5,700
Views
99
CrossRef citations to date
0
Altmetric
Review

Calcium signaling and salt tolerance are diversely entwined in plants

ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon, & ORCID Icon show all
Article: 1665455 | Received 24 Jul 2019, Accepted 28 Aug 2019, Published online: 28 Sep 2019

References

  • Negrão S, Schmöckel S, Tester M. Evaluating physiological responses of plants to salinity stress. Ann. Bot. 2017;119:1–15. doi:10.1093/aob/mcw191.
  • Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD. Economics of salt‐induced land degradation and restoration.  Nat Resour Forum. 2014;38:282–295. doi:10.1111/1477-8947.12054.
  • Valenzuela CE, Acevedo-Acevedo O, Miranda GS, Vergara-Barros P, Holuigue L, Figueroa CR, Figueroa PM. Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root. J Exp Bot. 2016;67:4209–4220. doi:10.1093/jxb/erw202.
  • Zhu J-K. Abiotic stress signaling and responses in plants. Cell. 2016;167:313–324. doi:10.1016/j.cell.2016.08.029.
  • Lu P, Magwanga R, Lu H, Kirungu J, Wei Y, Dong Q, Wang X, Cai X, Zhou Z, Wang K, et al. A novel G-protein-coupled receptors gene from upland cotton enhances salt stress tolerance in transgenic Arabidopsis. Genes. 2018;9:209. doi:10.3390/genes9040209.
  • Bano A, Fatima M. Salt tolerance in zea mays (L). following inoculation with rhizobium and pseudomonas. Biol Fertil Soils. 2009;45:405–413. doi:10.1007/s00374-008-0344-9.
  • Weimers K. Growth and phosphorus uptake of potato (Solanum tuberosum L.) in an alkaline soil as affected by mineral nitrogen forms and inoculation with phosphate-solubilizing bacteria and mycorrhizal fungi, SLU, Swedish University of Agricultural Sciences Faculty of Landscape Architecture, Horticulture and Crop Production Science, Department of Biosystems and Technology. 2017.
  • Keisham M, Mukherjee S, Bhatla S. Mechanisms of sodium transport in plants—progresses and challenges. Int J Mol Sci. 2018;19:647. doi:10.3390/ijms19030647.
  • Pottosin I, Dobrovinskaya O. Non-selective cation channels in plasma and vacuolar membranes and their contribution to K+ transport. J Plant Physiol. 2014;171:732–742. doi:10.1016/j.jplph.2013.11.013.
  • Zhang W-D, Wang P, Bao Z, Ma Q, Duan L-J, Bao A-K, Zhang JL, Wang SM. SOS1, HKT1; 5, and NHX1 synergistically modulate Na+ homeostasis in the halophytic grass Puccinellia tenuiflora. Front Plant Sci. 2017;8:576.
  • Chen X, Lu X, Shu N, Wang D, Wang S, Wang J, Guo L, Guo X, Fan W, Lin Z, et al. GhSOS1, a plasma membrane Na+/H+ antiporter gene from upland cotton, enhances salt tolerance in transgenic Arabidopsis thaliana. PLoS One. 2017;12:e0181450. doi:10.1371/journal.pone.0181450.
  • Pardo JM, Rubio F. Na+ and K+ transporters in plant signaling. Transporters and pumps in plant signaling.  Berlin, Heidelberg: Springer; 2011. p. 65–98. doi:10.1007/978-3-642-14369-4_3.
  • Teakle NL, Tyerman SD. Mechanisms of Cl− transport contributing to salt tolerance. Plant Cell Environ. 2010;33:566–589. doi:10.1111/j.1365-3040.2009.02060.x.
  • Barbier-Brygoo H, De Angeli A, Filleur S, Frachisse J-M, Gambale F, Thomine S, Wege S. Anion channels/transporters in plants: from molecular bases to regulatory networks. Annu. Rev. Plant Biol. 2011;62:25–51. doi:10.1146/annurev-arplant-042110-103741.
  • Shabala S. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann. Bot. 2013;112:1209–1221. doi:10.1093/aob/mct205.
  • Wegner LH. Root pressure and beyond: energetically uphill water transport into xylem vessels? J Exp Bot. 2013;65:381–393. doi:10.1093/jxb/ert391.
  • Fricke W. The significance of water co-transport for sustaining transpirational water flow in plants: a quantitative approach. J Exp Bot. 2015;66:731–739. doi:10.1093/jxb/eru466.
  • Henderson SW, Wege S, Qiu J, Blackmore DH, Walker AR, Tyerman SD, Walker RR, Gilliham M. Grapevine and Arabidopsis cation-chloride cotransporters localize to the golgi and trans-golgi network and indirectly influence long-distance ion transport and plant salt tolerance. Plant Physiol. 2015;169:2215–2229. doi:10.1104/pp.15.00499.
  • Tao -J-J, Chen H-W, Ma B, Zhang W-K, Chen S-Y, Zhang J-S. The role of ethylene in plants under salinity stress. Front Plant Sci. 2015;6:1059. doi:10.3389/fpls.2015.01059.
  • Kamiyoshihara Y, Iwata M, Fukaya T, Tatsuki M, Mori H. Turnover of LeACS2, a wound‐inducible 1‐aminocyclopropane‐1‐carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J. 2010;64:140–150. doi:10.1111/j.1365-313X.2010.04316.x.
  • Liang W, Ma X, Wan P, Liu L. Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun. 2018;495:286–291. doi:10.1016/j.bbrc.2017.11.043.
  • Aldon D, Mbengue M, Mazars C, Galaud J-P. Calcium signalling in plant biotic interactions. Int. J. Mol. Sci. 2018;19:665. doi:10.3390/ijms19030665.
  • Zhang M, Smith JAC, Harberd NP, Jiang C. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol. 2016;91:651–659. doi:10.1007/s11103-016-0488-1.
