Salt Stress and tolerance mechanisms by plants: A Review
Subject Areas : Stress Physiology
REYAZ MIR
1
,
Ramamurthy Somasundaram
2
1 - Department of Botany, Annamalai University, Annamalai Nagar-608 002, Tamil Nadu, India
2 - Department of Botany, Annamalai University, Annamalai Nagar-608 002, Tamil Nadu, India
Keywords: Salt stress, antioxidants, ROS, osmolytes, Organelle stress,
Abstract :
Saline stress has remained a hot and threatened topic towards population explosion due to shrinkage of agricultural land. Soil salinity being a natural process, is further worsening by anthropogenic activities. The result is decline in plant growth performance and crop productivity. In the present review we have discussed the negative impact of NaCl stress and its action in plants by enhancing ROS formation. Further, their quenching by various physiological and biochemical activities triggered by plants are also presented in the review. Because, sodium chloride represents a wide spread salt, responsible for plant stress. Moreover, increasing antioxidants, compatible solutes and ion homeostasis helps in tolerant as well as sensitive plants to overcome stress. But among different species range of tolerance persists over a specific time and depends upon genotype of species. Furthermore, besides the role of antioxidants and osmolytes, role of various organelles during stress is also discussed. In conclusion, understanding their mechanism at various levels may help to get plants with a range of tolerance at different growth stages, when subject to salt stress. So, increasing crop productivity might replenishes the need of food scarcity over population burst in future.
Abdelaal, K.A., Y.M. Hafez, M.M. El-Afry, D.S. Tantawy, and T. Alshaal. 2018. Effect of some osmoregulators on photosynthesis, lipid peroxidation, antioxidative capacity, and productivity of barley (Hordeum vulgare L.) under water deficit stress. Environmental Science and Pollution Research. 25:30199-30211.
Abdelaziz, M.N., T.D. Xuan, A.M.M. Mekawy, H. Wang, and T.D. Khanh. 2018. Relationship of salinity tolerance to Na+ exclusion, proline accumulation, and antioxidant enzyme activity in rice seedlings. Agriculture. 8:166.
Aldesuquy, H., Z. Baka, and B. Mickky. 2014. Kinetin and spermine mediated induction of salt tolerance in wheat plants: Leaf area, photosynthesis and chloroplast ultrastructure of flag leaf at ear emergence. Egyptian Journal of Basic and Applied Sciences. 1:77-87.
Alscher, R.G., N. Erturk, and L.S. Heath. 2002. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of experimental botany. 53:1331-1341.
Annunziata, M.G., L.F. Ciarmiello, P. Woodrow, E. Dell’Aversana, and P. Carillo. 2019. Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses. Frontiers in plant science. 10:230.
Asada, K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual review of plant biology. 50:601-639.
Ashraf, M., and M.R. Foolad. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and experimental botany. 59:206-216.
Ashraf, M., S.M. Shahzad, M. Imtiaz, and M.S. Rizwan. 2018. Salinity effects on nitrogen metabolism in plants–focusing on the activities of nitrogen metabolizing enzymes: A review. Journal of Plant Nutrition. 41:1065-1081.
Baath, G.S., M.K. Shukla, P.W. Bosland, R.L. Steiner, and S.J. Walker. 2017. Irrigation water salinity influences at various growth stages of Capsicum annuum. Agricultural water management. 179:246-253.
Barupal, T., M. Meena, and K. Sharma. 2019. Inhibitory effects of leaf extract of Lawsonia inermis on Curvularia lunata and characterization of novel inhibitory compounds by GC–MS analysis. Biotechnology Reports. 23:e00335.
Blumwald, E., G.S. Aharon, and M.P. Apse. 2000. Sodium transport in plant cells. Biochimica et Biophysica Acta (BBA)-Biomembranes. 1465:140-151.
Bose, J., R. Munns, S. Shabala, M. Gilliham, B. Pogson, and S.D. Tyerman. 2017. Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes. Journal of Experimental Botany. 68:3129-3143.
Bulgari, R., A. Trivellini, and A. Ferrante. 2019. Effects of two doses of organic extract-based biostimulant on greenhouse lettuce grown under increasing NaCl concentrations. Frontiers in plant science. 9:1870.
