Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

A New Insight of Salt Stress Signaling in Plant

  • Park, Hee Jin (Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center) ;
  • Kim, Woe-Yeon (Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center) ;
  • Yun, Dae-Jin (Division of Applied Life Science (BK21 Plus Program), Plant Molecular Biology and Biotechnology Research Center)
  • Received : 2016.04.04
  • Accepted : 2016.05.16
  • Published : 2016.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Many studies have been conducted to understand plant stress responses to salinity because irrigation-dependent salt accumulation compromises crop productivity and also to understand the mechanism through which some plants thrive under saline conditions. As mechanistic understanding has increased during the last decades, discovery-oriented approaches have begun to identify genetic determinants of salt tolerance. In addition to osmolytes, osmoprotectants, radical detoxification, ion transport systems, and changes in hormone levels and hormone-guided communications, the Salt Overly Sensitive (SOS) pathway has emerged to be a major defense mechanism. However, the mechanism by which the components of the SOS pathway are integrated to ultimately orchestrate plant-wide tolerance to salinity stress remains unclear. A higher-level control mechanism has recently emerged as a result of recognizing the involvement of GIGANTEA (GI), a protein involved in maintaining the plant circadian clock and control switch in flowering. The loss of GI function confers high tolerance to salt stress via its interaction with the components of the SOS pathway. The mechanism underlying this observation indicates the association between GI and the SOS pathway and thus, given the key influence of the circadian clock and the pathway on photoperiodic flowering, the association between GI and SOS can regulate growth and stress tolerance. In this review, we will analyze the components of the SOS pathways, with emphasis on the integration of components recognized as hallmarks of a halophytic lifestyle.

Keywords

References

  1. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J., and Harberd, N.P. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91-94. https://doi.org/10.1126/science.1118642
  2. Adams, P., Nelson, D.E., Chmara, W., Bohnert, H.J., and Griffiths H. (1998). Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytol. 138, 171-190. https://doi.org/10.1046/j.1469-8137.1998.00111.x
  3. Ali, Z., Park, H.C., Ali, A., Oh, D.-H., Aman, R., Kropornicka, A., Hong, H., Choi, W., Chung, W.S., Kim, W.-Y., et al. (2012). TsHKT1;2, a HKT1 homolog from the extremophile Arabidopsis relative Thellungiella salsuginea, shows $K^+$ specificity in the presence of NaCl. Plant Physiol. 158, 1463-1474. https://doi.org/10.1104/pp.111.193110
  4. Andres, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639. https://doi.org/10.1038/nrg3291
  5. Ashley, M.K., Grant, M., and Grabov, A. (2006). Plant responses to potassium deficiencies: a role for potassium transport proteins. J. Exp. Bot. 57, 425-436. https://doi.org/10.1093/jxb/erj034
  6. Aukerman, M. J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15, 2730-2741. https://doi.org/10.1105/tpc.016238
  7. de Azevedo Neto, A.D., Prisco, J. T., Eneas-Filho, J., Abreu, C.E.B. de, and Gomes-Filho, E. (2006). Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salttolerant and salt-sensitive maize genotypes. Env. Exp. Bot. 56, 87-94. https://doi.org/10.1016/j.envexpbot.2005.01.008
  8. Bajguz, A., and Hayat, S. (2009). Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol. Biochem. 47, 1-8. https://doi.org/10.1016/j.plaphy.2008.10.002
  9. Balazadeh, S., Siddiqui, H., Allu, A.D., Matallana-Ramirez, L.P., Caldana, C., Mehrnia, M., Zanor, M.-I., Kohler, B., and Mueller-Roeber, B. (2010). A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during saltpromoted senescence. Plant J. 62, 250-264. https://doi.org/10.1111/j.1365-313X.2010.04151.x
  10. Barajas-Lopez, J. de D., Serrato, A.J., Cazalis, R., Meyer, Y., Chueca, A., Reichheld, J.P., and Sahrawy, M. (2011). Circadian regulation of chloroplastic f and m thioredoxins through control of the CCA1 transcription factor. J. Exp. Bot. 62, 2039-2051. https://doi.org/10.1093/jxb/erq394
  11. Barba-Espin, G., Clemente-Moreno, M.J., Alvarez, S., Garcia-Legaz, M.F., HernAndez, J.A., and Diaz-Vivancos, P. (2011). Salicylic acid negatively affects the response to salt stress in pea plants. Plant Biol. 13, 909-917. https://doi.org/10.1111/j.1438-8677.2011.00461.x
  12. BarragAn, V., Leidi, E.O., Andres, Z., Rubio, L., De Luca, A., FernAndez, J.A., Cubero, B., and Pardo, J.M. (2012). Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24,1127-1142. https://doi.org/10.1105/tpc.111.095273
  13. Batelli, G., Verslues, P.E., Agius, F., Qiu, Q., Fujii, H., Pan, S., Schumaker, K.S., Grillo, S., and Zhu, J.-K. (2007). SOS2 promotes salt tolerance in part by interacting with the vacuolar $H^+$- ATPase and upregulating its transport activity. Mol. Cell Biol. 27, 7781-7790. https://doi.org/10.1128/MCB.00430-07
  14. Bendix, C., Mendoza, J.M., Stanley, D.N., Meeley, R., and Harmon, F.G. (2013). The circadian clock-associated gene gigantea1 affects maize developmental transitions. Plant Cell Environ. 36, 1379-1390. https://doi.org/10.1111/pce.12067
  15. Bianco, C., and Defez, R. (2009). Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acidoverproducing Sinorhizobium meliloti strain. J. Exp. Bot. 60, 3097-3107. https://doi.org/10.1093/jxb/erp140
  16. Black, R. (1960). Effects of naci on the ion uptake and growth of Atriplex vesicaria Heward. Aust. J. Biol. Sci. 13, 249-266. https://doi.org/10.1071/BI9600249
  17. BlAzquez, M.A., Trenor, M., and Weigel, D. (2002). Independent control of gibberellin biosynthesis and flowering time by the circadian clock in Arabidopsis. Plant Physiol. 130, 1770-1775. https://doi.org/10.1104/pp.007625
  18. Bleecke, A.B., and Patterson, S.E. (1997). Last exit: senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9, 1169-1179. https://doi.org/10.1105/tpc.9.7.1169
  19. Blokhina, O., Virolainen, E., and Fagerstedt, K.V. (2003). Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91, 179-194. https://doi.org/10.1093/aob/mcf118
  20. Bohnert, H.J., and Jensen, R.G. (1996). Strategies for engineering water-stress tolerance in plants. Trends Biotechnol. 14, 89-97. https://doi.org/10.1016/0167-7799(96)80929-2
  21. Bohnert, H.J., and Cushman, J.C. (2000). The ice plant cometh: lessons in abiotic stress tolerance. J. Plant Growth Regul. 19, 334-346. https://doi.org/10.1007/s003440000033
  22. Bohnert, H.J., Nelson, D.E., and Jensen, R.G. (1995). Adaptations to environmental stresses. Plant Cell 7, 1099-1111. https://doi.org/10.1105/tpc.7.7.1099
  23. Cao, S., Ye, M., and Jiang, S. (2005). Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant Cell Rep. 24, 683-690. https://doi.org/10.1007/s00299-005-0061-x
  24. Cao, S., Jiang, S., and Zhang, R. (2006). The role of GIGANTEA gene in mediating the oxidative stress response and in Arabidopsis. Plant Growth Regul. 48, 261-270. https://doi.org/10.1007/s10725-006-0012-8
  25. Cao, S.Q., Song, Y.Q., and Su, L. (2007a). Freezing sensitivity in the gigantea mutant of Arabidopsis is associated with sugar deficiency. Biol. Plant 51, 359-362. https://doi.org/10.1007/s10535-007-0073-1
  26. Cao, W.-H., Liu, J., He, X.-J., Mu, R.-L., Zhou, H.-L., Chen, S.-Y., and Zhang, J.-S. (2007b). Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol. 143, 707-719.
  27. Cheong, M., and Yun, D.-J. (2007). Salt-stress signaling. J. Plant Biol. 50, 148-155. https://doi.org/10.1007/BF03030623
  28. Cheong, Y.H., Kim, K.-N., Pandey, G.K., Gupta, R., Grant, J.J., and Luan, S. (2003). CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15, 1833-1845. https://doi.org/10.1105/tpc.012393
  29. Chung, J.-S., Zhu, J.-K., Bressan, R.A., Hasegawa, P.M., and Shi, H. (2008). Reactive oxygen species mediate $Na^+$-induced SOS1 mRNA stability in Arabidopsis. Plant J. 53, 554-565.
  30. Covington, M.F., and Harmer, S.L. (2007). The circadian clock regulates auxin signaling and responses in Arabidopsis. PLoS One 5, e222.