  • Verma V, Ravindran P, Kumar PP. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016;16:86. doi:10.1186/s12870-016-0796-2.
  • Gravino M, Savatin DV, Macone A, De Lorenzo G. Ethylene production in B otrytis cinerea‐and oligogalacturonide‐induced immunity requires calcium‐dependent protein kinases. Plant J. 2015;84:1073–1086. doi:10.1111/tpj.13057.
  • Lee HY, Back K. Mitogen‐activated protein kinase pathways are required for melatonin‐mediated defense responses in plants. J Pineal Res. 2016;60:327–335. doi:10.1111/jpi.12314.
  • Schmöckel SM, Garcia AF, Berger B, Tester M, Webb AA, Roy SJ. Different NaCl-induced calcium signatures in the Arabidopsis thaliana ecotypes Col-0 and C24. PLoS One. 2015;10:e0117564. doi:10.1371/journal.pone.0117564.
  • Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu M-C, Maman J, Steinhorst L, Schmitz-Thom I, et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol. 2018;28:666–75. e5. doi:10.1016/j.cub.2018.01.023.
  • Wu H. Plant salt tolerance and Na+ sensing and transport. Crop J. 2018;6:215–225. doi:10.1016/j.cj.2018.01.003.
  • Zörb C, Mühling KH, Kutschera U, Geilfus C-M. Salinity stiffens the epidermal cell walls of salt-stressed maize leaves: is the epidermis growth-restricting? PLoS One. 2015;10:e0118406. doi:10.1371/journal.pone.0118406.
  • Geilfus C-M. Expansin expression and apoplastic pH in expanding leaves under NaCl stress. Christian-Albrechts Universität Kiel, Germany; 2011.
  • Dinneny JR, Long TA, Wang JY, Jung JW, Mace D, Pointer S, Barron C, Brady SM, Schiefelbein J, Benfey PN. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science. 2008;320:942–945. doi:10.1126/science.1153795.
  • Okubo-Kurihara E, Ohtani M, Kurihara Y, Kakegawa K, Kobayashi M, Nagata N, Komatsu T, Kikuchi J, Cutler S, Demura T, et al. Modification of plant cell wall structure accompanied by enhancement of saccharification efficiency using a chemical, lasalocid sodium. Sci Rep. 2016;6:34602. doi:10.1038/srep34602.
  • Tran L-SP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, Yamaguchi-Shinozaki K Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 2007; 104:20623–20628. 10.1073/pnas.0706547105
  • Zhu J-K. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol. 2003;6:441–445.
  • Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N Identification of histidine kinases that act as sensors in the perception of salt stress in synechocystis sp. PCC 6803. Proc Natl Acad Sci USA. 2003;100:9061–9066. https://www.scimagojr.com/journalsearch.php?q=21121&tip=sid.
  • Jin Y, Jing W, Zhang Q, Zhang W. Cyclic nucleotide gated channel 10 negatively regulates salt tolerance by mediating Na+ transport in Arabidopsis. J Plant Res. 2015;128:211–220. doi:10.1007/s10265-014-0679-2.
  • González-Fontes A, Navarro-Gochicoa MT, Ceacero CJ, Herrera-Rodríguez MB, Camacho-Cristóbal JJ, Rexach J. Understanding calcium transport and signaling, and its use efficiency in vascular plants. Plant Macronutrient Use Efficiency: Elsevier; 2017. p. 165–180. doi:10.1016/B978-0-12-811308-0.00009-0
  • Finka A, Cuendet AFH, Maathuis FJ, Saidi Y, Goloubinoff P. Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell. 2012;24:3333–3348. doi:10.1105/tpc.112.095844.
  • Fischer C, DeFalco TA, Karia P, Snedden WA, Moeder W, Yoshioka K, Dietrich P. Calmodulin as a Ca2+-sensing subunit of Arabidopsis cyclic nucleotide-gated channel complexes. Plant Cell Physiol. 2017;58:1208–1221. doi:10.1093/pcp/pcx052.
  • Wang P, Li Z, Wei J, Zhao Z, Sun D, Cui S. A Na+/Ca2+ exchanger-like protein (AtNCL) involved in salt stress in Arabidopsis. J Biol Chem. 2012;287:44062–44070. doi:10.1074/jbc.M112.351643.
  • Shabala S, Wu H, Bose J. Salt stress sensing and early signalling events in plant roots: current knowledge and hypothesis. Plant Sci. 2015;241:109–119. doi:10.1016/j.plantsci.2015.10.003.
  • Li P, Zhang G, Gonzales N, Guo Y, Hu H, Park S, Zhao J. Ca2+‐regulated and diurnal rhythm‐regulated Na+/Ca2+ exchanger AtNCL affects flowering time and auxin signalling in Arabidopsis. Plant Cell Environ. 2016;39:377–392. doi:10.1111/pce.v39.2.
  • Huang WY, Alvarez S, Lee YK, Kondo Y, Chung JK, Lam HYM, Kuriyan J, Groves JT. Molecular timing of membrane signaling reactions. Biophys J. 2018;114:202a. doi:10.1016/j.bpj.2017.11.1130.
  • Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X. The Salt Overly Sensitive (SOS) pathway: established and emerging roles. Mol Plant. 2013;6:275–286. doi:10.1093/mp/sst017.
  • Julkowska MM, Testerink C. Tuning plant signaling and growth to survive salt. Trends Plant Sci. 2015;20:586–594. doi:10.1016/j.tplants.2015.06.008.
  • Quan R, Wang J, Yang D, Zhang H, Zhang Z, Huang R. EIN3 and SOS2 synergistically modulate plant salt tolerance. Sci Rep. 2017;7:44637. doi:10.1038/srep44637.
