Understanding the roles of osmolytes for acclimatizing plants to changing environment: a review of potential mechanism

References

• Mittler R, Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol. 2010;1–13.
   PubMed Web of Science ®Google Scholar
• Surabhi G-K. Update in root proteomics with special reference to abiotic stresses: achievements and challenges. J Proteins Proteomics. 2018;9:31–35.
   Google Scholar
• Ali S, Eum H-I, Cho J et al. Assessment of climate extremes in future projections downscaled by multiple statistical downscaling methods over Pakistan. Atmos Res. 2019;222:114–133.
   Web of Science ®Google Scholar
• Boyer JS. Plant Productivity and Environment. Science. 1982;218(4571):443–448. doi:https://doi.org/10.1126/science.218.4571.443.
   PubMed Web of Science ®Google Scholar
• Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012;63(10):3523–3543. doi:https://doi.org/10.1093/jxb/ers100.
   PubMed Web of Science ®Google Scholar
• Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R. Abiotic and biotic stress combinations. New Phytol. 2014;203(1):32–43. doi:https://doi.org/10.1111/nph.12797.
   PubMed Web of Science ®Google Scholar
• Singh S, Srivastava PK, Kumar D, Tripathi DK, Chauhan DK, Prasad SM. Morpho-anatomical and biochemical adapting strategies of maize (Zea mays L.) seedlings against lead and chromium stresses. Biocatal Agric Biotechnol. 2015;4(3):286–295. doi:https://doi.org/10.1016/j.bcab.2015.03.004.
   Web of Science ®Google Scholar
• Zhu J-K. Abiotic Stress Signaling and Responses in Plants. Cell. 2016;167(2):313–324. doi:https://doi.org/10.1016/j.cell.2016.08.029.
   PubMed Web of Science ®Google Scholar
• Jeandroz S, Lamotte O. Editorial: plant Responses to Biotic and Abiotic Stresses: lessons from Cell Signaling. Front Plant Sci. 2017;8:81772. doi:https://doi.org/10.3389/fpls.2017.01772.
   Web of Science ®Google Scholar
• Tripathi DK, Singh S, Singh S, Chauhan DK, Dubey NK, Prasad R. Silicon as a beneficial element to combat the adverse effect of drought in agricultural crops. Water Stress and Crop Plants. West Sussex, UK: John Wiley & Sons, Ltd; 2016. p.682–694. https://:10.1002/9781119054450.ch39
   Google Scholar
• Tripathi A, Tripathi DK, Chauhan DK, Kumar N. Chromium (VI)-induced phytotoxicity in river catchment agriculture: evidence from physiological, biochemical and anatomical alterations in Cucumis sativus(L.) used as model species. Chem Ecol. 2016;32(1):12–33. doi:https://doi.org/10.1080/02757540.2015.1115841.
   Web of Science ®Google Scholar
• Tripathi A, Liu S, Singh PK, et al. Differential phytotoxic responses of silver nitrate (AgNO3) and silver nanoparticle (AgNps) in Cucumis sativus L. Plant Gene. 2017;11255–11264. doi:https://doi.org/10.1016/j.plgene.2017.07.005.
   Google Scholar
• Tripathi DK, Shweta SS, Yadav V. Silicon: a potential element to combat adverse impact of UV‐B in plants. UV-B radiation: from environmental stressor to regulator of plant growth. 2017;1:175–195.
   Google Scholar
• Cheng C, Pei L, Yin T, Zhang K. Seed treatment with glycine betaine enhances tolerance of cotton to chilling stress. J Agric Sci. 2018;156(3):323–332. doi:https://doi.org/10.1017/S0021859618000278.
   Web of Science ®Google Scholar
• Choudhary V, Chander S, Chethan C, Kumar B, Hasanuzzaman M, Fujita M, et al. Effect of seed priming on abiotic stress tolerance in plants. Plant Tolerance Environ Stress Role Phytoprotectants. 2019;29–46.
   Google Scholar
• Dutta T, Neelapu NR, Wani SH, Challa S. Compatible solute engineering of crop plants for improved tolerance toward abiotic stresses. Biochemical, physiological and molecular avenues for combating abiotic stress tolerance in plants: UK: Elsevier; 2018. p. 221–254.
   Google Scholar
• Khan MIR, Reddy PS, Ferrante A, Khan NA. Plant signaling molecules: role and regulation under stressful environments. Woodhead Publishing; 2019.
   Google Scholar
• Arif N, Yadav V, Singh S et al. Assessment of Antioxidant Potential of Plants in Response to Heavy Metals. Plant Responses to Xenobiotics: Springer Singapore; 2016. p. 97–125. https://:10.1007/978-981-10-2860-1_5
   Google Scholar
• Arif N, Yadav V, Singh S, Singh S, Ahmad P, Mishra RK, Mishra RK. Influence of High and Low Levels of Plant-Beneficial Heavy Metal Ions on Plant Growth and Development. Frontiers Environ Sci. 2016;4:4. doi:https://doi.org/10.3389/fenvs.2016.00069.
   Web of Science ®Google Scholar
• Singh S, Tripathi DK, Singh S, et al. Toxicity of aluminium on various levels of plant cells and organism: a review. Environ Exp Bot. 2017;137177–137193. doi:https://doi.org/10.1016/j.envexpbot.2017.01.005.
   Google Scholar
• Bohnert HJ, Jensen RG. Strategies for engineering water-stress tolerance in plants. Trends Biotechnol. 1996;14(3):89–97. doi:https://doi.org/10.1016/0167-7799(96)80929-2.
   Web of Science ®Google Scholar
• Kuznetsov VV, Rakitin VYU, Zholkevich VN. Effects of preliminary heat-shock treatment on accumulation of osmolytes and drought resistance in cotton plants during water deficiency. Physiol Plant. 1999;107(4):399–406. doi:https://doi.org/10.1034/j.1399-3054.1999.100405.x.
   Web of Science ®Google Scholar
• Parvanova D, Ivanov S, Konstantinova T, Karanov E, Atanassov A, Tsvetkov T, Alexieva V, Djilianov D. Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. Plant Physiol Biochem. 2004;42(1):57–63. doi:https://doi.org/10.1016/j.plaphy.2003.10.007.
   PubMed Web of Science ®Google Scholar
• Yancey PH. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol. 2005;208(15):2819–2830. doi:https://doi.org/10.1242/jeb.01730.
   PubMed Web of Science ®Google Scholar
• Sharma SS, Dietz K-J. The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot. 2006;57(4):711–726. doi:https://doi.org/10.1093/jxb/erj073.
   PubMed Web of Science ®Google Scholar
• Burg MB, Ferraris JD. Intracellular organic osmolytes: function and regulation. J Biol Chem. 2008;283(12):7309–7313. doi:https://doi.org/10.1074/jbc.R700042200.
   PubMed Web of Science ®Google Scholar
• Ashraf M, Harris PJC. Potential biochemical indicators of salinity tolerance in plants. Plant Sci. 2004;166(1):3–16. doi:https://doi.org/10.1016/j.plantsci.2003.10.024.