  31. Covington, M., Maloof, J., Straume, M., Kay, S., and Harmer, S. (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130. https://doi.org/10.1186/gb-2008-9-8-r130
  32. Craig Plett, D., and Moller, I.S. (2010). $Na^+$ transport in glycophytic plants: what we know and would like to know. Plant Cell Env. 33, 612-626. https://doi.org/10.1111/j.1365-3040.2009.02086.x
  33. Cramer, G.R., and Jones, R.L. (1996). Osmotic stress and abscisic acid reduce cytosolic calcium activities in roots of Arabidopsis thaliana. Plant Cell Env. 19, 1291-1298. https://doi.org/10.1111/j.1365-3040.1996.tb00007.x
  34. Crepy, M., Yanovsky, M.J., and Casal, J.J. (2007). Blue rhythms between GIGANTEA and phytochromes. Plant Signal. Behav. 2, 530-532. https://doi.org/10.4161/psb.2.6.4744
  35. Dalchau, N., Baek, S.J., Briggs, H.M., Robertson, F.C., Dodd, A.N., Gardner, M.J., Stancombe, M.A., Haydon, M.J., Stan, G.-B., Goncalves, J.M., et al. (2011). The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc. Natl. Acad. Sci. USA 108, 5104-5109. https://doi.org/10.1073/pnas.1015452108
  36. Dassanayake, M., Oh, D.-H., Haas, J.S., Hernandez, A., Hong, H., Ali, S., Yun, D.-J., Bressan, R.A., Zhu, J.-K., Bohnert, H.J., et al. (2011). The genome of the extremophile crucifer Thellungiella parvula. Nat Genet. 43, 913-918. https://doi.org/10.1038/ng.889
  37. David, K.M., Armbruster, U., Tama, N., and Putterill, J. (2006). Arabidopsis GIGANTEA protein is post-transcriptionally regulated by light and dark. FEBS Lett. 580, 1193-1197. https://doi.org/10.1016/j.febslet.2006.01.016
  38. DeWald, D.B., Torabinejad, J., Jones, C.A., Shope, J.C., Cangelosi, A.R., Thompson, J.E., Prestwich, G.D., and Hama, H. (2001). Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol. 126, 759-769. https://doi.org/10.1104/pp.126.2.759
  39. Dietz, K.-J. (2003). Plant peroxiredoxins. Annu. Rev. Plant Biol. 54, 93-107. https://doi.org/10.1146/annurev.arplant.54.031902.134934
  40. Dodd, A.N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J.M., Millar, A.J., and Webb, A.A.R. (2005a). Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633. https://doi.org/10.1126/science.1115581
  41. Dodd, A.N., Love, J., and Webb, A.A.R. (2005b). The plant clock shows its metal: circadian regulation of cytosolic free $Ca^{2+}$. Trends Plant Sci. 10, 15-21. https://doi.org/10.1016/j.tplants.2004.12.001
  42. Dodd, A.N., Jakobsen, M.K., Baker, A.J., Telzerow, A., Hou, S.-W., Laplaze, L., Barrot, L., Scott Poethig, R., Haseloff, J., and Webb, A.A.R. (2006). Time of day modulates low-temperature $Ca^{2+}$ signals in Arabidopsis. Plant J. 48, 962-973. https://doi.org/10.1111/j.1365-313X.2006.02933.x
  43. Dodd, A.N., Gardner, M.J., Hotta, C.T., Hubbard, K.E., Dalchau, N., Love, J., Assie, J.-M., Robertson, F.C., Jakobsen, M.K., Goncalves, J., et al. (2007). The Arabidopsis circadian clock incorporates a cADPR-based feedback loop. Science 318, 1789-1792. https://doi.org/10.1126/science.1146757
  44. Dong, H., Zhen, Z., Peng, J., Chang, L., Gong, Q., and Wang, N.N. (2011). Loss of ACS7 confers abiotic stress tolerance by modulating ABA sensitivity and accumulation in Arabidopsis. J. Exp. Bot. 62, 4875-4887. https://doi.org/10.1093/jxb/err143
  45. Ducrocq, S., Madur, D., Veyrieras, J.-B., Camus-Kulandaivelu, L., Kloiber-Maitz, M., Presterl, T., Ouzunova, M., Manicacci, D., and Charcosset, A. (2008). Key impact of Vgt1 on flowering time adaptation in maize: Evidence from association mapping and ecogeographical information. Genetics 178, 2433-2437. https://doi.org/10.1534/genetics.107.084830
  46. Eimert, K., Wang, S.M., Lue, W.I., and Chen, J. (1995). Monogenic recessive mutations causing both late floral initiation and excess starch accumulation in Arabidopsis. Plant Cell 7, 1703-1712. https://doi.org/10.1105/tpc.7.10.1703
  47. Etchegaray, J.-P., Lee, C., Wade, P.A., and Reppert, S.M. (2003). Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421, 177-182. https://doi.org/10.1038/nature01314
  48. Farre, E.M., Harmer, S.L., Harmon, F.G., Yanovsky, M.J., and Kay, S.A. (2005). Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian clock. Curr. Biol. 15, 47-54. https://doi.org/10.1016/j.cub.2004.12.067
  49. Flowers, T.J. (2004). Improving crop salt tolerance. J. Exp. Bot. 55, 307-319. https://doi.org/10.1093/jxb/erh003
  50. Flowers, T.J., and Colmer, T.D. (2008). Salinity tolerance in halophytes. New Phytol. 179, 945-963. https://doi.org/10.1111/j.1469-8137.2008.02531.x
  51. Flowers, T.J., Troke, P.F., and Yeo, A.R. (1977). The mechanism of salt tolerance in halophytes. Annu. Rev. Plant Physiol. 28, 89-121. https://doi.org/10.1146/annurev.pp.28.060177.000513
  52. Flowers, T., Galal, H., and Bromham, L. (2010). Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct. Plant Biol. 37, 604-612. https://doi.org/10.1071/FP09269
  53. Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., Coupland, G., and Putterill, J. (1999). GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 18, 4679-4688. https://doi.org/10.1093/emboj/18.17.4679
  54. Fowler, S.G., Cook, D., and Thomashow, M.F. (2005). Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137, 961-968. https://doi.org/10.1104/pp.104.058354
  55. Fricke, W., Akhiyarova, G., Wei, W., Alexandersson, E., Miller, A., Kjellbom, P.O., Richardson, A., Wojciechowski, T., Schreiber, L., Veselov, D., et al. (2006). The short-term growth response to salt of the developing barley leaf. J. Exp. Bot. 57, 1079-1095. https://doi.org/10.1093/jxb/erj095
  56. Fujimori, T., Sato, E., Yamashino, T., and Mizuno, T. (2005). PRR5 (PSEUDO-RESPONSE REGULATOR 5) plays antagonistic roles to CCA1 (CIRCADIAN CLOCK-ASSOCIATED 1) in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 69, 426-430. https://doi.org/10.1271/bbb.69.426
  57. Gemes, K., Poor, P., HorvAth, E., Kolbert, Z., Szopko, D., Szepesi, A., and Tari, I. (2011). Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity. Physiol. Plant 142, 179-192. https://doi.org/10.1111/j.1399-3054.2011.01461.x
  58. Gepstein, S., Sabehi, G., Carp, M.-J., Hajouj, T., Nesher, M.F.O., Yariv, I., Dor, C., and Bassani, M. (2003). Large-scale identification of leaf senescence-associated genes. Plant J. 36, 629-642. https://doi.org/10.1046/j.1365-313X.2003.01908.x
  59. Ghassemi, F., Jakeman, A.J., and Nix, H.A. (1995). "Salinisation of land and water resources: Human causes, extent, management, and case studies," (Wallingford, England: CAB international).