  • Cramer GR. Sodium-calcium interactions under salinity stress. Salinity: environment-plants-molecules.Dordrecht: Springer; 2002. p. 205–227. doi:10.1007/0-306-48155-3_10.
  • Lynch J, Polito VS, Läuchli AJPP. Salinity stress increases cytoplasmic Ca activity in maize root protoplasts. Plant Physiol. 1989;90:1271–1274. doi:10.1104/pp.90.4.1271.
  • Knight H, Trewavas AJ, Knight MRJTPC. Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant J. 1996;8:489–503.
  • Steinhorst L, Kudla J. Signaling in cells and organisms—calcium holds the line. Curr Opin Plant Biol. 2014;22:14–21. doi:10.1016/j.pbi.2014.08.003.
  • Boudsocq M, Sheen J. Stress signaling II: calcium sensing and signaling. Abiotic Stress Adaptation in Plants.Dordrecht: Springer; 2009. p. 75–90. doi:10.1007/978-90-481-3112-9_4.
  • Wan S, Wang W, Zhou T, Zhang Y, Chen J, Xiao B, Yang Y, Yu Y. Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress. Plant Growth Regul. 2018;84:481–492. doi:10.1007/s10725-017-0354-4.
  • Fasani E, DalCorso G, Costa A, Zenoni S, Furini AJPMB. The Arabidopsis thaliana transcription factor MYB59 regulates calcium signalling during plant growth and stress response. Plant Mol Biol. 2019;99:517–534.
  • Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ, Goloubinoff P. The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell. 2009;21:2829–2843. doi:10.1105/tpc.108.065318.
  • Stephan AB, Kunz -H-H, Yang E, Schroeder J. Rapid hyperosmotic-induced Ca2+ responses in Arabidopsis thaliana exhibit sensory potentiation and involvement of plastidial KEA transporters. Proc Natl Acad Sci U S A. 2016;113:E5242–E9. doi:10.1073/pnas.1519555113.
  • Wilkins KA, Matthus E, Swarbreck SM, Davies J. Calcium-mediated abiotic stress signaling in roots. Front Plant Sci. 2016;7:1296. doi:10.3389/fpls.2016.01296.
  • Knight H, Trewavas AJ, Knight MRJTPJ. Calcium signalling in Arabidopsis thaliana responding to drought and salinity. Plant J. 1997;12:1067–1078. doi:10.1046/j.1365-313x.1997.12051067.x.
  • Tracy FE, Gilliham M, Dodd AN, Webb AA, Tester MJP. cell, environment. NaCl‐induced changes in cytosolic free Ca2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell Environ. 2008;31:1063–1073. doi:10.1111/j.1365-3040.2008.01817.x.
  • Miseta A, Kellermayer R, Aiello DP, Fu L, Bedwell D. The vacuolar Ca2+/H+ exchanger Vcx1p/Hum1p tightly controls cytosolic Ca2+ levels in S. cerevisiae. FEBS Lett. 1999;451:132–136. doi:10.1016/s0014-5793(99)00519-0.
  • Chakraborty K, Basak N, Bhaduri D, Ray S, Vijayan J, Chattopadhyay K, Sarkar RK. Ionic basis of salt tolerance in plants: nutrient homeostasis and oxidative stress tolerance. Plant Nutrients and Abiotic Stress Tolerance.Singapore: Springer; 2018. p. 325–362. doi:10.1007/978-981-10-9044-8_14.
  • Sze H, Liang F, Hwang I, Curran AC, Harper J. Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:433–462. doi:10.1146/annurev.arplant.51.1.433.
  • Yokoi S, Bressan RA, Hasegawa P. Salt stress tolerance of plants. JIRCAS. 2002;23:25–33.
  • Munns R, James RA, Läuchli A. Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot. 2006;57:1025–1043. doi:10.1093/jxb/erj100.
  • Flowers T, Koyama M, Flowers S, Sudhakar C, Singh K, Yeo A. QTL: their place in engineering tolerance of rice to salinity. J Exp Bot. 2000;51:99–106.
  • Luan S, Lan W, Lee S. Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL–CIPK network. Curr Opin Cell Biol. 2009. Vol. 12. p. 339–346.
  • Tuteja N. Mechanisms of high salinity tolerance in plants. Methods in enzymology. Elsevier; 2007. Vol.428. p. 419–438. doi:10.1016/S0076-6879(07)28024-3.
  • Nikalje CG, Nikam DT, Suprasanna P. Looking at halophytic adaptation to high salinity through genomics landscape. Curr Genomics. 2017;18:542–552. doi:10.2174/1389202918666170228143007.
  • Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C, Zhang J, Theprungsirikul L, Shrift T, Krichilsky B, Johnson DM. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature. 2014;514:367–371.
  • Chinnusamy V, Jagendorf A, Zhu J-KJCS. Understanding and improving salt tolerance in plants. Crop Sci. 2005;45:437–448. doi:10.2135/cropsci2005.0437.
  • Lv S, Jiang P, Tai F, Wang D, Feng J, Fan P, Bao H, Li Y. The V-ATPase subunit A is essential for salt tolerance through participating in vacuolar Na+ compartmentalization in Salicornia europaea. Planta. 2017;246:1177–1187. doi:10.1007/s00425-017-2762-0.
  • Choi W-G, Toyota M, Kim S-H, Hilleary R, Gilroy S. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci. 2014;111:6497–6502. doi:10.1073/pnas.1319955111.
  • Ben-Johny M, Dick EI, Sang L, Limpitikul BW, Wei KP, Niu J, Banerjee R, Yang W, Babich JS, Issa JB, et al. Towards a unified theory of calmodulin regulation (calmodulation) of voltage-gated calcium and sodium channels. Curr Mol Pharmacol. 2015;8:188–205.