   Web of Science ®Google Scholar
• Ashraf M, Foolad MR. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot. 2007;59(2):206–216. doi:https://doi.org/10.1016/j.envexpbot.2005.12.006.
   Web of Science ®Google Scholar
• Chen H, Jiang J-G. Osmotic adjustment and plant adaptation to environmental changes related to drought and salinity. Environl Rev. 2010;18(NA):309–319. doi:https://doi.org/10.1139/a10-014.
   Google Scholar
• Liang X, Zhang L, Natarajan SK, Becker DF. Proline mechanisms of stress survival. Antioxid Redox Signal. 2013;19(9):998–1011. doi:https://doi.org/10.1089/ars.2012.5074.
   PubMed Web of Science ®Google Scholar
• Flowers TJ, Colmer TD. Salinity tolerance in halophytes*. New Phytol. 2008;179(4):945–963. doi:https://doi.org/10.1111/j.1469-8137.2008.02531.x.
   PubMed Web of Science ®Google Scholar
• Türkan I, Demiral T. Recent developments in understanding salinity tolerance. Environ Exp Bot. 2009;67(1):2–9. doi:https://doi.org/10.1016/j.envexpbot.2009.05.008.
   Web of Science ®Google Scholar
• Roychoudhury A, Chakraborty M. Biochemical and molecular basis of varietal difference in plant salt tolerance. Annu Res Rev Biol. 2013;422–454.
   Google Scholar
• Roychoudhury A, Das K. Functional role of polyamines and polyamine-metabolizing enzymes during salinity, drought and cold stresses. In: Plant Adaptation to Environmental Change: significance of Amino Acids And Their Derivatives. Wallingford (UK): CAB International Publishers; 2014. p. 141–156.
   Google Scholar
• Roychoudhury A, Banerjee A. Endogenous glycine betaine accumulation mediates abiotic stress tolerance in plants. Trop Plant Res. 2016;3:105–111.
   Google Scholar
• Hussain TM, Hazara M, Sultan Z, Saleh BK, Gopal GR. Recent advances in salt stress biology a review. Biotechnol Mol Biol Rev. 2008;3:8–13.
   Google Scholar
• Khan SH, Ahmad N, Ahmad F, Kumar R. Naturally occurring organic osmolytes: from cell physiology to disease prevention. IUBMB Life. 2010;62(12):891–895. doi:https://doi.org/10.1002/iub.406.
   PubMed Web of Science ®Google Scholar
• Groppa M, Benavides M. Polyamines and abiotic stress: recent advances. Amino Acids. 2008;34(1):35. doi:https://doi.org/10.1007/s00726-007-0501-8.
   PubMed Web of Science ®Google Scholar
• Munns R, Tester M. Mechanisms of Salinity Tolerance. Annu Rev Plant Biol. 2008;59(1):651–681. doi:https://doi.org/10.1146/annurev.arplant.59.032607.092911.
   PubMed Web of Science ®Google Scholar
• Beebe S, Ramirez J, Jarvis A, Rao IM, Mosquera G, Bueno JM, et al. Genetic improvement of common beans and the challenges of climate change. Crop Adapt Clim Change. 2011;356–369.
   Google Scholar
• Khater M, Dawood MG, Sadak MS, Shalaby M, El-Awadi M, El-Din KG. Enhancement the performance of cowpea plants grown under drought conditions via trehalose application. Middle East J Agric Res. 2018;7:782–800.
   Google Scholar
• Bekka S, Abrous-belbachir O, Djebbar R. Effects of exogenous proline on the physiological characteristics of Triticum aestivum L. and Lens culinaris Medik. under drought stress. Acta agriculturae Slovenica. 2018;111(2):477–491. doi:https://doi.org/10.14720/aas.2018.111.2.20.
   Google Scholar
• Priya M, Sharma L, Kaur R, Bindumadhava H, Nair RM, Siddique K, Nayyar H. GABA (γ-aminobutyric acid), as a thermo-protectant, to improve the reproductive function of heat-stressed mungbean plants. Sci Rep. 2019;9(1):1–14. doi:https://doi.org/10.1038/s41598-019-44163-w.
   PubMedGoogle Scholar
• Patel N, Gantait S, Panigrahi J. Extension of postharvest shelf-life in green bell pepper (Capsicum annuum L.) using exogenous application of polyamines (spermidine and putrescine). Food Chem. 2019;275:681–687.
   PubMed Web of Science ®Google Scholar
• Wu X, Jia Q, Ji S, Gong B, Li J, Lü G, Gao H. Gamma-aminobutyric acid (GABA) alleviates salt damage in tomato by modulating Na+ uptake, the GAD gene, amino acid synthesis and reactive oxygen species metabolism. BMC Plant Biol. 2020;20(1):1–21. doi:https://doi.org/10.1186/s12870-020-02669-w.
   PubMed Web of Science ®Google Scholar
• Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K. Regulation of Levels of Proline as an Osmolyte in Plants under Water Stress. Plant Cell Physiol. 1997;38(10):1095–1102. doi:https://doi.org/10.1093/oxfordjournals.pcp.a029093.
   PubMed Web of Science ®Google Scholar
• Hare PD, Cress WA, Van Staden J. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 1998;21(6):535–553. doi:https://doi.org/10.1046/j.1365-3040.1998.00309.x.
   Web of Science ®Google Scholar
• Karakas B, Ozias-Akins P, Stushnoff C, Suefferheld M, Rieger M. Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant Cell Environ. 1997;20(5):609–616. doi:https://doi.org/10.1111/j.1365-3040.1997.00132.x.
   Web of Science ®Google Scholar
• Giri J. Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav. 2011;6(11):1746–1751. doi:https://doi.org/10.4161/psb.6.11.17801.
   PubMedGoogle Scholar
• Kishor PBK, Hong Z, Miao GH, Hu CAA, Verma DPS. Overexpression of [delta]-Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants. Plant Physiol. 1995;108(4):1387–1394. doi:https://doi.org/10.1104/pp.108.4.1387.
   PubMed Web of Science ®Google Scholar
• Shen B, Jensen RG, Bohnert HJ. Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiol. 1997;113(4):1177–1183. doi:https://doi.org/10.1104/pp.113.4.1177.
   PubMed Web of Science ®Google Scholar
• Sakamoto A, Murata N. The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ. 2002;25(2):163–171. doi:https://doi.org/10.1046/j.0016-8025.2001.00790.x.
   PubMed Web of Science ®Google Scholar
• Yang Q, Chen -Z-Z, Zhou X-F, Yin H-B, Li X, Xin X-F, Hong X-H, Zhu J-K, Gong Z. Overexpression of SOS (Salt Overly Sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant. 2009;2(1):22–31. doi:https://doi.org/10.1093/mp/ssn058.
   PubMed Web of Science ®Google Scholar
• Zhu J-K. Plant salt tolerance. Trends Plant Sci. 2001;6(2):66–71. doi:https://doi.org/10.1016/s1360-1385(00)01838-0.
   PubMed Web of Science ®Google Scholar
• Munns R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002;25(2):239–250. doi:https://doi.org/10.1046/j.0016-8025.2001.00808.x.