  60. Gill, S.S., and Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909-930. https://doi.org/10.1016/j.plaphy.2010.08.016
  61. Graf, A., Schlereth, A., Stitt, M., and Smith, A.M. (2010). Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc. Natl. Acad. Sci. USA 107, 9458-9463 https://doi.org/10.1073/pnas.0914299107
  62. Hanikenne, M., Kroymann, J., Trampczynska, A., Bernal, M., Motte, P., Clemens, S., and Kramer, U. (2013). Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. PLoS Genet. 9, e1003707. https://doi.org/10.1371/journal.pgen.1003707
  63. Hao, L., Zhao, Y., Jin, D., Zhang, L., Bi, X., Chen, H., Xu, Q., Ma, C., and Li, G. (2012). Salicylic acid-altering Arabidopsis mutants response to salt stress. Plant Soil. 354, 81-95. https://doi.org/10.1007/s11104-011-1046-x
  64. Harmer, S.L. (2009). The circadian system in higher plants. Annu. Rev. Plant Biol. 60, 357-377. https://doi.org/10.1146/annurev.arplant.043008.092054
  65. Harmer, S.L., Hogenesch, J.B., Straume, M., Chang, H.-S., Han, B., Zhu, T., Wang, X., Kreps, J.A., and Kay, S.A. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113. https://doi.org/10.1126/science.290.5499.2110
  66. Hedrich, R., and Neher, E. (1987). Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles. Nature 329, 833-836. https://doi.org/10.1038/329833a0
  67. Hollister, J.D., Arnold, B.J., Svedin, E., Xue, K.S., Dilkes, B.P., and Bomblies, K. (2012). Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 8, e1003093. https://doi.org/10.1371/journal.pgen.1003093
  68. Hong, S., Kim, S.A., Guerinot, M.L., and McClung, C.R. (2013). Reciprocal interaction of the circadian clock with the iron homeostasis network in Arabidopsis. Plant Physiol. 161, 893-903. https://doi.org/10.1104/pp.112.208603
  69. HorvAth, E., Szalai, G., and Janda, T. (2007). Induction of abiotic stress tolerance by salicylic acid signaling. J. Plant Growth Regul. 26, 290-300. https://doi.org/10.1007/s00344-007-9017-4
  70. Hotta, C.T., Gardner, M.J., Baek, S.J., Suhita, D., and Webb, A.A.R. (2007). Modulation of environmental responses of plants by circadian clocks. Plant Cell Env. 30, 333-349. https://doi.org/10.1111/j.1365-3040.2006.01627.x
  71. Howell, S.H. (2013). Endoplasmic Reticulum Stress Responses in Plants. Annu. Rev. Plant Biol. 64, 477-499. https://doi.org/10.1146/annurev-arplant-050312-120053
  72. Huq, E., Tepperman, J.M., and Quail, P.H. (2000). GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 97, 9789-9794. https://doi.org/10.1073/pnas.170283997
  73. Jain, M., and Khurana, J.P. (2009). Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J. 276, 3148-3162. https://doi.org/10.1111/j.1742-4658.2009.07033.x
  74. Jayakannan, M., Bose, J., Babourina, O., Rengel, Z., and Shabala, S. (2013). Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced $K^+$ loss via a GORK channel. J. Exp. Bot. 64, 2255-2268. https://doi.org/10.1093/jxb/ert085
  75. Ji, H., Pardo, J.M., Batelli, G., Van Oosten, M.J., Bressan, R.A., and Li, X. (2013). The Salt Overly Sensitive (SOS) pathway: established and emerging roles. Mol. Plant. 6, 275-286. https://doi.org/10.1093/mp/sst017
  76. Jiang, X., Leidi, E.O., and Pardo, J.M. (2010). How do vacuolar NHX exchangers function in plant salt tolerance? Plant Signal Behav. 5, 792-795. https://doi.org/10.4161/psb.5.7.11767
  77. Jibran, R., Hunter, D., and Dijkwel, P. (2013). Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol. 82, 1-15. https://doi.org/10.1007/s11103-013-0031-6
  78. Jung, C., and Muller, A.E. (2009). Flowering time control and applications in plant breeding. Trends Plant Sci. 14, 563-573. https://doi.org/10.1016/j.tplants.2009.07.005
  79. Jung, J.-H., Seo, Y.-H., Seo, P.J., Reyes, J.L., Yun, J., Chua, N.-H., and Park, C.-M. (2007). The GIGANTEA-regulated MicroRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19, 2736-2748. https://doi.org/10.1105/tpc.107.054528
  80. Kar, R.K. (2011). Plant responses to water stress: Role of reactive oxygen species. Plant Signal. Behav. 6, 1741-1745. https://doi.org/10.4161/psb.6.11.17729
  81. Katiyar-Agarwal, S., Zhu, J., Kim, K., Agarwal, M., Fu, X., Huang, A., and Zhu, J.-K. (2006). The plasma membrane $Na^+$/$H^+$ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. USA 103, 18816-18821. https://doi.org/10.1073/pnas.0604711103
  82. Kawasaki, S., Borchert, C., Deyholos, M., Wang, H., Brazille, S., Kawai, K., Galbraith, D., and Bohnert, H.J. (2001). Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13, 889-905. https://doi.org/10.1105/tpc.13.4.889
  83. Kellermeier, F., Chardon, F., and Amtmann, A. (2013). Natural variation of Arabidopsis root architecture reveals complementing adaptive strategies to potassium starvation. Plant Physiol. 161, 1421-1432. https://doi.org/10.1104/pp.112.211144
  84. Kende, H., and Zeevaart, J.A. (1997). The five "classical" plant hormones. Plant Cell 9, 1197-1210. https://doi.org/10.1105/tpc.9.7.1197
  85. Ketchum, K., and Poole, R. (1991). Cytosolic calcium regulates a potassium current in corn (Zea mays) protoplasts. J. Membr. Biol. 119, 277-288. https://doi.org/10.1007/BF01868732
  86. Kidokoro, S., Maruyama, K., Nakashima, K., Imura, Y., Narusaka, Y., Shinwari, Z. K., Osakabe, Y., Fujita, Y., Mizoi, J., Shinozaki, K., et al. (2009). The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol. 151, 2046-2057. https://doi.org/10.1104/pp.109.147033
  87. Kim, B.-G., Waadt, R., Cheong, Y.H., Pandey, G.K., Dominguez-Solis, J.R., Schultke, S., Lee, S.C., Kudla, J., and Luan, S. (2007a). The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis. Plant J. 52, 473-484. https://doi.org/10.1111/j.1365-313X.2007.03249.x
  88. Kim, D.-W., Shibato, J., Agrawal, G.K., Fujihara, S., Iwahashi, H., Kim, D.H., Shim, I.-S., and Rakwal, R. (2007b). Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Mol. Cells 24, 45-59.
  89. Kim, W.-Y., Fujiwara, S., Suh, S.-S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H.G., and Somers, D.E. (2007c). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356-360. https://doi.org/10.1038/nature06132
  90. Kim, W.-Y., Salome, P.A., Fujiwara, S., Somers, D.E., and McClung, C.R. (2010). Chapter 19-Characterization of pseudo-response regulators in plants. In methods enzymol. Simon, Melvin I., Crane, Brian R., and Crane, Alexandrine eds., (Academic Press), pp. 357-378.
  91. Kim, Y., Yeom, M., Kim, H., Lim, J., Koo, H. J., Hwang, D., Somers, D., and Nam, H.G. (2012). GIGANTEA and EARLY FLOWERING 4 in Arabidopsis exhibit differential phase-specific genetic influences over a diurnal cycle. Mol. Plant 5, 678-687. https://doi.org/10.1093/mp/sss005
  92. Kim, W.-Y., Ali, Z., Park, H.J., Park, S.J., Cha, J.-Y., Perez-Hormaeche, J., Quintero, F.J., Shin, G., Kim, M.R., Qiang, Z., et al. (2013). Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat. Commun. 4, 1352. https://doi.org/10.1038/ncomms2357
  93. Kinnunen, P.K.J. (2000). Lipid bilayers as osmotic response elements. Cell. Physiol. Biochem. 10, 243-250. https://doi.org/10.1159/000016360
  94. Konig, S., Mosblech, A., and Heilmann, I. (2007). Stress-inducible and constitutive phosphoinositide pools have distinctive fatty acid patterns in Arabidopsis thaliana. FASEB J. 21, 1958-1967. https://doi.org/10.1096/fj.06-7887com
  95. Kopittke, P. (2012). Interactions between Ca, Mg, Na and K: alleviation of toxicity in saline solutions. Plant Soil. 352, 353-362. https://doi.org/10.1007/s11104-011-1001-x
  96. Krasensky, J., and Jonak, C. (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 63, 1593-1608. https://doi.org/10.1093/jxb/err460
  97. Krebs, M., Beyhl, D., Gorlich, E., Al-Rasheid, K.A.S., Marten, I., Stierhof, Y.-D., Hedrich, R., and Schumacher, K. (2010). Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc. Natl. Acad. Sci. USA 107, 3251-3256. https://doi.org/10.1073/pnas.0913035107
  98. Kreps, J.A., Wu, Y., Chang, H.-S., Zhu, T., Wang, X., and Harper, J.F. (2002). Transcriptome Changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129-2141. https://doi.org/10.1104/pp.008532
  99. Krishnamurthy, A., and Rathinasabapathi, B. (2013). Auxin and its transport play a role in plant tolerance to arsenite-induced oxidative stress in Arabidopsis thaliana. Plant Cell Env. 36, 1838-1849. https://doi.org/10.1111/pce.12093
  100. Kronzucker, H.J., and Britto, D.T. (2011). Sodium transport in plants: a critical review. New Phytol. 189, 54-81. https://doi.org/10.1111/j.1469-8137.2010.03540.x
  101. Kurepa, J., Smalle, J., Va, M., Montagu, N., and Inze, D. (1998). Oxidative stress tolerance and longevity in Arabidopsis: the lateflowering mutant gigantea is tolerant to paraquat. Plant J. 14, 759-764. https://doi.org/10.1046/j.1365-313x.1998.00168.x
  102. Lee, S.C., Lan, W.-Z., Kim, B.-G., Li, L., Cheong, Y.H., Pandey, G.K., Lu, G., Buchanan, B.B., and Luan, S. (2007). A protein phosphorylation/dephosphorylation network regulates a plant potassium channel. Proc. Natl. Acad. Sci. USA 104, 15959-15964. https://doi.org/10.1073/pnas.0707912104
  103. Legnaioli, T., Cuevas, J., and Mas, P. (2009). TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J. 28, 3745-3757. https://doi.org/10.1038/emboj.2009.297
  104. Li, K., Wang, Y., Han, C., Zhang, W., Jia, H., and Li, X. (2007). GA signaling and CO/FT regulatory module mediate salt-induced late flowering in Arabidopsis thaliana. Plant Growth Regul. 53, 195-206. https://doi.org/10.1007/s10725-007-9218-7
  105. Lim, P.O., Kim, H.J., and Nam, G.H. (2007). Leaf senescence. Annu. Rev. Plant Biol. 58, 115-136. https://doi.org/10.1146/annurev.arplant.57.032905.105316
  106. Liu, X., Zhai, S., Zhao, Y., Sun, B., Liu, C., Yang, A., and Zhang, J. (2013a). Overexpression of the phosphatidylinositol synthase gene (ZmPIS) conferring drought stress tolerance by altering membrane lipid composition and increasing ABA synthesis in maize. Plant Cell Environ. 36, 1037-1055. https://doi.org/10.1111/pce.12040
  107. Liu, D., Ford, K.L., Roessner, U., Natera, S., Cassin, A.M., Patterson, J.H., and Bacic, A. (2013b). Rice suspension cultured cells are evaluated as a model system to study salt responsive networks in plants using a combined proteomic and metabolomic profiling approach. Proteomics 13, 2046-2062 https://doi.org/10.1002/pmic.201200425
  108. Lutts, S., Kinet, J.M., and Bouharmont, J. (1995). Changes in plant response to NaCl during development of rice (Oryza sativa L.) varieties differing in salinity resistance. J. Exp. Bot. 46, 1843-1852. https://doi.org/10.1093/jxb/46.12.1843
  109. Ma, T., Wang, J., Zhou, G., Yue, Z., Hu, Q., Chen, Y., Liu, B., Qiu, Q., Wang, Z., Zhang, J., et al. (2013). Genomic insights into salt adaptation in a desert poplar. Nat. Commun. 4, 2797 https://doi.org/10.1038/ncomms3797
