https://doi.org/10.1080/07352689991309207

Leidi EO, Barragán V, Rubio L, El?Hamdaoui A, Ruiz MT, Cubero B, Fernández JA, Bressan RA, Hasegawa PM, Quintero F. The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant. 2010;J61:495-06.

Published

30-03-2024 — Updated on 30-05-2024

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1.
Maach M, Akodad M, Pilar Rodríguez-Rosal M, Venema K, Skalli A, Ait Hmeid H, El haddaji H, Gueddari H, Baghour M. Strategies of NHX antiporters to deal with salt stress. Plant Sci. Today [Internet]. 2024 May 30 [cited 2024 Jul. 3];10(sp2). Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/2442

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