   PubMed Web of Science ®Google Scholar
• Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol. 2005;16(2):123–132. doi:https://doi.org/10.1016/j.copbio.2005.02.001.
   PubMed Web of Science ®Google Scholar
• Jogawat A. Osmolytes and their role in abiotic stress tolerance in plants. Mol Plant Abiotic Stress Biol Biotechnol. 2019;91–104.
   Google Scholar
• Dubey RS, Singh AK. Salinity Induces Accumulation of Soluble Sugars and Alters the Activity of Sugar Metabolising Enzymes in Rice Plants. Biologia Plantarum. 1999;42(2):233–239. doi:https://doi.org/10.1023/a:1002160618700.
   Web of Science ®Google Scholar
• Strand A, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, Stitt M. Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol. 1999;119(4):1387–1398. doi:https://doi.org/10.1104/pp.119.4.1387.
   PubMed Web of Science ®Google Scholar
• Gill PK, Sharma AD, Singh P, Bhullar SS. Effect of various abiotic stresses on the growth, soluble sugars and water relations of sorghum seedlings grown in light and darkness. Bulg J Plant Physiol. 2001;27:72–84.
   Google Scholar
• Koch KE. Carbohydrate-Modulated Gene Expression in Plants. Annu Rev Plant Physiol Plant Mol Biol. 1996;47(1):509–540. doi:https://doi.org/10.1146/annurev.arplant.47.1.509.
   PubMedGoogle Scholar
• López M, Tejera NA, Iribarne C, Lluch C, Herrera-Cervera JA. Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiol Plant. 2008;134(4):575–582. doi:https://doi.org/10.1111/j.1399-3054.2008.01162.x.
   PubMed Web of Science ®Google Scholar
• Cha-Um S, Charoenpanich A, Roytrakul S, Kirdmanee C. Sugar accumulation, photosynthesis and growth of two indica rice varieties in response to salt stress. Acta Physiologiae Plantarum. 2009;31(3):477–486. doi:https://doi.org/10.1007/s11738-008-0256-1.
   Web of Science ®Google Scholar
• Keunen ELS, Peshev D, Vangronsveld J, Van Den Ende WIM, Cuypers ANN. Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ. 2013;36(7):1242–1255. doi:https://doi.org/10.1111/pce.12061.
   PubMed Web of Science ®Google Scholar
• Kerepesi I, Galiba G. Osmotic and Salt Stress-Induced Alteration in Soluble Carbohydrate Content in Wheat Seedlings. Crop Sci. 2000;40(2):482–487. doi:https://doi.org/10.2135/cropsci2000.402482x.
   Web of Science ®Google Scholar
• Norwood M, Truesdale MR, Richter A, Scott P. Photosynthetic carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. J Exp Bot. 2000;51(343):159–165. doi:https://doi.org/10.1093/jexbot/51.343.159.
   PubMed Web of Science ®Google Scholar
• Whittaker A, Bochicchio A, Vazzana C, Lindsey G, Farrant J. Changes in leaf hexokinase activity and metabolite levels in response to drying in the desiccation-tolerant species Sporobolus stapfianus and Xerophyta viscosa. J Exp Bot. 2001;52(358):961–969. doi:https://doi.org/10.1093/jexbot/52.358.961.
   PubMed Web of Science ®Google Scholar
• Rontein D, Basset G, Hanson AD. Metabolic Engineering of Osmoprotectant Accumulation in Plants. Metab Eng. 2002;4(1):49–56. doi:https://doi.org/10.1006/mben.2001.0208.
   PubMed Web of Science ®Google Scholar
• Delorge I, Janiak M, Carpentier S, Van Dijck P. Fine tuning of trehalose biosynthesis and hydrolysis as novel tools for the generation of abiotic stress tolerant plants. Front Plant Sci. 2014: 5147–147. doi:https://doi.org/10.3389/fpls.2014.00147.
   Google Scholar
• ElSayed AI, Rafudeen MS, Golldack D, Weber A. Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol. 2013;16(1):1–8. doi:https://doi.org/10.1111/plb.12053.
   PubMed Web of Science ®Google Scholar
• Valluru R, Van Den Ende W. Myo-inositol and beyond– emerging networks under stress. Plant Sci. 2011;181(4):387–400. doi:https://doi.org/10.1016/j.plantsci.2011.07.009.
   PubMed Web of Science ®Google Scholar
• Radomiljac JD, Whelan J, Van Der Merwe M. Coordinating metabolite changes with our perception of plant abiotic stress responses: emerging views revealed by integrative-omic analyses. Metabolites. 2013;3(3):761–786. doi:https://doi.org/10.3390/metabo3030761.
   PubMedGoogle Scholar
• Kumutha D, Sairam R, Meena R. Role of root carbohydrate reserves and their mobilization in imparting waterlogging tolerance in green gram (Vigna radiata (L.) Wilczek) genotypes. Indian J Plant Physiol. 2008;13:339–346.
   Google Scholar
• Sheokand S. Effect of waterlogging, salinity and their interaction on growth, oxidative and carbohydrate metabolism in pigeonpea (Cajanus cajan L. Millsp.) genotypes. CCSHAU; 2016.
   Google Scholar
• Theerakulpisut P, Gunnula W. Exogenous Sorbitol and Trehalose mitigated salt stress damage in salt-sensitive but not salt-tolerant rice seedlings. Asian J Crop Sci. 2012;4(4):165–170. doi:https://doi.org/10.3923/ajcs.2012.165.170.
   Google Scholar
• Rhodes D, Handa S, Bressan RA. Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol. 1986;82(4):890–903. doi:https://doi.org/10.1104/pp.82.4.890.
   PubMed Web of Science ®Google Scholar
• Lugan R, Niogret M-F, Leport L, Guégan J-P, Larher FR, Savouré A, et al. Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. The Plant Journal 2010; 64(2):215–229. https://doi:10.1111/j.1365-313x.2010.04323.x
   Google Scholar
• Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, et al. Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol. 2000;122(3):747–756. https://doi:10.1104/pp.122.3.747
   PubMed Web of Science ®Google Scholar
• Suprasanna P, Rai AN, HimaKumari P, Kumar SA, Kavi Kishor P. Modulation of proline: implications in plant stress tolerance and development. In: Anjum NA, Gill SS, Gill R, editors. Plant Adaptation to Environmental Change. UK: CABI Publishers; 2014. p. 68–93.
   Google Scholar
• Hare P, Cress W. Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 1997;21(2):79–102. doi:https://doi.org/10.1023/A:1005703923347.
   Web of Science ®Google Scholar
• Kavi Kishor PB, Sreenivasulu N. Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ. 2013;37(2):300–311. doi:https://doi.org/10.1111/pce.12157.
   PubMed Web of Science ®Google Scholar
• Smirnoff N, Cumbes QJ. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry. 1989;28(4):1057–1060. doi:https://doi.org/10.1016/0031-9422(89)80182-7.
   Web of Science ®Google Scholar
• Mohanty P, Matysik J. Effect of proline on the production of singlet oxygen. Amino Acids. 2001;21(2):195–200. doi:https://doi.org/10.1007/s007260170026.