  110. Maas, E.V., and Hoffman, G.J. (1977). Crop salt tolerance-current assessment. J. Irrig. Drain. Div. 103, 115-134.
  111. Martinez-Atienza, J., Jiang, X., Garciadeblas, B., Mendoza, I., Zhu, J.-K., Pardo, J.M., and Quintero, F.J. (2007). Conservation of the salt overly sensitive pathway in rice. Plant Physiol. 143, 1001-1012.
  112. del Martinez-Ballesta, M.C., Silva, C., Lopez-Berenguer, C., Cabanero, F.J., and Carvajal, M. (2006). Plant aquaporins: new perspectives on water and nutrient uptake in saline environment. Plant Biol. 8, 535-546. https://doi.org/10.1055/s-2006-924172
  113. Mas, P., Kim, W.-Y., Somers, D.E., and Kay, S.A. (2003). Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature. 426, 567-570. https://doi.org/10.1038/nature02163
  114. Maxwell, B.B., Andersson, C.R., Poole, D.S., Kay, S.A., and Chory, J. (2003). HY5, Circadian Clock-Associated 1, and a cis-Element, DET1 Dark Response Element, mediate DET1 regulation of Chlorophyll a/b-Binding Protein 2 Expression. Plant Physiol. 133, 1565-1577. https://doi.org/10.1104/pp.103.025114
  115. McClung, C.R. (2011). "Chapter 4-The Genetics of Plant Clocks," in Adv. Genet., ed. Stuart Brody (Academic Press), pp. 105-139.
  116. McClung, C.R., and Davis, S.J. (2010). Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr. Biol. 20, R1086-R1092. https://doi.org/10.1016/j.cub.2010.10.035
  117. Michael, T.P., Breton, G., Hazen, S.P., Priest, H., Mockler, T.C., Kay, S.A., and Chory, J. (2008). A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol. 6, e225. https://doi.org/10.1371/journal.pbio.0060225
  118. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., and Mittler, R. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Env. 33, 453-467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
  119. Mittova, V., Tal, M., Volokita, M., and Guy, M. (2002). Salt stress induces up-regulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol. Plant 115, 393-400. https://doi.org/10.1034/j.1399-3054.2002.1150309.x
  120. Mizoguchi, T., Wright, L., Fujiwara, S., Cremer, F., Lee, K., Onouchi, H., Mouradov, A., Fowler, S., Kamada, H., Putterill, J., et al. (2005). Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17, 2255-2270. https://doi.org/10.1105/tpc.105.033464
  121. Munne-Bosch, S., and Alegre, L. (2004). Die and let live: leaf senescence contributes to plant survival under drought stress. Funct. Plant Biol. 31, 203-216. https://doi.org/10.1071/FP03236
  122. Munnik T., and Vermeer, J.E.M. (2010). Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ. 33, 655-669. https://doi.org/10.1111/j.1365-3040.2009.02097.x
  123. Munns, R. (2002). Comparative physiology of salt and water stress. Plant Cell Env. 25, 239-250. https://doi.org/10.1046/j.0016-8025.2001.00808.x
  124. Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytol. 167, 645-663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
  125. Munns, R., and Tester, M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
  126. Nagamiya, K., Motohashi, T., Nakao, K., Prodhan, S., Hattori, E., Hirose, S., Ozawa, K., Ohkawa, Y., Takabe, T., Takabe, T., et al. (2007). Enhancement of salt tolerance in transgenic rice expressing an Escherichia coli catalase gene, katE. Plant Biotechnol. Rep. 1, 49-55. https://doi.org/10.1007/s11816-007-0007-6
  127. Nakagami, H., Pitzschke, A., and Hirt, H. (2005). Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10, 339-346. https://doi.org/10.1016/j.tplants.2005.05.009
  128. Nakamichi, N., Kita, M., Ito, S., Sato, E., Yamashino, T., and Mizuno, T. (2005a). The Arabidopsis Pseudo-response Regulators, PRR5 and PRR7, coordinately play essential roles for circadian clock function. Plant Cell Physiol. 46, 609-619. https://doi.org/10.1093/pcp/pci061
  129. Nakamichi, N., Kita, M., Ito, S., Yamashino, T., and Mizuno, T. (2005b). PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. 46, 686-698. https://doi.org/10.1093/pcp/pci086
  130. Nakamichi, N., Kusano, M., Fukushima, A., Kita, M., Ito, S., Yamashino, T., Saito, K., Sakakibara, H., and Mizuno, T. (2009). Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol. 50, 447-462. https://doi.org/10.1093/pcp/pcp004
  131. Nawaz, K., Hussain, K., Majeed, A., Khan, F., Afghan, S., and Ali, K. (2010). Fatality of salt stress to plants : Morphological, physiological and biochemical aspects. Afr. J .Biotechnol. 9, 5475-5480.