Byrt, C.S., B. Xu, M. Krishnan, D.J. Lightfoot, A. Athman, A.K. Jacobs, N.S. Watson‐Haigh, D. Plett, R. Munns, and M. Tester. 2014. The Na+ transporter, Ta hkt 1; 5‐d, limits shoot na+ accumulation in bread wheat. The Plant Journal. 80:516-526.
Carmen, B., and D. Roberto. 2011. Soil bacteria support and protect plants against abiotic stresses. Abiotic stress in plants-Mechanisms and daptations, Italy:143-170.
Chartzoulakis, K., and G. Klapaki. 2000. Response of two greenhouse pepper hybrids to NaCl salinity during different growth stages. Scientia horticulturae. 86:247-260.
Chen, T.H., and N. Murata. 2002. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Current opinion in plant biology. 5:250-257.
Chen, T.H., and N. Murata. 2008. Glycinebetaine: an effective protectant against abiotic stress in plants. Trends in plant science. 13:499-505.
Cherlet, M., C. Hutchinson, J. Reynolds, J. Hill, S. Sommer, and M.G. VON. 2018. World atlas of desertification.
Chinnusamy, V., A. Jagendorf, and J.K. Zhu. 2005. Understanding and improving salt tolerance in plants. Crop science. 45:437-448.
Chu, P., G.X. Yan, Q. Yang, L.N. Zhai, C. Zhang, F.Q. Zhang, and R.Z. Guan. 2015. iTRAQ-based quantitative proteomics analysis of Brassica napus leaves reveals pathways associated with chlorophyll deficiency. Journal of proteomics. 113:244-259.
Cramer, G.R., and D.C. Bowman. 1993. Cell elongation control under stress conditions. Handbook of Plant and Crop Stress, M Pessarakli (Ed.). Marcel Dekker, New York:303-319.
de Dios Barajas-López J., N.E. Blanco, and Å. Strand. 2013. Plastid-to-nucleus communication, signals controlling the running of the plant cell. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research. 1833:425-437.
del Río, L.A., F.J. Corpas, E. López-Huertas, and J.M. Palma. 2018. Plant superoxide dismutases: Function under abiotic stress conditions. Antioxidants and antioxidant enzymes in higher plants:1-26.
Dellero, Y., M. Jossier, J. Schmitz, V.G. Maurino, and M. Hodges. 2016. Photorespiratory glycolate–glyoxylate metabolism. Journal of Experimental Botany. 67:3041-3052.
Demidchik, V., D. Straltsova, S.S. Medvedev, G.A. Pozhvanov, A. Sokolik, and V. Yurin. 2014. Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of experimental botany. 65:1259-1270.
Desoky, E.-S.M., A.I. ElSayed, A.-R.M. Merwad, and M.M. Rady. 2019a. Stimulating antioxidant defenses, antioxidant gene expression, and salt tolerance in Pisum sativum seedling by pretreatment using licorice root extract (LRE) as an organic biostimulant. Plant physiology and biochemistry. 142:292-302.
Desoky, E., S. Ibrahim, and A. Merwad. 2019b. Mitigation of salinity stress effects on growth, physio-chemical parameters and yield of snapbean (Phaseolus vulgaris L.) by exogenous application of glycine betaine. International Letters of Natural Sciences. 76:60-71.
Dietz, K.-J., N. Tavakoli, C. Kluge, T. Mimura, S. Sharma, G. Harris, A. Chardonnens, and D. Golldack. 2001. Significance of the V‐type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. Journal of experimental botany. 52:1969-1980.
El-Ramady, H., T. Alshaal, N. Elhawat, A. Ghazi, T. Elsakhawy, A.E.-D. Omara, S. El-Nahrawy, M. Elmahrouk, N. Abdalla, and É. Domokos-Szabolcsy. 2018. Plant nutrients and their roles under saline soil conditions. Plant nutrients and abiotic stress tolerance:297-324.
El-Ramady, H., T. Alshaal, T. Elsakhawy, A.E.-D. Omara, N. Abdalla, and E.C. Brevik. 2019. Soils and humans. The soils of Egypt:201-213.
Endler, A., C. Kesten, R. Schneider, Y. Zhang, A. Ivakov, A. Froehlich, N. Funke, and S. Persson. 2015. A mechanism for sustained cellulose synthesis during salt stress. Cell. 162:1353-1364.