   PubMed Web of Science ®Google Scholar
• Matysik J, Alia BB, Mohanty P. Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci. 2002;525–532.
   Web of Science ®Google Scholar
• Dos Reis SP, Lima AM, De Souza CRB. Recent molecular advances on downstream plant responses to abiotic stress. Int J Mol Sci. 2012;13(7):8628–8647. doi:https://doi.org/10.3390/ijms13078628.
   PubMed Web of Science ®Google Scholar
• Rai AN, Penna S. Molecular evolution of plant P5CS gene involved in proline biosynthesis. Mol Biol Rep. 2013;40(11):6429–6435. doi:https://doi.org/10.1007/s11033-013-2757-2.
   PubMed Web of Science ®Google Scholar
• Delauney A, Hu C, Kishor P, Verma D. Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem. 1993;268(25):18673–18678. doi:https://doi.org/10.1016/S0021-9258(17)46682-8.
   PubMed Web of Science ®Google Scholar
• Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot. 2015;115(3):433–447. doi:https://doi.org/10.1093/aob/mcu239.
   PubMed Web of Science ®Google Scholar
• Lokhande VH, Nikam TD, Patade VY, Ahire ML, Suprasanna P. Effects of optimal and supra-optimal salinity stress on antioxidative defence, osmolytes and in vitro growth responses in Sesuvium portulacastrum L. Plant Cell, Tissue and Organ Culture (PCTOC). 2011;104(1):41–49. doi:https://doi.org/10.1007/s11240-010-9802-9.
   Web of Science ®Google Scholar
• Deuschle K, Funck D, Hellmann H, Däschner K, Binder S, Frommer WB. A nuclear gene encoding mitochondrial Δ1-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. Plant J. 2001;27(4):345–356. doi:https://doi.org/10.1046/j.1365-313X.2001.01101.x.
   PubMed Web of Science ®Google Scholar
• Khedr AHA. Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot. 2003;54(392):2553–2562. doi:https://doi.org/10.1093/jxb/erg277.
   PubMed Web of Science ®Google Scholar
• Cvikrová M, Gemperlová L, Martincová O, Vanková R. Effect of drought and combined drought and heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Physiol Biochem. 2013: 737–15. doi:https://doi.org/10.1016/j.plaphy.2013.08.005.
   Google Scholar
• Singh VP, Srivasatava J, Bansal R. Biochemical responses as stress indicator to water logging in pigeon pea (Cajanus cajan L.). 2017.
   Google Scholar
• Ullah I, Waqas M, Khan MA, Lee I-J, Kim W-C. Exogenous ascorbic acid mitigates flood stress damages of Vigna angularis. Appl Biol Chem. 2017;60:603–614.
   Web of Science ®Google Scholar
• Kahlaoui B, Hachicha M, Misle E, Fidalgo F, Teixeira J. Physiological and biochemical responses to the exogenous application of proline of tomato plants irrigated with saline water. J Saudi Soc Agric Sci. 2018;17(1):17–23. doi:https://doi.org/10.1016/j.jssas.2015.12.002.
   Google Scholar
• El Sabagh A, Sorour S, Ragab A, Islam MS, Barutçular C, Ueda A, et al. Alleviation of adverse effects of salt stress on soybean (Glycine max. L.) by using osmoprotectants and organic nutrients. Int J Agric Biol Eng. 2015;9(9):1014–1018.
   Google Scholar
• El Sabagh A, Sorour S, Omar A, Islam M, Ueda A, Saneoka H, et al. Soybean (Glycine Max L.) Growth Enhancement under Water Stress Conditions. International Conference on Chemical, Agricultural and Biological Sciences Istanbul, Turkey. Int J Agric Biol Eng. 2015:144–148.
   Google Scholar
• Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments: a review. Plant Signal Behav. 2012;7(11):1456–1466.
   PubMedGoogle Scholar
• Shahid MA, Balal RM, Pervez MA, Abbas T, Aqeel MA, Javaid MM, Garcia-Sanchez F. Exogenous proline and proline-enriched Lolium perenne leaf extract protects against phytotoxic effects of nickel and salinity in Pisum sativum by altering polyamine metabolism in leaves. Turkish J Bot. 2014;38(5):914–926. doi:https://doi.org/10.3906/bot-1312-13.
   Web of Science ®Google Scholar
• Wu G, Feng R, Li S, Du Y. Exogenous application of proline alleviates salt-induced toxicity in sainfoin seedlings. J Anim Plant Sci. 2017;27:246–251.
   Web of Science ®Google Scholar
• Hossain MA, Hasanuzzaman M, Fujita M. Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean. Frontiers Agric China. 2011;5(1):1–14. doi:https://doi.org/10.1007/s11703-010-1070-2.
   Google Scholar
• Molla MR, Ali MR, Hasanuzzaman M, Al-Mamun MH, Ahmed A, Nazim-Ud-Dowla M, Rohman MM. Exogenous Proline and Betaine-induced Upregulation of Glutathione Transferase and Glyoxalase I in Lentil (Lens culinaris) under Drought Stress. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2014;42(1):73–80. doi:https://doi.org/10.15835/nbha4219324.
   Web of Science ®Google Scholar
• Abdelhamid MT, Rady MM, Osman AS, Abdalla MA. Exogenous application of proline alleviates salt-induced oxidative stress in Phaseolus vulgaris L. plants. J Hortic Sci Biotechnol. 2013;88(4):439–446. doi:https://doi.org/10.1080/14620316.2013.11512989.
   Web of Science ®Google Scholar
• Aggarwal M, Sharma S, Kaur N, Pathania D, Bhandhari K, Kaushal N, Kaur R, Singh K, Srivastava A, Nayyar H. Exogenous proline application reduces phytotoxic effects of selenium by minimising oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings. Biol Trace Elem Res. 2011;140(3):354–367. doi:https://doi.org/10.1007/s12011-010-8699-9.
   PubMed Web of Science ®Google Scholar
• Nayyar H, Kaur R, Kaur S, Singh R. γ-Aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Regul. 2014;33(2):408–419. doi:https://doi.org/10.1007/s00344-013-9389-6.
   Web of Science ®Google Scholar
• Michaeli S, Fromm H. Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Front Plant Sci. 2015;6:419.
   Web of Science ®Google Scholar
• Sita K, Kumar V. Role of Gamma Amino Butyric Acid (GABA) against abiotic stress tolerance in legumes: a review. Plant Physiol Rep. 2020;1–10.
   Google Scholar
• Barbosa JM, Singh NK, Cherry JH, Locy RD. Nitrate uptake and utilization is modulated by exogenous γ-aminobutyric acid in Arabidopsis thaliana seedlings. Plant Physiol Biochem. 2010;48(6):443–450. doi:https://doi.org/10.1016/j.plaphy.2010.01.020.
   PubMed Web of Science ®Google Scholar
• Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, et al. The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol. 2010; 1020–20. doi:https://doi.org/10.1186/1471-2229-10-20.
   Google Scholar
• Kinnersley AM, Turano FJ. Gamma Aminobutyric Acid (GABA) and Plant Responses to Stress. CRC Crit Rev Plant Sci. 2000;19(6):479–509. doi:https://doi.org/10.1080/07352680091139277.