  132. Nuccio, M.L., Rhodest, D., McNeil, S.D., and Hanson, A.D. (1999). Metabolic engineering of plants for osmotic stress resistance. Curr. Opin. Plant Biol. 2, 128-134. https://doi.org/10.1016/S1369-5266(99)80026-0
  133. Oh, D.-H., Lee, S.Y., Bressan, R.A., Yun, D.-J., and Bohnert, H.J. (2010). Intracellular consequences of SOS1 deficiency during salt stress. J. Exp. Bot. 61, 1205-1213. https://doi.org/10.1093/jxb/erp391
  134. Oh, D.-H., Hong, H., Lee, S.Y., Yun, D.-J., Bohnert, H.J., and Dassanayake, M. (2014). Genome Structures and Transcriptomes Signify Niche Adaptation for the Multiple-Ion-Tolerant Extremophyte Schrenkiella parvula. Plant Physiol. 164, 2123-2138. https://doi.org/10.1104/pp.113.233551
  135. Olias, R., Eljakaoui, Z., Li, J., De Morales, P. A., Carmen, M.-M.M., Pardo, J.M., and Belver, A. (2009). The plasma membrane $Na^+$/$H^+$ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of $Na^+$ between plant organs. Plant Cell Env. 32, 904-916. https://doi.org/10.1111/j.1365-3040.2009.01971.x
  136. Oliverio, K.A., Crepy, M., Martin-Tryon, E.L., Milich, R., Harmer, S.L., Putterill, J., Yanovsky, M.J., and Casal, J.J. (2007). GIGANTEA regulates phytochrome a-mediated photomorphogenesis independently of its role in the circadian clock. Plant Physiol. 144, 495-502. https://doi.org/10.1104/pp.107.097048
  137. Olszewski, N., Sun, T., and Gubler, F. (2002). Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14, S61-S80. https://doi.org/10.1105/tpc.010476
  138. Olszewski, N.E., West, C.M., Sassi, S.O., and Hartweck, L.M. (2010). O-GlcNAc protein modification in plants: evolution and function. Biochim. Biophys. Acta. 1800, 49-56. https://doi.org/10.1016/j.bbagen.2009.11.016
  139. Opdenakker, K., Remansemail, T., Vangronsveld, J., and Cuypers, A. (2012). Mitogen-activated protein (MAP) kinases in plant metal stress: regulation and responses in comparison to other biotic and abiotic stresses. Int. J. Mol. Sci. 13, 7828-7853. https://doi.org/10.3390/ijms13067828
  140. Paltiel, J., Amin, R., Gover, A., Ori, N., and Samach, A. (2006). Novel roles for GIGANTEA revealed under environmental conditions that modify its expression in Arabidopsis and Medicago truncatula. Planta 224, 1255-1268. https://doi.org/10.1007/s00425-006-0305-1
  141. Pardo, J.M. (2010). Biotechnology of water and salinity stress tolerance. Curr. Opin. Biotech. 21, 185-196. https://doi.org/10.1016/j.copbio.2010.02.005
  142. Park, D.H., Somers, D.E., Kim, Y.S., Choy, Y.H., Lim, H.K., Soh, M.S., Kim, H.J., Kay, S.A., and Nam, H.G. (1999). Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579-1582. https://doi.org/10.1126/science.285.5433.1579
  143. Park, H.J., Kim, W.-Y., and Yun, D.-J. (2013). A role for GIGANTEA: Keeping the balance between flowering and salinity stress tolerance. Plant Signal. Behav. 8, e24820. https://doi.org/10.4161/psb.24820
  144. Perales, M., and MAs, P. (2007). A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19, 2111-2123. https://doi.org/10.1105/tpc.107.050807
  145. Pyo, Y.J., Gierth, M., Schroeder, J.I., and Cho, M.H. (2010). Highaffinity $K^+$ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiol. 153, 863-875. https://doi.org/10.1104/pp.110.154369
  146. Qi, Z., and Spalding, E.P. (2004). Protection of plasma membrane $K^+$ transport by the salt overly sensitive1 $Na^+$/$H^+$ antiporter during salinity stress. Plant Physiol. 136, 2548-2555. https://doi.org/10.1104/pp.104.049213
  147. Qin, F., Kodaira, K.-S., Maruyama, K., Mizoi, J., Tran, L.-S. P., Fujita, Y., Morimoto, K., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2011). SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol. 157, 1900-1913. https://doi.org/10.1104/pp.111.187302
  148. Quintero, F. ., Ohta, M., Shi, H., Zhu, J.-K., and Pardo, J.M. (2002). Reconstitution in yeast of the Arabidopsis SOS signaling pathway for $Na^+$ homeostasis. Proc. Natl. Acad. Sci. USA 99, 9061-9066. https://doi.org/10.1073/pnas.132092099
  149. Rengel, Z. (1992). The role of calcium in salt toxicity. Plant Cell Env. 15, 625-632. https://doi.org/10.1111/j.1365-3040.1992.tb01004.x
  150. Riboni, M., Galbiati, M., Tonelli, C., and Conti, L. (2013). GIGANTEA enables drought escape response via abscisic aciddependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1. Plant Physiol. 162, 1706-1719. https://doi.org/10.1104/pp.113.217729
  151. Rivas-San Vicente, M., and Plasencia, J. (2011). Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62, 3321-3338. https://doi.org/10.1093/jxb/err031
  152. Rodrigo-Moreno, A., Poschenrieder, C., and Shabala, S. (2013). Transition metals: A double edge sward in ROS generation and signaling. Plant Signal. Behav. 8, e23425. https://doi.org/10.4161/psb.23425
  153. Rontein, D., Basset, G., and Hanson, A.D. (2002). Metabolic engineering of osmoprotectant accumulation in plants. Metab. Eng. 4, 49-56. https://doi.org/10.1006/mben.2001.0208
  154. Rosa, M., Prado, C., Podazza, G., Interdonato, R., GonzAlez, J.A., Hilal, M., and Prado, F.E. (2009). Soluble sugars: Metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal. Behav. 4, 388-393. https://doi.org/10.4161/psb.4.5.8294
  155. Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B., Matsumoto, T.K., Koiwa, H., Zhu, J.-K., Bressan, R.A., and Hasegawa, P. M. (2001). AtHKT1 is a salt tolerance determinant that controls $Na^+$ entry into plant roots. Proc. Natl. Acad. Sci. USA 98, 14150-14155. https://doi.org/10.1073/pnas.241501798
  156. Rus, A., Lee, B., Munoz-Mayor, A., Sharkhuu, A., Miura, K., Zhu, J.-K., Bressan, R.A., and Hasegawa, P.M. (2004). AtHKT1 facilitates $Na^+$ homeostasis and $K^+$ nutrition in planta. Plant Physiol. 136, 2500-2511. https://doi.org/10.1104/pp.104.042234
  157. Sahi, C., Singh, A., Kumar, K., Blumwald, E., and Grover, A. (2006). Salt stress response in rice: genetics, molecular biology, and comparative genomics. Funct. Integr. Genomics 6, 263-284. https://doi.org/10.1007/s10142-006-0032-5
  158. Sairam, R.K., and Tyagi, A. (2004). Physiology and molecular biology of salinity stress tolerance in plants. Curr. Sci. 86, 407-421.
  159. Sakamoto, A., and Murata, N. (2002). The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Env. 25, 163-171. https://doi.org/10.1046/j.0016-8025.2001.00790.x
  160. Salome, P.A., and McClung, C.R. (2005). PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of the Arabidopsis circadian clock. Plant Cell 17, 791-803. https://doi.org/10.1105/tpc.104.029504
  161. Salter, M.G., Franklin, K.A., and Whitelam, G.C. (2003). Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature. 426, 680-683. https://doi.org/10.1038/nature02174
  162. Sanders, D., Pelloux, J., Brownlee, C., and Harper, J.F. (2002). Calcium at the crossroads of signaling. Plant Cell 14, S401-S417. https://doi.org/10.1105/tpc.002899
  163. Sanchez, A., Shin, J., and Davis, S.J. (2011). Abiotic stress and the plant circadian clock. Plant Signal. Behav. 6, 223-231. https://doi.org/10.4161/psb.6.2.14893
  164. Sawa, M., and Kay, S.A. (2011). GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 108, 11698-11703. https://doi.org/10.1073/pnas.1106771108
  165. Sawa, M., Nusinow, D.A., Kay, S.A., and Imaizumi, T. (2007). FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318, 261-265. https://doi.org/10.1126/science.1146994
  166. Schaffer, R., Ramsay, N., Samach, A., Corden, S., Putterill, J., Carre, I.A., and Coupland, G. (1998). The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219-1229. https://doi.org/10.1016/S0092-8674(00)81465-8
  167. Sehgal, D., Rajaram, V., Armstead, I., Vadez, V., Yadav, Y., Hash, C., and Yadav, R. (2012). Integration of gene-based markers in a pearl millet genetic map for identification of candidate genes underlying drought tolerance quantitative trait loci. BMC Plant Biol. 12, 9. https://doi.org/10.1186/1471-2229-12-9
  168. Seo, P., Park, J.-M., Kang, S., Kim, S.-G., and Park, C.-M. (2011). An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233, 189-200. https://doi.org/10.1007/s00425-010-1293-8
  169. Seung, D., Risopatron, J., Jones, B., and Marc, J. (2012). Circadian clock-dependent gating in ABA signalling networks. Protoplasma 249, 445-457. https://doi.org/10.1007/s00709-011-0304-3
  170. Shabala, S., and Cuin, T.A. (2007). Potassium transport and plant salt tolerance. Physiol. Plant 133, 651-669.
  171. Shao, H.-B., Chu, L.-Y., Lu, Z.-H., and Kang, C.-M. (2008). Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells. Int. J. Biol. Sci. 4, 8-14.