Eyidogan, F., and M.T. Öz. 2007. Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiologiae Plantarum. 29:485-493.
Farhangi-Abriz, S., and S. Torabian. 2017. Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotoxicology and environmental safety. 137:64-70.
Farooq, A., S.A. Bukhari, N.A. Akram, M. Ashraf, L. Wijaya, M.N. Alyemeni, and P. Ahmad. 2020. Exogenously applied ascorbic acid-mediated changes in osmoprotection and oxidative defense system enhanced water stress tolerance in different cultivars of safflower (Carthamus tinctorious L.). Plants. 9:104.
Farooq, M., M. Hussain, A. Wakeel, and K.H. Siddique. 2015. Salt stress in maize: effects, resistance mechanisms, and management. A review. Agronomy for Sustainable Development. 35:461-481.
Feng, Z., Y. Deng, H. Fan, Q. Sun, N. Sui, and B. Wang. 2014. Effects of NaCl stress on the growth and photosynthetic characteristics of Ulmus pumila L. seedlings in sand culture. Photosynthetica. 52:313-320.
Flowers, T.J., P.M. Gaur, C.L. Gowda, L. Krishnamurthy, S. Samineni, K.H. Siddique, N.C. Turner, V. Vadez, R.K. Varshney, and T.D. Colmer. 2010. Salt sensitivity in chickpea. Plant, Cell & Environment. 4:490-509.
Flowers, T.J., R. Munns, and T.D. Colmer. 2015. Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Annals of botany. 115:419-431.
Flügel, F., S. Timm, S. Arrivault, A. Florian, M. Stitt, A.R. Fernie, and H. Bauwe. 2017. The photorespiratory metabolite 2-phosphoglycolate regulates photosynthesis and starch accumulation in Arabidopsis. The Plant Cell. 29:2537-2551.
Food, A. 2011. of the United Nations, and London, The State of the Worlds Land and Water Resources for Food and Agriculture (SOLAW) Managing Systems at Risk. FAO.
Frukh, A., T.O. Siddiqi, M.I.R. Khan, and A. Ahmad. 2020. Modulation in growth, biochemical attributes and proteome profile of rice cultivars under salt stress. Plant Physiology and Biochemistry. 146:55-70.
Galvez‐Valdivieso, G., and P.M. Mullineaux. 2010. The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiologia Plantarum. 138:430-439.
Gill, S.S., and N. Tuteja. 2010. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant physiology and biochemistry. 48:909-930.
Grattan, S.R., J.D. Oster, J. Letey, and S.R. Kaffka. 2014. Drainage water reuse: concepts, practices and potential crops. Salinity and Drainage in San Joaquin Valley, California: Science, Technology, and Policy:277-302.
Guo, Y., Q.-S. Qiu, F.J. Quintero, J.M. Pardo, M. Ohta, C. Zhang, K.S. Schumaker, and J.-K. Zhu. 2004. Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. The Plant Cell. 16:435-449.
Hannachi, S., and M.-C. Van Labeke. 2018. Salt stress affects germination, seedling growth and physiological responses differentially in eggplant cultivars (Solanum melongena L.). Scientia Horticulturae. 228:56-65.
Hasegawa, P.M. 2013. Sodium (Na+) homeostasis and salt tolerance of plants. Environmental and experimental botany. 92:19-31.
Hassannejad, S., R. Lotfi, S.P. Ghafarbi, A. Oukarroum, A. Abbasi, H.M. Kalaji, and A. Rastogi. 2020. Early identification of herbicide modes of action by the use of chlorophyll fluorescence measurements. Plants. 9:529.
He, J., Y. Duan, D. Hua, G. Fan, L. Wang, Y. Liu, Z. Chen, L. Han, L.-J. Qu, and Z. Gong. 2012. DEXH box RNA helicase–mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling. The Plant Cell. 24:1815-1833.
Hua, B.-G., R.W. Mercier, Q. Leng, and G.A. Berkowitz. 2003. Plants do it differently. A new basis for potassium/sodium selectivity in the pore of an ion channel. Plant Physiology. 132:1353-1361.
Iannone, M.F., M.D. Groppa, and M.P. Benavides. 2015. Cadmium induces different biochemical responses in wild type and catalase-deficient tobacco plants. Environmental and Experimental Botany. 109:201-211.