   Web of Science ®Google Scholar
• Zhang J, Zhang Y, Du Y, Chen S, Tang H. Dynamic Metabonomic Responses of Tobacco (Nicotiana tabacum) Plants to Salt Stress. J Proteome Res. 2011;10(4):1904–1914. doi:https://doi.org/10.1021/pr101140n.
   PubMed Web of Science ®Google Scholar
• Shi S-Q, Shi Z, Jiang Z-P, Qi L-W, Sun X-M, Li C-X, Liu J-F, Xiao W-F, Zhang S-G. Effects of exogenous GABA on gene expression ofCaragana intermedia roots under NaCl stress: regulatory roles for H2O2and ethylene production. Plant Cell Environ. 2010;33(2):149–162. doi:https://doi.org/10.1111/j.1365-3040.2009.02065.x.
   PubMed Web of Science ®Google Scholar
• Rezaei-Chiyaneh E, Seyyedi SM, Ebrahimian E, Moghaddam SS, Damalas CA. Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Ind Crops Prod. 2018;112:741–748.
   Web of Science ®Google Scholar
• Kaur R, Zhawar VK, Kaur G, Asthir B. Gamma-amino butyric acid effect in the alleviation of saline–alkaline stress conditions in rice. Cereal Res Commun. 2020;1–9.
   Web of Science ®Google Scholar
• Hu X, Xu Z, Xu W, Li J, Zhao N, Zhou Y. Application of γ-aminobutyric acid demonstrates a protective role of polyamine and GABA metabolism in muskmelon seedlings under Ca (NO3) 2 stress. Plant Physiol Biochem. 2015; 92:1–10.
   Web of Science ®Google Scholar
• Shang H, Cao S, Yang Z, Cai Y, Zheng Y. Effect of exogenous γ-aminobutyric acid treatment on proline accumulation and chilling injury in peach fruit after long-term cold storage. J Agric Food Chem. 2011;59(4):1264–1268. doi:https://doi.org/10.1021/jf104424z.
   PubMed Web of Science ®Google Scholar
• Krishnan S, Laskowski K, Shukla V, Merewitz EB. Mitigation of drought stress damage by exogenous application of a non-protein amino acid γ–aminobutyric acid on perennial ryegrass. J Am Soc Hortic Sci. 2013;138(5):358–366. doi:https://doi.org/10.21273/JASHS.138.5.358.
   Web of Science ®Google Scholar
• Vijayakumari K, Puthur JT. γ-Aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress. Plant Growth Regul. 2016;78(1):57–67. doi:https://doi.org/10.1007/s10725-015-0074-6.
   Web of Science ®Google Scholar
• Rhodes D, Hanson AD. Quaternary Ammonium and Tertiary Sulfonium Compounds in Higher Plants. Annu Rev Plant Physiol Plant Mol Biol. 1993;44(1):357–384. doi:https://doi.org/10.1146/annurev.pp.44.060193.002041.
   Google Scholar
• Chen THH, Murata N. Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci. 2008;13(9):499–505. doi:https://doi.org/10.1016/j.tplants.2008.06.007.
   PubMed Web of Science ®Google Scholar
• Saneoka H, Nagasaka C, Hahn DT, Yang WJ, Premachandra GS, Joly RJ, Rhodes D. Salt Tolerance of Glycinebetaine-Deficient and -Containing Maize Lines. Plant Physiol. 1995;107(2):631–638. doi:https://doi.org/10.1104/pp.107.2.631.
   PubMed Web of Science ®Google Scholar
• Chen THH, Murata N. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol. 2002;5(3):250–257. doi:https://doi.org/10.1016/s1369-5266(02)00255-8.
   PubMed Web of Science ®Google Scholar
• McCue K, Hanson A. Drought and salt tolerance: towards understanding and application. Trends Biotechnol. 1990:8358–8362. doi:https://doi.org/10.1016/0167-7799(90)90225-m.
   Google Scholar
• Yang W-J, Rich PJ, Axtell JD, Wood KV, Bonham CC, Ejeta G, Mickelbart MV, Rhodes D. Genotypic Variation for Glycinebetaine in Sorghum. Crop Sci. 2003;43(1):162. doi:https://doi.org/10.2135/cropsci2003.1620.
   Web of Science ®Google Scholar
• Chen TH, Murata N. Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ. 2011;34(1):1–20. doi:https://doi.org/10.1111/j.1365-3040.2010.02232.x.
   PubMed Web of Science ®Google Scholar
• Al-Taweel K, Iwaki T, Yabuta Y, Shigeoka S, Murata N, Wadano A. A bacterial transgene for catalase protects translation of d1 protein during exposure of salt-stressed tobacco leaves to strong light. Plant Physiol. 2007;145(1):258–265. doi:https://doi.org/10.1104/pp.107.101733.
   PubMed Web of Science ®Google Scholar
• Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 2008;13(4):178–182. doi:https://doi.org/10.1016/j.tplants.2008.01.005.
   PubMed Web of Science ®Google Scholar
• Farooq M, Ali S, Hameed A, Bharwana S, Rizwan M, Ishaque W, et al. Cadmium stress in cotton seedlings: physiological, photosynthesis and oxidative damages alleviated by glycinebetaine. S Afr J Bot. 2016;10461–10468.
   Web of Science ®Google Scholar
• Razavi F, Mahmoudi R, Rabiei V, Aghdam MS, Soleimani A. Glycine betaine treatment attenuates chilling injury and maintains nutritional quality of hawthorn fruit during storage at low temperature. Sci Hortic (Amsterdam). 2018;233188–233194.
   Web of Science ®Google Scholar
• Abdelmotlb N, Abdel-All F, Abd EL-Hady S, EL-Miniawy S, Ghoname A. Glycine betaine and sugar beet extract ameliorated salt stress adverse effect on green bean irrigated with saline water. Middle East J Agric Res. 2019;91:42–54.
   Google Scholar
• Rezaei MA, Kaviani B, Masouleh AK. The effect of exogenous glycine betaine on yield of soybean [Glycine max (L.) Merr.] in two contrasting cultivars Pershing and DPX under soil salinity stress. Plant Omics. 2012;5:87.
   Web of Science ®Google Scholar
• Malekzadeh P. Influence of exogenous application of glycinebetaine on antioxidative system and growth of salt-stressed soybean seedlings (Glycine max L.). Physiol Mol Biol Plants. 2015;21(2):225–232. doi:https://doi.org/10.1007/s12298-015-0292-4.
   PubMed Web of Science ®Google Scholar
• Smirnoff N. Plant resistance to environmental stress. Curr Opin Biotechnol. 1998;9(2):214–219. doi:https://doi.org/10.1016/s0958-1669(98)80118-3.
   PubMed Web of Science ®Google Scholar
• Tarczynski MC, Jensen RG, Bohnert HJ Expression of a bacterial mtlD gene in transgenic tobacco leads to production and accumulation of mannitol. Proceedings of the National Academy of Sciences of the United States of America 1992; 89( 7):2600–2604. https://doi.org/10.1073/pnas.89.7.2600.