  172. Shatil-Cohen, A., Attia, Z., and Moshelion, M. (2011). Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant J. 67, 72-80. https://doi.org/10.1111/j.1365-313X.2011.04576.x
  173. Shavrukov, Y. (2013). Salt stress or salt shock: which genes are we studying? J. Exp. Bot. 64, 119-127. https://doi.org/10.1093/jxb/ers316
  174. Shen, B., Jensen, R.G., and Bohnert, H.J. (1997). Mannitol protects against oxidation by hydroxyl radicals. Plant Physiol. 115, 527-532. https://doi.org/10.1104/pp.115.2.527
  175. Shi, H., Ishitani, M., Kim, C., and Zhu, J.-K. (2000). The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative $Na^+$/$H^+$ antiporter. Proc. Natl. Acad. Sci. USA 97, 6896-6901. https://doi.org/10.1073/pnas.120170197
  176. Shi, H., Quintero, F.J., Pardo, J.M., and Zhu, J.-K. (2002). The putative plasma membrane $Na^+$/$H^+$ antiporter SOS1 controls long-distance $Na^+$ transport in plants. Plant Cell 14, 465-477. https://doi.org/10.1105/tpc.010371
  177. Shi, H., Lee, B., Wu, S.-J., and Zhu, J.-K. (2003). Overexpression of a plasma membrane $Na^+$/$H^+$ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat. Biotech. 21, 81-85. https://doi.org/10.1038/nbt766
  178. Sothern, R.B., Tseng, T.-S., Orcutt, S.L., Olszewski, N.E., and Koukkari, W.L. (2002). GIGANTEA and SPINDLY genes linked to the clock pathway that controls circadian characteristics of transpiration in Arabidopsis. Chronobiol. Int. 19, 1005-1022. https://doi.org/10.1081/CBI-120015965
  179. Sunkar, R., Kapoor, A., and Zhu, J.-K. (2006). Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18, 2051-2065. https://doi.org/10.1105/tpc.106.041673
  180. Szczerba, M.W., Britto, D.T., and Kronzucker, H.J. (2009). $K^+$ transport in plants: Physiology and molecular biology. J. Plant Physiol. 166, 447-466. https://doi.org/10.1016/j.jplph.2008.12.009
  181. Tang, R.-J., Liu, H., Bao, Y., Lv, Q.-D., Yang, L., and Zhang, H.-X. (2010). The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Mol. Biol. 74, 367-380. https://doi.org/10.1007/s11103-010-9680-x
  182. Thain, S.C., Vandenbussche, F., Laarhoven, L.J.J., Dowson-Day, M.J., Wang, Z.-Y., Tobin, E.M., Harren, F.J. M., Millar, A.J., and Van Der Straeten, D. (2004). Circadian rhythms of ethylene emission in Arabidopsis. Plant Physiol. 136, 3751-3761. https://doi.org/10.1104/pp.104.042523
  183. Thines, B., and Harmon, F.G. (2011). Four easy pieces: mechanisms underlying circadian regulation of growth and development. Curr. Opin. Plant Biol. 14, 31-37. https://doi.org/10.1016/j.pbi.2010.09.009
  184. Tripathy, B.C., and Oelmuller, R. (2012). Reactive oxygen species generation and signaling in plants. Plant Signal. Behav. 7, 1621-1633. https://doi.org/10.4161/psb.22455
  185. Tseng, T.-S., Salome, P.A., McClung, C.R., and Olszewski, N.E. (2004). SPINDLY and GIGANTEA interact and act in Arabidopsis thaliana pathways involved in light responses, flowering, and rhythms in cotyledon movements. Plant Cell 16, 1550-1563. https://doi.org/10.1105/tpc.019224
  186. Tyerman, S.D., Bohnert, H.J., Maurel, C., Steudle, E., and Smith, J.A.C. (1999). Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J. Exp. Bot. 50, 1055-1071.
  187. Umezawa, T., Fujita, M., Fujita, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2006). Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr. Opin. Plant Biotech. 17, 113-122. https://doi.org/10.1016/j.copbio.2006.02.002
  188. Ushakova, S.A., Kovaleva, N.P., Gribovskaya, I.V., Dolgushev, V.A., and Tikhomirova, N. A. (2005). Effect of NaCl concentration on productivity and mineral composition of Salicornia europaea as a potential crop for utilization NaCl in LSS. Adv. Space Res. 36, 1349-1353. https://doi.org/10.1016/j.asr.2004.09.017
  189. Vaidyanathan, H., Sivakumar, P., Chakrabarty, R., and Thomas, G. (2003). Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.)-differential response in salt-tolerant and sensitive varieties. Plant Sci. 165, 1411-1418. https://doi.org/10.1016/j.plantsci.2003.08.005
  190. Verslues, P. E., Batelli, G., Grillo, S., Agius, F., Kim, Y.-S., Zhu, J., Agarwal, M., Katiyar-Agarwal, S., and Zhu, J.-K. (2007). Interaction of SOS2 with nucleoside diphosphate kinase 2 and catalases reveals a point of connection between salt stress and $H_2O_2$ signaling in Arabidopsis thaliana. Mol. Cell Biol. 27, 7771-7780. https://doi.org/10.1128/MCB.00429-07
  191. Wahid, A., Gelani, S., Ashraf, M., and Foolad, M.R. (2007). Heat tolerance in plants: sn overview. Env. Exp. Bot. 61, 199-223. https://doi.org/10.1016/j.envexpbot.2007.05.011
  192. Wang, X.-F., and Zhang, A.-P. (2008). Abscisic acid receptors: Multiple signal-perception sites. Ann. Bot. 101, 311-317.
  193. Wang, Z.Y., Kenigsbuch, D., Sun, L., Harel, E., Ong, M.S., and Tobin, E. M. (1997). A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9, 491-507. https://doi.org/10.1105/tpc.9.4.491
  194. Wang, S., Bai, Y., Shen, C., Wu, Y., Zhang, S., Jiang, D., Guilfoyle, T., Chen, M., and Qi, Y. (2010). Auxin-related gene families in abiotic stress response in Sorghum bicolor. Funct. Integr. Genomics. 10, 533-546. https://doi.org/10.1007/s10142-010-0174-3
  195. Wang, W., Barnaby, J.Y., Tada, Y., Li, H., Tor, M., Caldelari, D., Lee, D., Fu, X.-D., and Dong, X. (2011). Timing of plant immune responses by a central circadian regulator. Nature. 470, 110-114. https://doi.org/10.1038/nature09766
  196. Weigel, D. (2012). Natural variation in Arabidopsis: from molecular genetics to ecological genomics. Plant Physiol. 158, 2-22. https://doi.org/10.1104/pp.111.189845
  197. Wilkins, O., Brautigam, K., and Campbell, M.M. (2010). Time of day shapes Arabidopsis drought transcriptomes. Plant J. 63, 715-727. https://doi.org/10.1111/j.1365-313X.2010.04274.x
  198. Wu, Y., Ding, N., Zhao, X., Zhao, M., Chang, Z., Liu, J., and Zhang, L. (2007). Molecular characterization of PeSOS1: the putative $Na^+$/$H^+$ antiporter of Populus euphratica. Plant Mol. Biol. 65, 1-11. https://doi.org/10.1007/s11103-007-9170-y
  199. Wu, H.-J., Zhang, Z., Wang, J.-Y., Oh, D.-H., Dassanayake, M., Liu, B., Huang, Q., Sun, H.-X., Xia, R., Wu, Y., et al. (2012). Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc. Natl. Acad. Sci. USA 109, 12219-12224. https://doi.org/10.1073/pnas.1209954109
  200. Xu, X., Hotta, C.T., Dodd, A.N., Love, J., Sharrock, R., Lee, Y.W., Xie, Q., Johnson, C.H., and Webb, A.A.R. (2007). Distinct light and clock modulation of cytosolic free $Ca^{2+}$ oscillations and rhythmic chlorophyll a/b binding protein2 promoter activity in Arabidopsis. Plant Cell 19, 3474-3490. https://doi.org/10.1105/tpc.106.046011
  201. Xu, H., Jiang, X., Zhan, K., Cheng, X., Chen, X., Pardo, J.M., and Cui, D. (2008). Functional characterization of a wheat plasma membrane $Na^+$/$H^+$ antiporter in yeast. Arch. Biochem. Biophys. 473, 8-15. https://doi.org/10.1016/j.abb.2008.02.018
  202. Xu, X., Graeff, R., Xie, Q., Gamble, K.L., Mori, T., and Johnson, C. H. (2009). Comment on "The Arabidopsis circadian clock incorporates a cADPR-based feedback loop." Science. 326, 230-230.
  203. Yang, Q., Chen, Z.-Z., Zhou, X.-F., Yin, H.-B., Li, X., Xin, X.-F., Hong, X.-H., Zhu, J.-K., and Gong, Z. (2009). Overexpression of sos (salt overly sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol. Plant 2, 22-31. https://doi.org/10.1093/mp/ssn058
  204. Yensen, N. (2006). Halophyte uses for the twenty-first century. In ecophysiology of high salinity tolerant plants tasks for vegetation science., M.A. Khan and D. Weber eds. (Springer Netherlands), pp. 367-396.