Iqbal, N., M. Fatma, N.A. Khan, and S. Umar. 2019. Regulatory role of proline in heat stress tolerance: modulation by salicylic acid. In Plant Signaling Molecules. Elsevier. 437-448.
Jendretzki, A., J. Wittland, S. Wilk, A. Straede, and J.J. Heinisch. 2011. How do I begin? Sensing extracellular stress to maintain yeast cell wall integrity. European journal of cell biology. 90:740-744.
Kalaji, H., A. Rastogi, M. Živčák, M. Brestic, A. Daszkowska-Golec, K. Sitko, K. Alsharafa, R. Lotfi, P. Stypiński, and I. Samborska. 2018. Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica. 56:953-961.
Kalaji, H.M., K. Bosa, J. Kościelniak, and K. Żuk-Gołaszewska. 2011. Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany. 73:64-72.
Kamanga, R.M., K. Echigo, K. Yodoya, A.M.M. Mekawy, and A. Ueda. 2020. Salinity acclimation ameliorates salt stress in tomato (Solanum lycopersicum L.) seedlings by triggering a cascade of physiological processes in the leaves. Scientia Horticulturae. 270:109434.
Kamanga, R.M., and L. Mndala. 2019. Crop abiotic stresses and nutrition of harvested food crops: a review of impacts, interventions and their effectiveness. African Journal of Agricultural Research. 14:118-135.
Kamran, M., K. Xie, J. Sun, D. Wang, C. Shi, Y. Lu, W. Gu, and P. Xu. 2020. Modulation of growth performance and coordinated induction of ascorbate-glutathione and methylglyoxal detoxification systems by salicylic acid mitigates salt toxicity in choysum (Brassica parachinensis L.). Ecotoxicology and environmental safety. 188:109877.
Kaur, G., and B. Asthir. 2015. Proline: a key player in plant abiotic stress tolerance. Biologia plantarum. 59:609-619.
Ke, Q., J. Ye, B. Wang, J. Ren, L. Yin, X. Deng, and S. Wang. 2018. Melatonin mitigates salt stress in wheat seedlings by modulating polyamine metabolism. Frontiers in plant science. 9:914.
Khan, H.A., K.H. Siddique, and T.D. Colmer. 2017. Vegetative and reproductive growth of salt-stressed chickpea are carbon-limited: sucrose infusion at the reproductive stage improves salt tolerance. Journal of Experimental Botany. 68:2001-2011.
Khan, M.A., I.A. Ungar, and A.M. Showalter. 2000b. Effects of salinity on growth, water relations and ion accumulation of the subtropical perennial halophyte, Atriplex griffithii var. stocksii. Annals of Botany. 85:225-232.
Khan, M.I.R., M. Fatma, T.S. Per, N.A. Anjum, and N.A. Khan. 2015. Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Frontiers in plant science. 6:462.
Khan, N.A., S. Syeed, A. Masood, R. Nazar, and N. Iqbal. 2010. Application of salicylic acid increases contents of nutrients and antioxidative metabolism in mungbean and alleviates adverse effects of salinity stress. International Journal of Plant Biology. 1:e1.
Khare, T., V. Kumar, and P.K. Kishor. 2015. Na+ and Cl− ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma. 252:1149-1165.
Kono, Y., and I. Fridovich. 1982. Superoxide radical inhibits catalase. Journal of biological chemistry. 257:5751-5754.
Kushwaha, B.K., S. Singh, D.K. Tripathi, S. Sharma, S.M. Prasad, D.K. Chauhan, V. Kumar, and V.P. Singh. 2019. New adventitious root formation and primary root biomass accumulation are regulated by nitric oxide and reactive oxygen species in rice seedlings under arsenate stress. Journal of hazardous materials. 361:134-140.
Lakra, N., C. Kaur, K. Anwar, S.L. Singla‐Pareek, and A. Pareek. 2018. Proteomics of contrasting rice genotypes: identification of potential targets for raising crops for saline environment. Plant, cell & environment. 41:947-969.
Läuchli, A., and E. Epstein. 1990. Plant responses to saline and sodic conditions. Agricultural salinity assessment and management. 71:113-137.
Liebthal, M., D. Maynard, and K.-J. Dietz. 2018. Peroxiredoxins and redox signaling in plants. Antioxidants & redox signaling. 28:609-624.