  • Yu Q, An L, Li W. The CBL–CIPK network mediates different signaling pathways in plants. Plant Cell Rep. 2014;33:203–214. doi:10.1007/s00299-013-1507-1.
  • Lan W-Z, Wang W, Wang S-M, Li L-G, Buchanan BB, Lin H-X, Gao JP, Luan S. A rice high-affinity potassium transporter (HKT) conceals a calcium-permeable cation channel. Proc Natl Acad Sci USA. 2010;107 (15):7089–7094. doi:10.1073/pnas.1000698107.
  • Schachtman DP, Schroeder JIJN. Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature. 1994;370:655. doi:10.1038/370655a0.
  • Wang TT, Ren ZJ, Liu ZQ, Feng X, Guo RQ, Li BG, Li L-G, Jing H-C. SbHKT1; 4, a member of the high‐affinity potassium transporter gene family from Sorghum bicolor, functions to maintain optimal Na+/K+ balance under Na+ stress. J Integr Plant Biol. 2014;56:315–332. doi:10.1111/jipb.12144.
  • Amtmann A, Sanders D. Mechanisms of Na+ uptake by plant cells. Advances in botanical research. 1998;29:75–112. doi:10.1016/S0065-2296(08)60310-9.
  • Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem WJTPC. Calmodulins and calcineurin B–like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell. 2002;14:S389–S400. doi:10.1105/tpc.001115.
  • Zhang X, Wang T, Liu M, Sun W, W-HJE Z, Botany E. Calmodulin-like gene MtCML40 is involved in salt tolerance by regulating MtHKTs transporters in medicago truncatula. Environ Exp Bot. 2019;157:79–90. doi:10.1016/j.envexpbot.2018.09.022.
  • Huang Y, Guan C, Liu Y, Chen B, Yuan S, Cui X, Zhang Y, Yang F. Enhanced growth performance and salinity tolerance in transgenic switchgrass via overexpressing vacuolar Na+ (K+)/H+ antiporter gene (PvNHX1). Front Plant Sci. 2017;8:458.
  • Li N, Wang X, Ma B, Du C, Zheng L, Wang Y. Expression of a Na+/H+ antiporter RtNHX1 from a recretohalophyte reaumuria trigyna improved salt tolerance of transgenic Arabidopsis thaliana. J Plant Physiol. 2017;218:109–120. doi:10.1016/j.jplph.2017.07.015.
  • Khan MS, Ahmad D, Khan MA. Trends in genetic engineering of plants with (Na+/H+) antiporters for salt stress tolerance. Biotechnol Biotechnol Equip. 2015;29:815–825. doi:10.1080/13102818.2015.1060868.
  • Bassil E, Ohto M-A, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E. The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell. 2011, 23(1):224–239 .
  • Hasegawa PM, Bressan RA, Zhu J-K, Bohnert H. Plant cellular and molecular responses to high salinity. Plant Physiol Plant Mol Biol. 2000;51:463–499. doi:10.1146/annurev.arplant.51.1.463.
  • Munns R, Tester MJARPB. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 2008;59:651–681. doi:10.1146/annurev.arplant.59.032607.092911.
  • Epstein EJPP. The essential role of calcium in selective cation transport by plant cells. Plant Physiol. 1961;36:437. doi:10.1104/pp.36.4.437.
  • Kramer G, Lynch J, Epstein EJPP. Influx of Na, K and Ca into roots of saltstressed cotton seedlings. Plant Physiol. 1987;83:510–516. doi:10.1104/pp.83.3.510.
  • Liu J, Zhu J-KJS. A calcium sensor homolog required for plant salt tolerance. Science. 1998;280:1943–1945. doi:10.1126/science.280.5371.1943.
  • Liu J, Ishitani M, Halfter U, Kim C-S, Zhu J-K. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA. 2000. 97:3730–3734.
  • Shi H, Ishitani M, Kim C, Zhu J-K. The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci. 2000;97:6896–6901. doi:10.1073/pnas.120170197.
  • Matsumoto TK, Ellsmore AJ, Cessna SG, Low PS, Pardo JM, Bressan RA, Hasegawa PM. An osmotically induced cytosolic Ca2+ transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance of Saccharomyces cerevisiae. J Biol Chem. 2002;277:33075–33080. doi:10.1074/jbc.M205037200.
  • Mansouri M, Naghavi MR, Alizadeh H, Mohammadi-Nejad G, Mousavi SA, Salekdeh GH, Tada Y. Transcriptomic analysis of aegilops tauschii during long-term salinity stress. Funct Integr Genomics. 2019;19:13–28. doi:10.1007/s10142-018-0623-y.
  • Batistic O, Kudla JJP. Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta. 2004;219:915–924. doi:10.1007/s00425-004-1333-3.
  • Zhao X, Wei P, Liu Z, Yu B, Shi H. Soybean Na+/H+ antiporter GmsSOS1 enhances antioxidant enzyme activity and reduces Na+ accumulation in Arabidopsis and yeast cells under salt stress. Acta Physiol Plant. 2017;39:19. doi:10.1007/s11738-016-2323-3.
  • Feki K, Tounsi S, Masmoudi K, Brini F. The durum wheat plasma membrane Na+/H+ antiporter SOS1 is involved in oxidative stress response. Protoplasma. 2017;254:1725–1734. doi:10.1007/s00709-016-1066-8.
  • Kumari PH, Kumar SA, Sivan P, Katam R, Suravajhala P, Rao K, Varshney RK, Kishor PBK. Overexpression of a plasma membrane bound Na+/H+ antiporter-like protein (SbNHXLP) confers salt tolerance and improves fruit yield in tomato by maintaining ion homeostasis. Front Plant Sci. 2017;7:2027. doi:10.3389/fpls.2016.02027.