   Google Scholar
• Thomas JC, Sepahi M, Arendall B, Bohnert HJ. Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant Cell Environ. 1995;18(7):801–806. doi:https://doi.org/10.1111/j.1365-3040.1995.tb00584.x
   Web of Science ®Google Scholar
• Yancey P, Clark M, Hand S, Bowlus R, Somero G. Living with water stress: evolution of osmolyte systems. Science. 1982;217(4566):1214–1222. doi:https://doi.org/10.1126/science.7112124.
   PubMed Web of Science ®Google Scholar
• Vernon DM, Bohnert HJ. A novel methyl transferase induced by osmotic stress in the facultative halophyte Mesembryanthemum crystallinum. Embo J. 1992;11(6):2077–2085. doi:https://doi.org/10.1002/j.1460-2075.1992.tb05266.x.
   PubMed Web of Science ®Google Scholar
• Adams P, Thomas JC, Vernon DM, Bohnert HJ, Jensen RG. Distinct cellular and organismic responses to salt stress. Plant Cell Physiol. 1992;33:1215–1223.
   Web of Science ®Google Scholar
• Rammesmayer G, Pichorner H, Adams P, Jensen RG, Bohnert HJ. Characterization of IMT1, myo-Inositol O-methyltransferase, from Mesembryanthemum crystallinum. Arch Biochem Biophys. 1995;322(1):183–188. doi:https://doi.org/10.1006/abbi.1995.1450.
   PubMed Web of Science ®Google Scholar
• Nelson DE, Rammesmayer G, Bohnert HJ. Regulation of cell-specific inositol metabolism and transport in plant salinity tolerance. Plant Cell. 1998;10(5):753–764. doi:https://doi.org/10.1105/tpc.10.5.753.
   PubMed Web of Science ®Google Scholar
• Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio AF. Plant Polyamines in Reproductive Activity and Response to Abiotic Stress*. Botanica Acta. 1997;110(3):197–207. doi:https://doi.org/10.1111/j.1438-8677.1997.tb00629.x.
   Google Scholar
• Thomas* T, Thomas TJ. Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell Mol Life Sci. 2001;58(2):244–258. doi:https://doi.org/10.1007/pl00000852.
   PubMed Web of Science ®Google Scholar
• Paschalidis KA, Roubelakis-Angelakis KA. Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant. Correlations with age, cell division/expansion, and differentiation. Plant Physiol. 2005;138(1):142–152. doi:https://doi.org/10.1104/pp.104.055483.
   PubMed Web of Science ®Google Scholar
• Paschalidis KA, Roubelakis-Angelakis KA. Sites and regulation of polyamine catabolism in the tobacco plant. Correlations with cell division/expansion, cell cycle progression, and vascular development. Plant Physiol. 2005;138(4):2174–2184. doi:https://doi.org/10.1104/pp.105.063941.
   PubMed Web of Science ®Google Scholar
• Liu JH. Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot. 2006;57(11):2589–2599. doi:https://doi.org/10.1093/jxb/erl018.
   PubMed Web of Science ®Google Scholar
• Zhao H, Yang H. Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Sci Hortic (Amsterdam). 2008;116(4):442–447. doi:https://doi.org/10.1016/j.scienta.2008.02.017.
   Web of Science ®Google Scholar
• Kusano T, Yamaguchi K, Berberich T, Takahashi Y. Advances in polyamine research in 2007. J Plant Res. 2007;120(3):345–350. doi:https://doi.org/10.1007/s10265-007-0074-3.
   PubMed Web of Science ®Google Scholar
• Kusano T, Yamaguchi K, Berberich T, Takahashi Y. The polyamine spermine rescues Arabidopsis from salinity and drought stresses. Plant Signal Behav. 2007;2(4):251–252. doi:https://doi.org/10.4161/psb.2.4.3866.
   PubMed Web of Science ®Google Scholar
• De Oliveira LF, Elbl P, Navarro BV, Macedo AF, Dos Santos AL, Floh EI, Cooke J. Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiol. 2017;37(1):116–130. doi:https://doi.org/10.1093/treephys/tpw107.
   PubMed Web of Science ®Google Scholar
• Reis RS, De Moura Vale E, Heringer AS, Santa-Catarina C, Silveira V. Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane. J Proteomics. 2016;130:170–179.
   Web of Science ®Google Scholar
• Mustafavi SH, Badi HN, Sękara A, Mehrafarin A, Janda T, Ghorbanpour M, Rafiee H. Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiologiae Plantarum. 2018;40(6):1–19. doi:https://doi.org/10.1007/s11738-018-2671-2.
   Web of Science ®Google Scholar
• Kaur-Sawhney R, Tiburcio AF, Altabella T, Galston AW. Polyamines in plants: an overview. J Cell Mol Biol. 2003; 2:1–12.
   Google Scholar
• Pang X-M, Zhang Z-Y, Wen X-P, Ban Y, Moriguchi T. Polyamines, all-purpose players in response to environment stresses in plants. Plant Stress. 2007;1:173–188.
   Google Scholar
• Kusano T, Berberich T, Tateda C, Takahashi Y. Polyamines: essential factors for growth and survival. Planta. 2008;228(3):367–381. doi:https://doi.org/10.1007/s00425-008-0772-7.
   PubMed Web of Science ®Google Scholar
• Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A. Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol. 2008;148(2):1094–1105. doi:https://doi.org/10.1104/pp.108.122945.
   PubMed Web of Science ®Google Scholar
• Nadeau P, Delaney S, Chouinard L. Effects of Cold Hardening on the Regulation of Polyamine Levels in Wheat (Triticum aestivum L.) and Alfalfa (Medicago sativa L.). Plant Physiol. 1987;84(1):73–77. doi:https://doi.org/10.1104/pp.84.1.73.
   PubMed Web of Science ®Google Scholar
• Roy P, Niyogi K, SenGupta DN, Ghosh B. Spermidine treatment to rice seedlings recovers salinity stress-induced damage of plasma membrane and PM-bound H+-ATPase in salt-tolerant and salt-sensitive rice cultivars. Plant Sci. 2005;168(3):583–591. doi:https://doi.org/10.1016/j.plantsci.2004.08.014.
   Web of Science ®Google Scholar
• Kuznetsov VV, Shevyakova NI. Polyamines and stress tolerance of plants. Plant Stress. 2007;1:50–71.
   Google Scholar
• Liu Y, Liang H, Lv X, Liu D, Wen X, Liao Y. Effect of polyamines on the grain filling of wheat under drought stress. Plant Physiol Biochem. 2016;100113–100129.
   Web of Science ®Google Scholar
• Mohammadi H, Ghorbanpour M, Brestic M. Exogenous putrescine changes redox regulations and essential oil constituents in field-grown Thymus vulgaris L. under well-watered and drought stress conditions. Ind Crops Prod. 2018;122:119–132.
   Web of Science ®Google Scholar
• Sadeghipour O. Polyamines protect mung bean [Vigna radiata (L.) Wilczek] plants against drought stress. Biologia Futura. 2019;70(1):71–78. doi:https://doi.org/10.1556/019.70.2019.09.