Liu, J., M. Ishitani, U. Halfter, C.-S. Kim, and J.-K. Zhu. 2000. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proceedings of the national academy of sciences. 97:3730-3734.
Liu, J.X., and S.H. Howell. 2016. Managing the protein folding demands in the endoplasmic reticulum of plants. New Phytologist. 211:418-428.
Liu, L., Y. Wang, N. Wang, Y.Y. Dong, X.D. Fan, X.M. Liu, J. Yang, and H.Y. Li. 2011. Cloning of a vacuolar H+‐pyrophosphatase gene from the halophyte Suaeda corniculata whose heterologous overexpression improves salt, saline‐alkali and drought tolerance in Arabidopsis. Journal of integrative plant biology. 53:731-742.
Maas, E.V., and S. Grattan. 1999. Crop yields as affected by salinity. Agricultural drainage. 38:55-108.
Maksimović, J.D., J. Zhang, F. Zeng, B.D. Živanović, L. Shabala, M. Zhou, and S. Shabala. 2013. Linking oxidative and salinity stress tolerance in barley: can root antioxidant enzyme activity be used as a measure of stress tolerance? Plant and Soil. 365:141-155.
Malekzadeh, P. 2015. Influence of exogenous application of glycinebetaine on antioxidative system and growth of salt-stressed soybean seedlings (Glycine max L.). Physiology and Molecular biology of Plants. 21:225-232.
Mansour, M.M.F., and E.F. Ali. 2017. Glycinebetaine in saline conditions: an assessment of the current state of knowledge. Acta Physiologiae Plantarum. 39:1-17.
Mbarki, S., O. Sytar, A. Cerda, M. Zivcak, A. Rastogi, X. He, A. Zoghlami, C. Abdelly, and M. Brestic. 2018. Strategies to mitigate the salt stress effects on photosynthetic apparatus and productivity of crop plants. Salinity Responses and Tolerance in Plants, Volume 1: Targeting Sensory, Transport and Signaling Mechanisms:85-136.
McCord, J.M., and I. Fridovich. 1969. Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). Journal of Biological chemistry. 244:6049-6055.
Meena, M., K. Divyanshu, S. Kumar, P. Swapnil, A. Zehra, V. Shukla, M. Yadav, and R. Upadhyay. 2019. Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon. 5:e02952.
Mehta, P., A. Jajoo, S. Mathur, and S. Bharti. 2010. Chlorophyll a fluorescence study revealing effects of high salt stress on Photosystem II in wheat leaves. Plant physiology and biochemistry. 48:16-20.
Mekawy, A.M.M., D.V. Assaha, and A. Ueda. 2020. Differential salt sensitivity of two flax cultivars coincides with differential sodium accumulation, biosynthesis of osmolytes and antioxidant enzyme activities. Journal of Plant Growth Regulation. 39:1119-1126.
Meloni, D.A., M.R. Gulotta, C.A. Martínez, and M.A. Oliva. 2004. The effects of salt stress on growth, nitrate reduction and proline and glycinebetaine accumulation in Prosopis alba. Brazilian Journal of Plant Physiology. 16:39-46.
Mignolet-Spruyt, L., E. Xu, N. Idänheimo, F.A. Hoeberichts, P. Mühlenbock, M. Brosché, F. Van Breusegem, and J. Kangasjärvi. 2016. Spreading the news: subcellular and organellar reactive oxygen species production and signalling. Journal of experimental botany. 67:3831-3844.
Mir, R.A., and R. Somasundaram. 2020. Effect of NaCl stress on pigment composition, membrane integrity and proline metabolism of little millet (Panicum sumatrense L.) CO-4 variety. International Journal of Botany Studies,. 5:586-593.
Mir, R.A., R. Somasundaram, and R. Panneerselvam. 2019. Changes in antioxidant enzymes activities mitigates deleterious effects of ROS in Panicum miliaceum (L.) under drought stress. Journal of Stress Physiology & Biochemistry. 15:81-91.
Mittler, R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in plant science. 7:405-410.
Mittler, R. 2017. ROS are good. Trends in plant science. 22:11-19.
Munns, R. 1993. Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant, Cell & Environment. 16:15-24.
Munns, R., and A. Termaat. 1986. Whole-plant responses to salinity. Functional Plant Biology. 13:143-160.