  • Qiu Q-S, Guo Y, Dietrich MA, Schumaker KS, Zhu J-K. Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci. 2002;99:8436–8441. doi:10.1073/pnas.122224699.
  • Cheng N-H, Pittman JK, Zhu J-K, Hirschi K. The protein kinase SOS2 activates the Arabidopsis H+/Ca2+ antiporter CAX1 to integrate calcium transport and salt tolerance. J Biol Chem. 2004;279:2922–2926. doi:10.1074/jbc.M309084200.
  • Zhu J-K. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol. 2002;53:247–273. doi:10.1146/annurev.arplant.53.091401.143329.
  • Zhu J-K. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol. 2003;6:441–445.
  • Türkan I, Demiral TJE, Botany E. Recent developments in understanding salinity tolerance. Environmental and Experimental Botany 2009;67:2–9.
  • Hu DG, Ma QJ, Sun CH, Sun MH, You CX, Hao YJ. Overexpression of MdSOS2L1, a CIPK protein kinase, increases the antioxidant metabolites to enhance salt tolerance in apple and tomato. Physiol Plant. 2016;156:201–214. doi:10.1111/ppl.12354.
  • Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez‐Solis JR, Schültke S, Lee SC, Kudla J, Luan S. The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 2007;52:473–484. doi:10.1111/j.1365-313X.2007.03249.x.
  • Albrecht V, Weinl S, Blazevic D, D’angelo C, Batistic O, Kolukisaoglu Ü, Bock R, Schulz B, Harter K, Kudla J. The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J. 2003;36:457–470. doi:10.1046/j.1365-313x.2003.01892.x.
  • Cheong YH, Kim K-N, Pandey GK, Gupta R, Grant JJ, Luan SJTPC. CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell. 2003;15:1833–1845. doi:10.1105/tpc.012393.
  • Pandey GK, Cheong YH, Kim K-N, Grant JJ, Li L, Hung W, D’Angelo C, Weinl S, Kudla J, Luan S. The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell. 2004;16:1912–1924. doi:10.1105/tpc.021311.
  • Apse MP, Aharon GS, Snedden WA, Blumwald EJS. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science. 1999;285:1256–1258. doi:10.1126/science.285.5431.1256.
  • Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo JM, Guo Y. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell. 2007;19:1415–1431. doi:10.1105/tpc.106.042291.
  • Lin H, Yang Y, Quan R, Mendoza I, Wu Y, Du W, Zhao S, Schumaker KS, Pardo JM, Guo Y. Phosphorylation of SOS3-LIKE CALCIUM BINDING PROTEIN8 by SOS2 protein kinase stabilizes their protein complex and regulates salt tolerance in Arabidopsis. Plant Cell. 2009;21:1607–1619. doi:10.1105/tpc.109.066217.
  • Ren XL, Qi GN, Feng HQ, Zhao S, Zhao SS, Wang Y, Wu W-H. Calcineurin B‐like protein CBL 10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis. Plant J. 2013;74:258–266. doi:10.1111/tpj.12123.
  • Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, Lo AC, D’Hooge R, Steer CJ, Thibodeau SN, et al. CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics. 2013;14:216. doi:10.1186/1471-2164-14-181.
  • Yoo JH, Park CY, Kim JC, Do Heo W, Cheong MS, Park HC, Kim MC, Moon BC, Choi MS, Kang YH, et al. Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. J Biol Chem. 2005;280:3697–3706. doi:10.1074/jbc.M408237200.
  • Huang DW, Sherman BT, Lempicki R. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2008;4:44. doi:10.1038/nprot.2008.211.
  • Aliniaeifard S, van Meeteren U. Can prolonged exposure to low VPD disturb the ABA signalling in stomatal guard cells? J Exp Bot. 2013;64:3551–3566. doi:10.1093/jxb/ert192.
  • Wang W-H, Yi X-Q, Han A-D, Liu T-W, Chen J, Wu F-H, Dong X-J, He J-X, Pei Z-M, Zheng H-L. Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J Exp Bot. 2011;63:177–190. doi:10.1093/jxb/err259.
  • McAinsh MR, Evans NH, Montgomery LT, North KA. Calcium signalling in stomatal responses to pollutants. New Phytol. 2002;153:441–447. doi:10.1046/j.0028-646X.2001.00336.x.
  • Monihan SM, Ryu C-H, Magness CA, Schumaker K. Linking duplication of a calcium sensor to salt tolerance in Eutrema salsugineum. Plant Physiol. 2018;2019:01400.
  • Aliniaeifard S, Hajilou J, Tabatabaei SJ, Sifi-Kalhor M. Effects of ascorbic acid and reduced glutathione on the alleviation of salinity stress in olive plants. Int J Fruit Sci. 2016;16:395–409. doi:10.1080/15538362.2015.1137533.
  • Tester M, Davenport R. Na+ tolerance and Na+ transport in higher plants. Ann Bot. 2003;91:503–527. doi:10.1093/aob/mcg058.
  • Sathee L, Sairam RK, Chinnusamy V, Jha S. Differential transcript abundance of salt overly sensitive (SOS) pathway genes is a determinant of salinity stress tolerance of wheat. Acta Physiol Plant. 2015;37:169. doi:10.1007/s11738-015-1910-z.
  • Nakamura T, Liu Y, Hirata D, Namba H, Harada S-I, Hirokawa T, Miyakawa T. Protein phosphatase type 2B (calcineurin)‐mediated, FK506‐sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. Embo J. 1993;12:4063–4071.
  • Mehlmer N, Wurzinger B, Stael S, Hofmann‐Rodrigues D, Csaszar E, Pfister B, Bayer R, Teige M. The Ca(2+</sup>++) -dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. Plant J. 2010;63:484–498. doi:10.1111/j.1365-313X.2010.04257.x.
  • Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J. WRKY transcription factors in plant responses to stresses. J Integr Plant Biol. 2017;59:86–101. doi:10.1111/jipb.12513.
  • Park CY, Lee JH, Yoo JH, Moon BC, Choi MS, Kang YH, Lee SM, Kim HS, Kang KY, Chung WS, et al. WRKY group IId transcription factors interact with calmodulin. FEBS Lett. 2005;579:1545–1550. doi:10.1016/j.febslet.2005.01.057.
  • Yan H, Jia H, Chen X, Hao L, An H, Guo XJP The cotton WRKY transcription factor GhWRKY17 functions in drought and salt stress in transgenic nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol. 2014;55:2060–2076. doi:10.1093/pcp/pcu133.
  • Jiang Y, Deyholos M. Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol. 2009;69:91–105. doi:10.1007/s11103-008-9408-3.
  • Eulgem T, Somssich I. Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol. 2007;10:366–371. doi:10.1016/j.pbi.2007.04.020.
  • Fan X-D, Wang J-Q, Yang N, Dong -Y-Y, Liu L, Wang F-W, Wang N, Chen H, Liu W-C, Sun Y-P, et al. Gene expression profiling of soybean leaves and roots under salt, saline–alkali and drought stress by high-throughput illumina sequencing. Gene. 2013;512:392–402. doi:10.1016/j.gene.2012.09.100.
  • Pathak MR, Teixeira Da Silva JA, Wani SH. Polyamines in response to abiotic stress tolerance through transgenic approaches. GM Crops Food. 2014;5:87–96. doi:10.4161/gmcr.28774.
  • Gupta K, Dey A, Gupta B. Plant polyamines in abiotic stress responses. Acta Physiol Plant. 2013;35:2015–2036. doi:10.1007/s11738-013-1239-4.
  • Chen D, Shao Q, Yin L, Younis A, Zheng B. Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci. 2018;9:1945. doi: 10.3389/fpls.2018.01945.
  • Gill SS, Tuteja N. Polyamines and abiotic stress tolerance in plants. Plant Signal Behav. 2010;5:26–33. doi:10.4161/psb.5.1.10291.
  • Shi H, Chan Z. Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Integr Plant Biol. 2014;56:114–121. doi:10.1111/jipb.12128.
  • Liu J, Nakajima I, Moriguchi T. Effects of salt and osmotic stresses on free polyamine content and expression of polyamine biosynthetic genes in Vitis vinifera. Biol. Plant. 2011;55:340–344. doi:10.1007/s10535-011-0050-6.
  • Liu J-H, Nada K, Honda C, Kitashiba H, Wen X-P, Pang X-M, Moriguchi T. Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. J Exp Bot. 2006;57:2589–2599. doi:10.1093/jxb/erl018.
  • Do PT, Drechsel O, Heyer AG, Hincha DK, Zuther E. Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: a comparison with responses to drought. Front Plant Sci. 2014;5:182. doi:10.3389/fpls.2014.00182.
  • Eom SH, Lee JK, Kim D-H, Kim H, Jang K-I, Ryu H, Hyun TK. Identification and expression profiling of flax (Linum usitatissimum L.) polyamine oxidase genes in response to stimuli. Acta Bot Croat. 2018;77:97–101. doi:10.1515/botcro-2017-0022.
  • Seifikalhor M, Aliniaeifard S, Hassani B, Niknam V, Lastochkina O. Diverse role of γ-aminobutyric acid in dynamic plant cell responses. Plant Cell Rep. 2019;30:847–867. doi:10.1007/s00299-019-02396-z.
  • Marco F, Alcazar R, Tiburcio AF, Carrasco P. Interactions between polyamines and abiotic stress pathway responses unraveled by transcriptome analysis of polyamine overproducers. OMICS. 2011;15:775–781. doi:10.1089/omi.2011.0084.
  • Kalhor MS, Aliniaeifard S, Seif M, Asayesh EJ, Bernard F, Hassani B, Li T. Title: enhanced salt tolerance and photosynthetic performance: implication of ɤ-amino butyric acid application in salt-exposed lettuce (Lactuca sativa L.) plants. Plant Physiol Biochem. 2018;130:157–172. doi:10.1016/j.plaphy.2018.07.003.
  • Zhao F, Song C-P, He J, Zhu H. Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol. 2007;145:1061–1072. doi:10.1104/pp.107.105882.
  • Velarde-Buendía AM, Shabala S, Cvikrova M, Dobrovinskaya O, Pottosin I. Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines. Plant Physiol Biochem. 2012;61:18–23. doi:10.1016/j.plaphy.2012.09.002.
  • Garufi A, Visconti S, Camoni L, Aducci P. Polyamines as physiological regulators of 14-3-3 interaction with the plant plasma membrane H+-ATPase. Plant Cell Physiol. 2007;48:434–440. doi:10.1093/pcp/pcm010.
  • Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B. Polyamines as redox homeostasis regulators during salt stress in plants. Front. Environ. Sci. 2015;3:21. doi:10.3389/fenvs.2015.00021.
  • Shabala S, Cuin TA, Pottosin I. Polyamines prevent NaCl‐induced K+ efflux from pea mesophyll by blocking non‐selective cation channels. FEBS Lett. 2007;581:1993–1999. doi:10.1016/j.febslet.2007.04.032.
  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta. 2010;231:1237–1249. doi:10.1007/s00425-010-1130-0.
  • Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R, Bose J, Shabala S, Muñiz-Murguía J, Pottosin II. Polyamines interact with hydroxyl radicals in activating Ca(2+++) and K(+) transport across the root epidermal plasma membranes. Plant Physiol. 2011;157:2167–2180. doi:10.1104/pp.111.179671.