  205. Yeo, A.R., and Flowers, T.J. (1980). Salt tolerance in the halophyte Suaeda maritima L. Dum.: Evaluation of the effect of salinity upon growth. J. Exp. Bot. 31, 1171-1183. https://doi.org/10.1093/jxb/31.4.1171
  206. Yoshimura, K., Miyao, K., Gaber, A., Takeda, T., Kanaboshi, H., Miyasaka, H., and Shigeoka, S. (2004). Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J. 37, 21-33. https://doi.org/10.1046/j.1365-313X.2003.01930.x
  207. Yuan, S., and Lin, H.-H. (2008). Role of salicylic acid in plant abiotic stress. Z. Naturforsch 63, 313-320.
  208. Zhai, S.-M., Gao, Q., Xue, H.-W., Sui, Z.-H., Yue, G.-D., Yang, A.-F., and Zhang, J.-R. (2012). Overexpression of the phosphatidylinositol synthase gene from Zea mays in tobacco plants alters the membrane lipids composition and improves drought stress tolerance. Planta 235, 69-84. https://doi.org/10.1007/s00425-011-1490-0
  209. Zhang, H.-X., and Blumwald, E. (2001). Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat. Biotech. 19, 765-768. https://doi.org/10.1038/90824
  210. Zhang, J., Jia, W., Yang, J., and Ismail, A.M. (2006). Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res. 97, 111-119. https://doi.org/10.1016/j.fcr.2005.08.018
  211. Zhang, J., Lu, Y., Yuan, Y., Zhang, X., Geng, J., Chen, Y., Cloutier, S., McVetty, P.B.E., and Li, G. (2009). Map-based cloning and characterization of a gene controlling hairiness and seed coat color traits in Brassica rapa. Plant Mol. Biol. 69, 553-563. https://doi.org/10.1007/s11103-008-9437-y
  212. Zhou, S., Hu, W., Deng, X., Ma, Z., Chen,, L., Huang, C., Wang, C., Wang, J., He, Y., Yang, G., et al. (2012). Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS One 7, e52439. https://doi.org/10.1371/journal.pone.0052439
  213. Zhu, J.-K. (2001). Plant salt tolerance. Trends Plant Sci. 6, 66-71.
  214. Zhu, J.-K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
  215. Zhu, J.-K. (2003). Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6, 441-445. https://doi.org/10.1016/S1369-5266(03)00085-2
  216. Zhu, J. (2007). Plant salt stress. In encyclopedia of life sciences (John Wiley & Sons).
  217. Zhu, J.-K., Liu, J., and Xiong, L. (1998). Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10, 1181-1191. https://doi.org/10.1105/tpc.10.7.1181

Cited by

  1. PnLRR-RLK27, a novel leucine-rich repeats receptor-like protein kinase from the Antarctic moss Pohlia nutans, positively regulates salinity and oxidation-stress tolerance vol.12, pp.2, 2017, https://doi.org/10.1371/journal.pone.0172869
  2. A Benzimidazole Proton Pump Inhibitor Increases Growth and Tolerance to Salt Stress in Tomato vol.8, 2017, https://doi.org/10.3389/fpls.2017.01220
  3. Identification of salt-stress responsive microRNAs from Solanum lycopersicum and Solanum pimpinellifolium vol.83, pp.1, 2017, https://doi.org/10.1007/s10725-017-0289-9
  4. Antifungal Effect of Arabidopsis SGT1 Proteins via Mitochondrial Reactive Oxygen Species vol.65, pp.38, 2017, https://doi.org/10.1021/acs.jafc.7b02808
  5. The Combination of Trichoderma harzianum and Chemical Fertilization Leads to the Deregulation of Phytohormone Networking, Preventing the Adaptive Responses of Tomato Plants to Salt Stress vol.8, 2017, https://doi.org/10.3389/fpls.2017.00294
  6. Chloride and carbonate salinity tolerance in Mimusops zeyheri seedlings during summer and winter shoot flushes vol.67, pp.8, 2017, https://doi.org/10.1080/09064710.2017.1343378
  7. Identification of MYB transcription factor genes and their expression during abiotic stresses in maize 2017, https://doi.org/10.1007/s10535-017-0756-1
  8. The Antarctic moss leucine-rich repeat receptor-like kinase (PnLRR-RLK2) functions in salinity and drought stress adaptation 2018, https://doi.org/10.1007/s00300-017-2195-z
  9. The Medicago truncatula R2R3-MYB transcription factor gene MtMYBS1 enhances salinity tolerance when constitutively expressed in Arabidopsis thaliana vol.490, pp.2, 2017, https://doi.org/10.1016/j.bbrc.2017.06.025
  10. Melatonin application confers enhanced salt tolerance by regulating Na+ and Cl− accumulation in rice 2017, https://doi.org/10.1007/s10725-017-0310-3
  11. The microtubule-associated RING finger protein 1 (OsMAR1) acts as a negative regulator for salt-stress response through the regulation of OCPI2 (O. sativa chymotrypsin protease inhibitor 2) vol.247, pp.4, 2018, https://doi.org/10.1007/s00425-017-2834-1
  12. Transcriptomic and proteomic feature of salt stress-regulated network in Jerusalem artichoke (Helianthus tuberosus L.) root based on de novo assembly sequencing analysis vol.247, pp.3, 2018, https://doi.org/10.1007/s00425-017-2818-1
  13. Enhanced multiple stress tolerance in Arabidopsis by overexpression of the polar moss peptidyl prolyl isomerase FKBP12 gene vol.37, pp.3, 2018, https://doi.org/10.1007/s00299-017-2242-9
  14. SORTING NEXIN 1 Functions in Plant Salt Stress Tolerance Through Changes of NO Accumulation by Regulating NO Synthase-Like Activity vol.9, pp.1664-462X, 2018, https://doi.org/10.3389/fpls.2018.01634
  15. Towards sustainable agriculture for the salt-affected soil pp.10853278, 2019, https://doi.org/10.1002/ldr.3218
  16. Structural and Functional Dynamics of Dehydrins: A Plant Protector Protein under Abiotic Stress vol.19, pp.11, 2018, https://doi.org/10.3390/ijms19113420
  17. Vinasse irrigation: effects on soil fertility and arbuscular mycorrhizal fungi population vol.18, pp.11, 2018, https://doi.org/10.1007/s11368-018-1996-1
  18. vol.41, pp.10, 2018, https://doi.org/10.1111/pce.13352
  19. The sucrose non-fermenting-1-related protein kinases SAPK1 and SAPK2 function collaboratively as positive regulators of salt stress tolerance in rice vol.18, pp.1, 2018, https://doi.org/10.1186/s12870-018-1408-0
  20. OsRACK1A, encodes a circadian clock-regulated WD40 protein, negatively affect salt tolerance in rice vol.11, pp.1, 2018, https://doi.org/10.1186/s12284-018-0232-3
  21. Salicylic acid alleviates salinity-caused damage to foliar functions, plant growth and antioxidant system in Ethiopian mustard (Brassica carinata A. Br.) vol.7, pp.1, 2018, https://doi.org/10.1186/s40066-018-0194-0
  22. NaCl- and cold-induced stress activate different Ca2+-permeable channels in Arabidopsis thaliana vol.87, pp.2, 2019, https://doi.org/10.1007/s10725-018-0464-7
  23. Humic Acid Confers HIGH-AFFINITY K+ TRANSPORTER 1-Mediated Salinity Stress Tolerance in Arabidopsis vol.40, pp.12, 2016, https://doi.org/10.14348/molcells.2017.0229
  24. Physiological and transcriptional responses to salt stress in salt‐tolerant and salt‐sensitive soybean (Glycine max [L.] Merr.) seedlings vol.29, pp.8, 2016, https://doi.org/10.1002/ldr.3005
  25. Elucidation and analyses of the regulatory networks of upland and lowland ecotypes of switchgrass in response to drought and salt stresses vol.13, pp.9, 2016, https://doi.org/10.1371/journal.pone.0204426
  26. Changes in gene expression in Camelina sativa roots and vegetative tissues in response to salinity stress vol.8, pp.None, 2016, https://doi.org/10.1038/s41598-018-28204-4
  27. Identification of key genes involved in the phenotypic alterations of res ( restored cell structure by salinity ) tomato mutant and its recovery induced by salt stress through transcriptomic analysi vol.18, pp.None, 2016, https://doi.org/10.1186/s12870-018-1436-9
  28. Salt-Tolerant Plant Growth Promoting Rhizobacteria for Enhancing Crop Productivity of Saline Soils vol.10, pp.None, 2016, https://doi.org/10.3389/fmicb.2019.02791
  29. Transcript profiling reveals an important role of cell wall remodeling and hormone signaling under salt stress in garlic vol.135, pp.None, 2016, https://doi.org/10.1016/j.plaphy.2018.11.033
  30. Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism vol.38, pp.3, 2019, https://doi.org/10.1007/s00299-019-02382-5
  31. A domestication‐associated reduction in K+‐preferring HKT transporter activity underlies maize shoot K+ accumulation and salt tolerance vol.222, pp.1, 2019, https://doi.org/10.1111/nph.15605
  32. Identification and Expression Profiling of the Regulator of Chromosome Condensation 1 (RCC1) Gene Family in Gossypium Hirsutum L. under Abiotic Stress and Hormone Treatments vol.20, pp.7, 2016, https://doi.org/10.3390/ijms20071727
  33. Role of exogenous signaling molecules in alleviating salt-induced oxidative stress in rice (Oryza sativa L.): a comparative study vol.41, pp.5, 2016, https://doi.org/10.1007/s11738-019-2861-6