Munns, R., and M. Tester. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59:651-681.
Nahar, K., M. Hasanuzzaman, A. Rahman, M.M. Alam, J.-A. Mahmud, T. Suzuki, and M. Fujita. 2016. Polyamines confer salt tolerance in mung bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems. Frontiers in Plant Science. 7:1104.
Negrão, S., S. Schmöckel, and M. Tester. 2017. Evaluating physiological responses of plants to salinity stress. Annals of botany. 119:1-11.
Ng, S., I. De Clercq, O. Van Aken, S.R. Law, A. Ivanova, P. Willems, E. Giraud, F. Van Breusegem, and J. Whelan. 2014. Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. Molecular plant. 7:1075-1093.
Noctor, G., and C.H. Foyer. 1998. A re-evaluation of the ATP: NADPH budget during C3 photosynthesis: a contribution from nitrate assimilation and its associated respiratory activity? Journal of Experimental Botany. 49:1895-1908.
Papageorgiou, G.C., and N. Murata. 1995. The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynthesis Research. 44:243-252.
Parihar, P., S. Singh, R. Singh, V.P. Singh, and S.M. Prasad. 2015. Effect of salinity stress on plants and its tolerance strategies: a review. Environmental science and pollution research. 22:4056-4075.
Ramel, F., S. Birtic, C. Ginies, L. Soubigou-Taconnat, C. Triantaphylidès, and M. Havaux. 2012. Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proceedings of the National Academy of Sciences. 109:5535-5540.
Raven, J. 1985. Regulation of pH and generation of osmolarity in vascular plants: a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytol. 101:25-77.
Rhodes, D., and A. Hanson. 1993. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annual review of plant biology. 44:357-384.
Roy, S.J., S. Negrão, and M. Tester. 2014. Salt resistant crop plants. Current opinion in Biotechnology. 26:115-124.
Rubio, F., M. Nieves‐Cordones, T. Horie, and S. Shabala. 2020. Doing ‘business as usual’comes with a cost: evaluating energy cost of maintaining plant intracellular K+ homeostasis under saline conditions. New Phytologist. 225:1097-1104.
Russell, N., R. Evans, P. Ter Steeg, J. Hellemons, A. Verheul, and T. Abee. 1995. Membranes as a target for stress adaptation. International journal of food microbiology. 28:255-261.
Sadak, M., M. El-Enany, B. Bakry, M. Abdallah, and H. El-Bassiouny. 2020. Signal molecules improving growth, yield and biochemical aspects of wheat cultivars under water stress. Asian J Plant Sci. 19:35-53.
Sameena, P., and J.T. Puthur. 2021. Exogenous application of cytokinins confers copper stress tolerance in Ricinus communis L. seedlings. Journal of Plant Growth Regulation:1-15.
Schroeder, J.I., E. Delhaize, W.B. Frommer, M.L. Guerinot, M.J. Harrison, L. Herrera-Estrella, T. Horie, L.V. Kochian, R. Munns, and N.K. Nishizawa. 2013. Using membrane transporters to improve crops for sustainable food production. Nature. 497:60-66.
Schubert, S. 2011. Salt resistance of crop plants: physiological characterization of a multigenic trait. The molecular and physiological basis of nutrient use efficiency in crops:443-455.
SEMİZ, G., A. Ünlükara, E. Yurtseven, D. Suarez, and I. Telci. 2012. Salinity impact on yield, water use, mineral and essential oil content of fennel (Foeniculum vulgare Mill.). Journal of Agricultural Sciences. 18:177-186.
Shao, Y., F. Xu, Y. Chen, Y. Huang, T. Beta, and J. Bao. 2015. Analysis of genotype, environment, and their interaction effects on the phytochemicals and antioxidant capacities of red rice (Oryza sativa L.). Cereal Chemistry. 92:204-210.
Sharma, D., and A. Singh. 2015. Salinity research in India-achievements, challenges and future prospects.
Sharma, P., A.B. Jha, R.S. Dubey, and M. Pessarakli. 2012. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of botany. 2012.
Shi, H., M. Ishitani, C. Kim, and J.-K. Zhu. 2000. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the national academy of sciences. 97:6896-6901.
Shrivastava, P., and R. Kumar. 2015. Soil salinity: A serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi journal of biological sciences. 22:123-131.