   PubMedGoogle Scholar
• Nahar K, Hasanuzzaman M, Rahman A, Alam M, Mahmud J-A, Suzuki T, et al. Polyamines confer salt tolerance in mung bean (Vigna radiata L.) by reducing sodium uptake, improving nutrient homeostasis, antioxidant defense, and methylglyoxal detoxification systems. Front Plant Sci. 2016;7:1104.
   PubMed Web of Science ®Google Scholar
• Garg N, Sharma A. Role of putrescine (Put) in imparting salt tolerance through modulation of put metabolism, mycorrhizal and rhizobial symbioses in Cajanus cajan (L.) Millsp. Symbiosis. 2019;79(1):59–74. doi:https://doi.org/10.1007/s13199-019-00621-7.
   Web of Science ®Google Scholar
• Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta. 2003;218(1):1–14. doi:https://doi.org/10.1007/s00425-003-1105-5.
   PubMed Web of Science ®Google Scholar
• Tan J, Wang C, Xiang BIN, Han R, Guo Z. Hydrogen peroxide and nitric oxide mediated cold- and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell Environ. 2012;36(2):288–299. doi:https://doi.org/10.1111/j.1365-3040.2012.02573.x.
   PubMed Web of Science ®Google Scholar
• Fan W, Zhang M, Zhang H, Zhang P, Park S. Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. PloS One. 2012;7(5):e37344–e37344. doi:https://doi.org/10.1371/journal.pone.0037344.
   PubMed Web of Science ®Google Scholar
• Pilon-Smits EAH, Terry N, Sears T, Kim H, Zayed A, Hwang S, Van Dun K, Voogd E, Verwoerd TC, Krutwagen RWHH. Trehalose-producing transgenic tobacco plants show improved growth performance under drought stress. J Plant Physiol. 1998;152(4–5):525–532. doi:https://doi.org/10.1016/s0176-1617(98)80273-3.
   Web of Science ®Google Scholar
• Su J, Hirji R, Zhang L, He C, Selvaraj G, Wu R. Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. J Exp Bot. 2006;57(5):1129–1135. doi:https://doi.org/10.1093/jxb/erj133.
   PubMed Web of Science ®Google Scholar
• Kathuria H, Giri J, Nataraja KN, Murata N, Udayakumar M, Tyagi AK. Glycinebetaine-induced water-stress tolerance incodA-expressing transgenicindicarice is associated with up-regulation of several stress responsive genes. Plant Biotechnol J. 2009;7(6):512–526. doi:https://doi.org/10.1111/j.1467-7652.2009.00420.x.
   PubMed Web of Science ®Google Scholar
• Abebe T, Guenzi AC, Martin B, Cushman JC. Tolerance of Mannitol-Accumulating Transgenic Wheat to Water Stress and Salinity. Plant Physiol. 2003;131(4):1748–1755. doi:https://doi.org/10.1104/pp.102.003616.
   PubMed Web of Science ®Google Scholar
• Cortina C, Culiáñez-Macià FA. Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci. 2005;169(1):75–82. doi:https://doi.org/10.1016/j.plantsci.2005.02.026.
   Web of Science ®Google Scholar
• Mattioli R, Marchese D, D’Angeli S, Altamura MM, Costantino P, Trovato M. Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Mol Biol. 2008;66(3):277–288. doi:https://doi.org/10.1007/s11103-007-9269-1.
   PubMed Web of Science ®Google Scholar
• Miranda JA, Avonce N, Suárez R, Thevelein JM, Van Dijck P, Iturriaga G. A bifunctional TPS–TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta. 2007;226(6):1411–1421. doi:https://doi.org/10.1007/s00425-007-0579-y.
   PubMed Web of Science ®Google Scholar
• Yeo E-T, Kwon H-B, Han S-E, Lee J-T, Ryu J-C, Byu M. Genetic engineering of drought resistant potato plants by introduction of the trehalose-6-phosphate synthase (TPS1) gene from Saccharomyces cerevisiae. Mol Cells. 2000;10:263–268.
   PubMed Web of Science ®Google Scholar
• Lilius G, Holmberg N, Bülow L. Enhanced NaCl Stress Tolerance in Transgenic Tobacco Expressing Bacterial Choline Dehydrogenase. Nat Biotechnol. 1996;14(2):177–180. doi:https://doi.org/10.1038/nbt0296-177.
   Google Scholar
• Holmström KO, Somersalo S, Mandal A, Palva TE, Welin B. Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot. 2000;51(343):177–185. doi:https://doi.org/10.1093/jexbot/51.343.177.
   PubMed Web of Science ®Google Scholar
• Zhang J, Tan W, Yang X-H, Zhang H-X. Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco. Plant Cell Rep. 2008;27(6):1113–1124. doi:https://doi.org/10.1007/s00299-008-0549-2.
   PubMed Web of Science ®Google Scholar
• Hasthanasombut S, Ntui V, Supaibulwatana K, Mii M, Nakamura I. Expression of Indica rice OsBADH1 gene under salinity stress in transgenic tobacco. Plant Biotechnol Rep. 2009;4(1):75–83. doi:https://doi.org/10.1007/s11816-009-0123-6.
   Web of Science ®Google Scholar
• Yang X, Liang Z, Wen X, Lu C. Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol. 2007;66(1–2):73–86. doi:https://doi.org/10.1007/s11103-007-9253-9.
   PubMed Web of Science ®Google Scholar
• Holmström K-O, Mäntylä E, Welin B, Mandal A, Palva ET, Tunnela OE, et al. Drought tolerance in tobacco. Nature. 1996;379(6567):683–684. doi:https://doi.org/10.1038/379683a0.
   Web of Science ®Google Scholar
• Karim S, Aronsson H, Ericson H, Pirhonen M, Leyman B, Welin B, Mäntylä E, Palva ET, Van Dijck P, Holmström K-O. Improved drought tolerance without undesired side effects in transgenic plants producing trehalose. Plant Mol Biol. 2007;64(4):371–386. doi:https://doi.org/10.1007/s11103-007-9159-6.
   PubMed Web of Science ®Google Scholar
• Nakayama H, Yoshida K, Ono H, Murooka Y, Shinmyo A. Ectoine, the compatible solute of Halomonas elongata, confers hyperosmotic tolerance in cultured tobacco cells. Plant Physiol. 2000;122(4):1239–1247. doi:https://doi.org/10.1104/pp.122.4.1239.
   PubMed Web of Science ®Google Scholar
• Moghaieb REA, Tanaka N, Saneoka H, Murooka Y, Ono H, Morikawa H, Nakamura A, Nguyen NT, Suwa R, Fujita K. Characterization of salt tolerance in ectoine-transformed tobacco plants (Nicotiana tabaccum): photosynthesis, osmotic adjustment, and nitrogen partitioning. Plant Cell Environ. 2006;29(2):173–182. doi:https://doi.org/10.1111/j.1365-3040.2005.01410.x.
   PubMed Web of Science ®Google Scholar
• Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y. Effects of free proline accumulation in petunias under drought stress. J Exp Bot. 2005;56(417):1975–1981. doi:https://doi.org/10.1093/jxb/eri195.