  • Pottosin I, Velarde-Buendía AM, Bose J, Fuglsang AT, Shabala S. Polyamines cause plasma membrane depolarization, activate Ca2+-, and modulate H+-ATPase pump activity in pea roots. J Exp Bot. 2014;65:2463–2472. doi:10.1093/jxb/eru133.
  • Pottosin I, Shabala S. Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci. 2014;5:154. doi:10.3389/fpls.2014.00154.
  • Pottosin I, Velarde-Buendía A-M, Zepeda-Jazo I, Dobrovinskaya O, Shabala S. Synergism between polyamines and ROS in the induction of Ca2+ and K+ fluxes in roots. Plant Signal Behav. 2012;7:1084–1087. doi:10.4161/psb.21185.
  • Pottosin I, Velarde-Buendía AM, Bose J, Zepeda-Jazo I, Shabala S, Dobrovinskaya O. Cross-talk between reactive oxygen species and polyamines in regulation of ion transport across the plasma membrane: implications for plant adaptive responses. J Exp Bot. 2014;65:1271–1283. doi:10.1093/jxb/ert423.
  • Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S. Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide. 2018;73:22–38. doi:10.1016/j.niox.2017.12.005.
  • Lombardo MC, Lamattina L. Abscisic acid and nitric oxide modulate cytoskeleton organization, root hair growth and ectopic hair formation in Arabidopsis. Nitric Oxide. 2018;80:89–97. doi:10.1016/j.niox.2018.09.002.
  • He J, Ren Y, Chen X, Chen H. Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf. 2014;108:114–119. doi:10.1016/j.ecoenv.2014.05.021.
  • Wang P, Du Y, Hou Y-J, Zhao Y, Hsu -C-C, Yuan F, Zhu X, Tao WA, Song C-P, Zhu J-K. Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A. 2015;112:613–618. doi:10.1073/pnas.1423481112.
  • Khurana A, Kumar R, Babbar SB. Nitric oxide is involved in salicylic acid-induced flowering of lemna aequinoctialis welw. Acta Physiol Plant. 2014;36:2827–2833. doi:10.1007/s11738-014-1600-2.
  • Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R. Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot. 2015;66:2877–2887. doi:10.1093/jxb/erv051.
  • Wang W, Sheng X, Shu Z, Li D, Pan J, Ye X, Chang P, Li X, Wang Y. Combined cytological and transcriptomic analysis reveals a nitric oxide signaling pathway involved in cold-inhibited camellia sinensis pollen tube growth. Front Plant Sci. 2016;7:456.
  • Siddiqui MH, Al-Whaibi MH, Basalah MO. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma. 2011;248:447–455. doi:10.1007/s00709-010-0206-9.
  • Xu Y, Sun X, Jin J, Zhou H. Protective effect of nitric oxide on light-induced oxidative damage in leaves of tall fescue. J Plant Physiol. 2010;167:512–518. doi:10.1016/j.jplph.2009.10.010.
  • Puyaubert J, Baudouin E. New clues for a cold case: nitric oxide response to low temperature. Plant Cell Environ. 2014;37:2623–2630. doi:10.1111/pce.12329.
  • Hasanuzzaman M, Nahar K, Alam MM, Fujita M. Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci. 2012;6:1314.
  • París R, Lamattina L, Casalongué CA. Nitric oxide promotes the wound-healing response of potato leaflets. Plant Physiolo Biochem. 2007;45:80–86. doi:10.1016/j.plaphy.2006.12.001.
  • Ahmad P, Abdel Latef AA, Hashem A, Abd_Allah EF, Gucel S, Tran L-SP. Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci. 2016;7:347. doi:10.3389/fpls.2016.00347.
  • Wimalasekera R, Tebartz F, Scherer GF. Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci. 2011;181:593–603. doi:10.1016/j.plantsci.2011.04.002.
  • Santolini J, André F, Jeandroz S, Wendehenne D. Nitric oxide synthase in plants: where do we stand? Nitric Oxide. 2017;63:30–38. doi:10.1016/j.niox.2016.09.005.
  • Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF. AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J Biol Chem. 2008;283:32957–32967. doi:10.1074/jbc.M804838200.
  • Domingos P, Prado AM, Wong A, Gehring C, Feijo JA. Nitric oxide: a multitasked signaling gas in plants. Mol Plant. 2015;8:506–520. doi:10.1016/j.molp.2014.12.010.
  • Weidinger A, Kozlov A. Biological activities of reactive oxygen and nitrogen species: oxidative stress versus signal transduction. Biomolecules. 2015;5:472–484. doi:10.3390/biom5020472.
  • Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O. Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot. 2015;66:2857–2868. doi:10.1093/jxb/erv213.
  • Khan MN, Mohammad F, Mobin M, Saqib MA. Tolerance of plants to abiotic stress: a role of nitric oxide and calcium. Nitric oxide in plants: metabolism and role in stress physiology.Cham: Springer; 2014. p. 225–242. doi:10.1007/978-3-319-06710-0_14.
  • Courtois C, Besson A, Dahan J, Bourque S, Dobrowolska G, Pugin A, Wendehenne D. Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J Exp Bot. 2008;59:155–163. doi:10.1093/jxb/erm197.
  • Niu L, Yu J, Liao W, Yu J, Zhang M, Dawuda MM. Calcium and calmodulin are involved in nitric oxide-induced adventitious rooting of cucumber under simulated osmotic stress. Front Plant Sci. 2017;8:1684. doi:10.3389/fpls.2017.01684.
  • Ma W, Smigel A, Tsai Y-C, Braam J, Berkowitz GA. Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol. 2008;148:818–828. doi:10.1104/pp.108.125104.
  • Zaidi I, Ebel C, Belgaroui N, Ghorbel M, Amara I, Hanin M. The wheat MAP kinase phosphatase 1 alleviates salt stress and increases antioxidant activities in Arabidopsis. J Plant Physiol. 2016;193:12–21. doi:10.1016/j.jplph.2016.01.011.