Soares, C., S. Branco-Neves, A. de Sousa, M. Azenha, A. Cunha, R. Pereira, and F. Fidalgo. 2018. SiO2 nanomaterial as a tool to improve Hordeum vulgare L. tolerance to nano-NiO stress. Science of the Total Environment. 622:517-525.
Sofy, M.R., N. Elhawat, and T. Alshaal. 2020. Glycine betaine counters salinity stress by maintaining high K+/Na+ ratio and antioxidant defense via limiting Na+ uptake in common bean (Phaseolus vulgaris L.). Ecotoxicology and Environmental Safety. 200:110732.
Talon, M., M. Caruso, and F.G. Gmitter jr. 2020. The Genus Citrus. Woodhead Publishing.
Tenhaken, R. 2015. Cell wall remodeling under abiotic stress. Frontiers in plant science. 5:771.
Thiel, G., J. Lynch, and A. Läuchli. 1988. Short-term effects of salinity stress on the turgor and elongation of growing barley leaves. Journal of Plant Physiology. 132:38-44.
Tian, F., W. Wang, C. Liang, X. Wang, G. Wang, and W. Wang. 2017. Overaccumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. The Crop Journal. 5:73-82.
Vakilian, K.A., and J. Massah. 2017. A farmer-assistant robot for nitrogen fertilizing management of greenhouse crops. Computers and electronics in agriculture. 139:153-163.
Verslues, P.E., and S. Sharma. 2010. Proline metabolism and its implications for plant-environment interaction. The Arabidopsis Book/American Society of Plant Biologists. 8.
Wagner, D., D. Przybyla, R. op den Camp, C. Kim, F. Landgraf, K.P. Lee, M. Wursch, C. Laloi, M. Nater, and E. Hideg. 2004. The genetic basis of singlet oxygen induced stress responses of Arabidopsis thaliana. Science. 306:1183-1185.
Walter, P., and D. Ron. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. science. 334:1081-1086.
Wang, N., H. Qi, G. Su, J. Yang, H. Zhou, Q. Xu, Q. Huang, and G. Yan. 2016. Genotypic variations in ion homeostasis, photochemical efficiency and antioxidant capacity adjustment to salinity in cotton (Gossypium hirsutum L.). Soil Science and Plant Nutrition. 62:240-246.
Wang, Y., Y. Ying, J. Chen, and X. Wang. 2004. Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Science. 167:671-677.
Wani, S.H., S.N. Brajendra, Haribhushan Athokpam., and Iqbal Mir Javed. 2013. Compatible solute engineering in plants for abiotic stress tolerance-role of glycine betaine. Current genomics. 14:157-165.
Williams, W.P. 1994. The role of lipids in the structure and function of photosynthetic membranes. Progress in lipid research. 33:119-127.
Wu, L., Z. Fan, L. Guo, Y. Li, Z.-L. Chen, and L.-J. Qu. 2005. Over-expression of the bacterial nhaA gene in rice enhances salt and drought tolerance. Plant Science. 168:297-302.
Yousuf, P.Y., A. Ahmad, A.H. Ganie, O. Sareer, V. Krishnapriya, I.M. Aref, and M. Iqbal. 2017. Antioxidant response and proteomic modulations in Indian mustard grown under salt stress. Plant growth regulation. 81:31-50.
Yu, B.-j., H.-m. Lam, G.-h. Shao, and Y.-l. Liu. 2005. Effects of salinity on activities of H^+-ATPase, H^+-PPase and membrane lipid composition in plasma membrane and tonoplast vesicles isolated from soybean (Glycine max L.) seedlings. Journal of Environmental Sciences. 17:259-262.
Zhao, C., O. Zayed, Z. Yu, W. Jiang, P. Zhu, C.-C. Hsu, L. Zhang, W.A. Tao, R. Lozano-Durán, and J.-K. Zhu. 2018. Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proceedings of the National Academy of Sciences. 115:13123-13128.
Zhao, C., H. Zhang, C. Song, J.-K. Zhu, and S. Shabala. 2020. Mechanisms of plant responses and adaptation to soil salinity. The innovation. 1:100017.
Zhu, J.-K. 2003. Regulation of ion homeostasis under salt stress. Current opinion in plant biology. 6:441-445.