   PubMed Web of Science ®Google Scholar
• Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, Vieira LGE. Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol. 2007;164(10):1367–1376. doi:https://doi.org/10.1016/j.jplph.2007.05.001.
   PubMed Web of Science ®Google Scholar
• Simon-Sarkadi L, Kocsy G, Varhegyi A, Galiba G, Ronde JA. Stress-induced changes in the free amino acid composition in transgenic soybean plants having increased proline content. Biologia Plantarum. 2006;50(4):793–796. doi:https://doi.org/10.1007/s10535-006-0134-x.
   Web of Science ®Google Scholar
• Mwenye OJ, Van Rensburg L, Van Biljon A. Van der Merwe R. The role of proline and root traits on selection for drought-stress tolerance in soybeans: a review. S Afr J Plant Soil. 2016;33(4):245–256. doi:https://doi.org/10.1080/02571862.2016.1148786.
   Google Scholar
• Lv S, Yang A, Zhang K, Wang L, Zhang J. Increase of glycinebetaine synthesis improves drought tolerance in cotton. Mol Breed. 2007;20(3):233–248. doi:https://doi.org/10.1007/s11032-007-9086-x.
   Web of Science ®Google Scholar
• He C, Yang A, Zhang W, Gao Q, Zhang J. Improved salt tolerance of transgenic wheat by introducing betA gene for glycine betaine synthesis. Plant Cell, Tissue and Organ Culture (PCTOC). 2010;101(1):65–78. doi:https://doi.org/10.1007/s11240-009-9665-0.
   Web of Science ®Google Scholar
• Kumar S, Dhingra A, Daniell H. Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiol. 2004;136(1):2843–2854. doi:https://doi.org/10.1104/pp.104.045187.
   PubMed Web of Science ®Google Scholar
• Fitzgerald TL, Waters DLE, Henry RJ. Betaine aldehyde dehydrogenase in plants. Plant Biol. 2009;11(2):119–130. doi:https://doi.org/10.1111/j.1438-8677.2008.00161.x.
   PubMed Web of Science ®Google Scholar
• Garg AK, Kim J-K, Owens TG, Ranwala AP, Choi YD, Kochian LV, et al. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proceedings of the National Academy of Sciences of the United States of America 2002; 99( 25):15898–15903. https://doi.org/10.1073/pnas.252637799.
   Google Scholar
• Kondrák M, Marincs F, Antal F, Juhász Z, Bánfalvi Z. Effects of yeast trehalose-6-phosphate synthase 1 on gene expression and carbohydrate contents of potato leaves under drought stress conditions. BMC Plant Biol. 2012: 1274–74. doi:https://doi.org/10.1186/1471-2229-12-74.
   Google Scholar
• Shima S, Matsui H, Tahara S, Imai R. Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes. Febs J. 2007;274(5):1192–1201. doi:https://doi.org/10.1111/j.1742-4658.2007.05658.x.
   PubMed Web of Science ®Google Scholar
• Habibur Rahman Pramanik M, Imai R. Functional Identification of a Trehalose 6-phosphate Phosphatase Gene that is Involved in Transient Induction of Trehalose Biosynthesis during Chilling Stress in Rice. Plant Mol Biol. 2005;58(6):751–762. doi:https://doi.org/10.1007/s11103-005-7404-4.
   PubMed Web of Science ®Google Scholar
• Avonce N, Leyman B, Mascorro-Gallardo JO, Van Dijck P, Thevelein JM, Iturriaga G. The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol. 2004;136(3):3649–3659. doi:https://doi.org/10.1104/pp.104.052084.
   PubMed Web of Science ®Google Scholar
• Romero C, Bellés JM, Vayá JL, Serrano R, Culiáñez-Macià FA. Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta. 1997;201(3):293–297. doi:https://doi.org/10.1007/s004250050069.
   PubMed Web of Science ®Google Scholar
• Conde A, Silva P, Agasse A, Conde C, Geros H. Mannitol Transport and Mannitol Dehydrogenase Activities are Coordinated in Olea europaea Under Salt and Osmotic Stresses. Plant Cell Physiol. 2011;52(10):1766–1775. doi:https://doi.org/10.1093/pcp/pcr121.
   PubMed Web of Science ®Google Scholar
• Hu L, Lu H, Liu Q, Chen X, Jiang X. Overexpression of mtlD gene in transgenic Populus tomentosa improves salt tolerance through accumulation of mannitol. Tree Physiol. 2005;25(10):1273–1281. doi:https://doi.org/10.1093/treephys/25.10.1273.
   PubMed Web of Science ®Google Scholar
• Tarczynski MC, Jensen RG, Bohnert HJ. Stress Protection of Transgenic Tobacco by Production of the Osmolyte Mannitol. Science. 1993;259(5094):508–510. doi:https://doi.org/10.1126/science.259.5094.508.
   PubMed Web of Science ®Google Scholar
• Sheveleva E, Chmara W, Bohnert HJ, Jensen RG. Increased Salt and Drought Tolerance by D-Ononitol Production in Transgenic Nicotiana tabacum L. Plant Physiol. 1997;115(3):1211–1219. doi:https://doi.org/10.1104/pp.115.3.1211.
   PubMed Web of Science ®Google Scholar
• Pilon-Smits EAH, Ebskamp MJM, Paul MJ, Jeuken MJW, Weisbeek PJ, Smeekens SCM. Improved Performance of Transgenic Fructan-Accumulating Tobacco under Drought Stress. Plant Physiol. 1995;107(1):125–130. doi:https://doi.org/10.1104/pp.107.1.125.
   PubMed Web of Science ®Google Scholar
• Capell T, Bassie L, Christou P Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proceedings of the National Academy of Sciences of the United States of America 2004; 101( 26):9909–9914. https://doi.org/10.1073/pnas.0306974101.
   Google Scholar
• Peremarti A, Bassie L, Christou P, Capell T. Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Mol Biol. 2009;70(3):253–264. doi:https://doi.org/10.1007/s11103-009-9470-5.
   PubMed Web of Science ®Google Scholar
• Roy M, Wu R. Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci. 2002;163(5):987–992. doi:https://doi.org/10.1016/s0168-9452(02)00272-8.
   Web of Science ®Google Scholar
• Franceschetti M, Fornalè S, Tassoni A, Zuccherelli K, Mayer MJ, Bagni N. Effects of spermidine synthase overexpression on polyamine biosynthetic pathway in tobacco plants. J Plant Physiol. 2004;161(9):989–1001. doi:https://doi.org/10.1016/j.jplph.2004.02.004.
   PubMed Web of Science ®Google Scholar
• Wen X-P, Pang X-M, Matsuda N, Kita M, Inoue H, Hao Y-J, Honda C, Moriguchi T. Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res. 2007;17(2):251–263. doi:https://doi.org/10.1007/s11248-007-9098-7.
   PubMed Web of Science ®Google Scholar
• Prabhavathi VR, Rajam MV. Polyamine accumulation in transgenic eggplant enhances tolerance to multiple abiotic stresses and fungal resistance. Plant Biotechnol. 2007;24(3):273–282. doi:https://doi.org/10.5511/plantbiotechnology.24.273.
   Web of Science ®Google Scholar