  34. Salinity-induced modifications on growth, physiology and 20-hydroxyecdysone levels in Brazilian-ginseng [Pfaffia glomerata (Spreng.) Pedersen] vol.140, pp.None, 2019, https://doi.org/10.1016/j.plaphy.2019.05.002
  35. Induction of Antioxidant Metabolites in Moringa oleifera Callus by Abiotic Stresses vol.82, pp.9, 2016, https://doi.org/10.1021/acs.jnatprod.8b00801
  36. Pretreatment of forage legumes under moderate salinity with exogenous salicylic acid or spermidine vol.42, pp.None, 2019, https://doi.org/10.4025/actasciagron.v42i1.42809
  37. Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline-alkali stress vol.6, pp.None, 2016, https://doi.org/10.1038/s41438-019-0172-0
  38. Transcriptome analysis of rice-seedling roots under soil-salt stress using RNA-Seq method vol.13, pp.6, 2016, https://doi.org/10.1007/s11816-019-00550-3
  39. Exogenous melatonin promotes seed germination and osmotic regulation under salt stress in cotton ( Gossypium hirsutum L.) vol.15, pp.1, 2020, https://doi.org/10.1371/journal.pone.0228241
  40. Exogenous melatonin improves salt stress adaptation of cotton seedlings by regulating active oxygen metabolism vol.8, pp.None, 2016, https://doi.org/10.7717/peerj.10486
  41. Dodder-transmitted mobile signals prime host plants for enhanced salt tolerance vol.71, pp.3, 2016, https://doi.org/10.1093/jxb/erz481
  42. β-Aminobutyric Acid Pretreatment Confers Salt Stress Tolerance in Brassica napus L. by Modulating Reactive Oxygen Species Metabolism and Methylglyoxal Detoxification vol.9, pp.2, 2016, https://doi.org/10.3390/plants9020241
  43. Expression of Arabidopsis thaliana Thioredoxin-h2 in Brassica napus enhances antioxidant defenses and improves salt tolerance vol.147, pp.None, 2016, https://doi.org/10.1016/j.plaphy.2019.12.032
  44. Deciphering the involvement of glutathione in phytohormone signaling pathways to mitigate stress in planta vol.63, pp.1, 2016, https://doi.org/10.1007/s13237-019-00288-x
  45. Compensation of Mutation in Arabidopsis glutathione transferase ( AtGSTU ) Genes under Control or Salt Stress Conditions vol.21, pp.7, 2016, https://doi.org/10.3390/ijms21072349
  46. Morpho-Biological and Cytological Characterization of Tomato Roots (Solanum lycopersicum L., cv. Rekordsmen) Regenerated under NaCl Salinity in vitro vol.14, pp.3, 2016, https://doi.org/10.1134/s1990519x20030025
  47. 14-3-3 Proteins and Other Candidates form Protein-Protein Interactions with the Cytosolic C-terminal End of SOS1 Affecting Its Transport Activity vol.21, pp.9, 2016, https://doi.org/10.3390/ijms21093334
  48. Special issue in honour of Prof. Reto J. Strasser - Plant biomass in salt-stressed young maize plants can be modelled with photosynthetic performance vol.58, pp.spec, 2016, https://doi.org/10.32615/ps.2019.131
  49. Insights into the Physiological and Biochemical Impacts of Salt Stress on Plant Growth and Development vol.10, pp.7, 2016, https://doi.org/10.3390/agronomy10070938
  50. The Application of a Commercially Available Citrus-Based Extract Mitigates Moderate NaCl-Stress in Arabidopsis thaliana Plants vol.9, pp.8, 2016, https://doi.org/10.3390/plants9081010
  51. Overexpression of CmSOS1 confers waterlogging tolerance in Chrysanthemum vol.62, pp.8, 2020, https://doi.org/10.1111/jipb.12889
  52. Partial cloning, characterization, and analysis of expression and activity of plasma membrane H+-ATPase in Kallar grass [Leptochloa fusca (L.) Kunth] under salt stress vol.71, pp.3, 2020, https://doi.org/10.1007/s42977-020-00019-3
  53. Metabolism regulation during salt exposure in the halophyte Cakile maritima vol.177, pp.None, 2016, https://doi.org/10.1016/j.envexpbot.2020.104075
  54. Chitosan Modified Biochar Increases Soybean ( Glycine max L.) Resistance to Salt-Stress by Augmenting Root Morphology, Antioxidant Defense Mechanisms and the Expression of Stress-Responsive Genes vol.9, pp.9, 2020, https://doi.org/10.3390/plants9091173
  55. CAX1a TILLING Mutations Modify the Hormonal Balance Controlling Growth and Ion Homeostasis in Brassica rapa Plants Subjected to Salinity vol.10, pp.11, 2016, https://doi.org/10.3390/agronomy10111699
  56. The Liriodendron chinense MKK2 Gene Enhances Arabidopsis thaliana Salt Resistance vol.11, pp.11, 2020, https://doi.org/10.3390/f11111160
  57. Identification and characterization of a novel multi-stress responsive gene in Arabidopsis vol.15, pp.12, 2016, https://doi.org/10.1371/journal.pone.0244030
  58. The floral repressors TEMPRANILLO1 and 2 modulate salt tolerance by regulating hormonal components and photo‐protection in Arabidopsis vol.105, pp.1, 2016, https://doi.org/10.1111/tpj.15048
  59. Low pH alleviated salinity stress of ginger seedlings by enhancing photosynthesis, fluorescence, and mineral element contents vol.9, pp.None, 2016, https://doi.org/10.7717/peerj.10832
  60. Identification and Functional Analysis of Two Purple Acid Phosphatases AtPAP17 and AtPAP26 Involved in Salt Tolerance in Arabidopsis thaliana Plant vol.11, pp.None, 2016, https://doi.org/10.3389/fpls.2020.618716
  61. Resveratrol Alleviates the KCl Salinity Stress of Malus hupehensis Rhed vol.12, pp.None, 2016, https://doi.org/10.3389/fpls.2021.650485
  62. 제설제 피해지에서 토양개량제 처리에 따른 구절초의 생육특성 비교 vol.30, pp.3, 2016, https://doi.org/10.5322/jesi.2021.30.3.235
  63. Reassessing the role of ion homeostasis for improving salinity tolerance in crop plants vol.171, pp.4, 2016, https://doi.org/10.1111/ppl.13112
  64. Chloroplast Localized FIBRILLIN11 Is Involved in the Osmotic Stress Response during Arabidopsis Seed Germination vol.10, pp.5, 2016, https://doi.org/10.3390/biology10050368
  65. Regulation of Plant Responses to Salt Stress vol.22, pp.9, 2021, https://doi.org/10.3390/ijms22094609
  66. Cut Flower Characteristics and Growth Traits under Salt Stress in Lily Cultivars vol.10, pp.7, 2021, https://doi.org/10.3390/plants10071435
  67. The miR528-AO Module Confers Enhanced Salt Tolerance in Rice by Modulating the Ascorbic Acid and Abscisic Acid Metabolism and ROS Scavenging vol.69, pp.31, 2021, https://doi.org/10.1021/acs.jafc.1c01096
  68. Effect of CAX1a TILLING mutations on photosynthesis performance in salt-stressed Brassica rapa plants vol.311, pp.None, 2021, https://doi.org/10.1016/j.plantsci.2021.111013
  69. Adaptation to coastal soils through pleiotropic boosting of ion and stress hormone concentrations in wild Arabidopsis thaliana vol.232, pp.1, 2016, https://doi.org/10.1111/nph.17569
  70. Plant Group II LEA Proteins: Intrinsically Disordered Structure for Multiple Functions in Response to Environmental Stresses vol.11, pp.11, 2016, https://doi.org/10.3390/biom11111662
  71. AvNAC030, a NAC Domain Transcription Factor, Enhances Salt Stress Tolerance in Kiwifruit vol.22, pp.21, 2021, https://doi.org/10.3390/ijms222111897
  72. Soil Salinity, a Serious Environmental Issue and Plant Responses: A Metabolomics Perspective vol.11, pp.11, 2016, https://doi.org/10.3390/metabo11110724
  73. Salt responsive alternative splicing of a RING finger E3 ligase modulates the salt stress tolerance by fine-tuning the balance of COP9 signalosome subunit 5A vol.17, pp.11, 2021, https://doi.org/10.1371/journal.pgen.1009898
  74. Defective cytokinin signaling reprograms lipid and flavonoid gene-to-metabolite networks to mitigate high salinity in Arabidopsis vol.118, pp.48, 2021, https://doi.org/10.1073/pnas.2105021118
  75. Comparative transcriptomic and metabolic profiling provides insight into the mechanism by which the autophagy inhibitor 3-MA enhances salt stress sensitivity in wheat seedlings vol.21, pp.1, 2016, https://doi.org/10.1186/s12870-021-03351-5
  76. Integrated transcriptome and proteome analysis reveals complex regulatory mechanism of cotton in response to salt stress vol.4, pp.1, 2016, https://doi.org/10.1186/s42397-021-00085-5
  77. Moringa oleifera Leaf Extract Enhanced Growth, Yield, and Silybin Content While Mitigating Salt-Induced Adverse Effects on the Growth of Silybum marianum vol.11, pp.12, 2016, https://doi.org/10.3390/agronomy11122500
  78. The F-box E3 ubiquitin ligase AtSDR is involved in salt and drought stress responses in Arabidopsis vol.809, pp.None, 2022, https://doi.org/10.1016/j.gene.2021.146011
  79. Potential of plant growth-promoting rhizobacteria-plant interactions in mitigating salt stress for sustainable agriculture: A review vol.32, pp.2, 2016, https://doi.org/10.1016/s1002-0160(21)60070-x