  • Chen ZH, Wang Y, Wang JW, Babla M, Zhao C, García‐Mata C, Sani E, Differ C, Mak M, Hills A, et al. Nitrate reductase mutation alters potassium nutrition as well as nitric oxide‐mediated control of guard cell ion channels in Arabidopsis. New Phytol. 2016;209:1456–1469. doi:10.1111/nph.13714.
  • Laxalt AM, García-Mata C, Lamattina L. The dual role of nitric oxide in guard cells: promoting and attenuating the ABA and phospholipid-derived signals leading to the stomatal closure. Front Plant Sci. 2016;7:476. doi:10.3389/fpls.2016.00476.
  • Lamotte O, Courtois C, Dobrowolska G, Besson A, Pugin A, Wendehenne D. Mechanisms of nitric-oxide-induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radic Biol Med. 2006;40:1369–1376. doi:10.1016/j.freeradbiomed.2005.12.006.
  • Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, et al. Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol. 2004;136:2722–2733. doi:10.1104/pp.104.042812.
  • Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, Del Río LA. Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta. 2006;224:246–254. doi:10.1007/s00425-005-0205-9.
  • Khan MN, Siddiqui MH, Mohammad F, Naeem M. Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide. 2012;27:210–218. doi:10.1016/j.niox.2012.07.005.
  • Foyer CH, Noctor G. Redox signaling in plants. Antioxid Redox Signal. 2013;1;18(16):2087–2090. doi:10.1089/ars.2013.5278.
  • Liu S-L, Yang R-J, Ma M-D, Dan F, Zhao Y, Jiang P, Wang M-H. Effects of exogenous NO on the growth, mineral nutrient content, antioxidant system, and ATPase activities of Trifolium repens L. plants under cadmium stress. Acta Physiol Plant. 2015;37:1721. doi:10.1007/s11738-014-1721-7.
  • Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta. 2006;224:545–555. doi:10.1007/s00425-006-0242-z.
  • Mazid M, Khan TA, Mohammad F. Role of Nitric oxide in regulation of H2O2 mediating tolerance of plants to abiotic stress: A synergistic signaling approach. J. Stress Physiol. Biochem. 2011;34–74.
  • Sheokand S, Kumari A, Sawhney V. Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants. Physiol Mol Biol Plants. 2008;14:355–362. doi:10.1007/s12298-008-0034-y.
  • Hasanuzzaman M, Hossain MA, Fujita M. Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep. 2011;5:353. doi:10.1007/s11816-011-0189-9.
  • Kovacic P, Somanathan R. Integrated approach to nitric oxide in animals and plants (mechanism and bioactivity): cell signaling and radicals. J Recept Signal Transduct Res. 2011;31:111–120. doi:10.3109/10799893.2010.544317.
  • Wang H, Liang X, Wan Q, Wang X, Bi Y. Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta. 2009;230:293–307. doi:10.1007/s00425-009-0946-y.
  • Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol. 2004;134:849–857. doi:10.1104/pp.103.030023.
  • Pereira A. Plant abiotic stress challenges from the changing environment. Front Plant Sci. 2016;7:1123. doi:10.3389/fpls.2016.01123.
  • Singh M, Kumar J, Singh S, Singh VP, Prasad SM. Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Bio/Technol. 2015;14:407–426. doi:10.1007/s11157-015-9372-8.
  • Nahar K, Hasanuzzaman M, Fujita M. Roles of osmolytes in plant adaptation to drought and salinity. Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies.New Delhi: Springer; 2016. p. 37–68. doi:10.1007/978-81-322-2616-1_4.
  • Wutipraditkul N, Wongwean P, Buaboocha T. Alleviation of salt-induced oxidative stress in rice seedlings by proline and/or glycinebetaine. Biol. Plant. 2015;59:547–553. doi:10.1007/s10535-015-0523-0.
  • Awasthi R, Bhandari K, Nayyar H. Temperature stress and redox homeostasis in agricultural crops. Front Env Sci. 2015;3:11. doi:10.3389/fenvs.2015.00011.
  • Singh M, Kumar J, Singh S, Singh V, Prasad S, Singh M. Adaptation strategies of plants against heavy metal toxicity: a short review. Biochem Pharmacol (Los Angel). 2015;4:2167–2501. 1000161.
  • Chen H, Jiang J-G. Osmotic adjustment and plant adaptation to environmental changes related to drought and salinity. Environ Rev. 2010;18:309–319. doi:10.1139/A10-014.
  • Turan S, Cornish K, Kumar S. Salinity tolerance in plants: breeding and genetic engineering. Aust J Crop Sci. 2012;6:1337.
  • Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A. Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot. 2015;115:433–447. doi:10.1093/aob/mcu239.
  • Szabados L, Savoure A. Proline: a multifunctional amino acid. Trends Plant Sci. 2010;15:89–97. doi:10.1016/j.tplants.2009.11.009.
  • Rana V, Ram S, Nehra K. Review proline biosynthesis and its role in abiotic stress. IJAIR. 2017;6:2319–1473.
  • Joseph E, Radhakrishnan V, Mohanan K. A study on the accumulation of proline-an osmoprotectant amino acid under salt stress in some native rice cultivars of North Kerala, India. Universal J Agri Res. 2015;3:15–22.
  • Chen J, Zhang Y, Wang C, Lü W, Jin JB, Hua X. Proline induces calcium-mediated oxidative burst and salicylic acid signaling. Amino Acids. 2011;40:1473–1484. doi:10.1007/s00726-010-0757-2.
  • Rahman A, Nahar K, Hasanuzzaman M, Fujita M. Calcium supplementation improves Na+/K+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Front Plant Sci. 2016;7:609. doi:10.3389/fpls.2016.00609.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.