2,718
Views
60
CrossRef citations to date
0
Altmetric
Plant-Environment Interactions

Exogenous melatonin improves salt tolerance in tomato by regulating photosynthetic electron flux and the ascorbate–glutathione cycle

, , , , , & show all
Pages 453-463 | Received 11 Oct 2018, Accepted 11 Jul 2019, Published online: 19 Aug 2019

References

  • Afreen F, Zobayed SM, Kozai T. 2006. Melatonin in Glycyrrhiza uralensis: response of plant roots to spectral quality of light and UV-B radiation. J Pineal Res. 41:108. doi: 10.1111/j.1600-079X.2006.00337.x
  • Arnao M, Hernández-Ruiz J. 2009. Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. J Pineal Res. 46:58–63. doi: 10.1111/j.1600-079X.2008.00625.x
  • Arnao M, Hernández-Ruiz J. 2015. Functions of melatonin in plants: a review. J Pineal Res. 59:133. doi: 10.1111/jpi.12253
  • Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254. doi: 10.1016/0003-2697(76)90527-3
  • Cheng DD, Zhang ZS, Sun XB, Zhao M, Sun GY, Chow WS. 2016. Photoinhibition and photoinhibition-like damage to the photosynthetic apparatus in tobacco leaves induced by pseudomonas syringae pv. tabaci under light and dark conditions. BMC Plant Biol. 16:1–11. doi: 10.1186/s12870-015-0700-5
  • Fan X, Zhang Z, Gao H, Yang C, Liu M, Li Y. 2014. Photoinhibition-like damage to the photosynthetic apparatus in plant leaves induced by submergence treatment in the dark. Plos One. 9:e89067. doi: 10.1371/journal.pone.0089067
  • Foyer CH, Noctor G. 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal. 11:861–905. doi: 10.1089/ars.2008.2177
  • Galano A, Tan DX, Reiter RJ. 2011. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res. 51:1–16. doi: 10.1111/j.1600-079X.2011.00916.x
  • Gong M, Li YJ, Chen SZ. 1998. Abscisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems. J Plant Physiol. 153:488–496. doi: 10.1016/S0176-1617(98)80179-X
  • Haldimann P, Strasser RJ. 1999. Effects of anaerobiosis as probed by the polyphasic chlorophyll a fluorescence rise kinetic in pea (Pisum sativum L). Photosynth Res. 62:67–83. doi: 10.1023/A:1006321126009
  • Han Y, Wang S, Zhao N, Deng S, Zhao C, Li N. 2016. Exogenous abscisic acid alleviates cadmium toxicity by restricting Cd2+ influx in Populus euphratica cells. J Plant Growth Regul. 35:827–837. doi: 10.1007/s00344-016-9585-2
  • Hasan MK, Ahammed GJ, Yin L, Shi K, Xia X, Zhou Y. 2015. Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicuml. Front Plant Sci. 6:601. doi: 10.3389/fpls.2015.00601
  • Ibrahim MH, Jaafar HZ. 2012. Primary, secondary metabolites, H2O2, malondialdehyde and photosynthetic responses of Orthosiphon stamineus Benth to different irradiance levels. Molecules. 17:1159–1176. doi: 10.3390/molecules17021159
  • Kang K, Lee K, Park S, Kim Y S, Back K. 2010. Enhanced production of melatonin by ectopic overexpression of human serotonin N-acetyltransferase plays a role in cold resistance in transgenic rice seedlings. J Pineal Res. 49:176–182.
  • Kolář J, Macháčková I, Eder J, Prinsen E, Dongen WV, Onckelen HV. 1997. Melatonin: occurrence and daily rhythm in Chenopodium rubrum. Phytochem. 44:1407–1413. doi: 10.1016/S0031-9422(96)00568-7
  • Kudoh H, Sonoike K. 2002. Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. Planta. 215:541–548. doi: 10.1007/s00425-002-0790-9
  • Lei XY, Zhu RY, Zhang GY, Dai YR. 2004. Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: the possible involvement of polyamines. J Pineal Res. 36:126–131. doi: 10.1046/j.1600-079X.2003.00106.x
  • Li P, Cheng L, Gao H, et al. 2009. Heterogeneous behavior of PSII in soybean (glycine max) leaves with identical PSII photochemistry efficiency under different high temperature treatments. J Plant Physiol. 166:1607. doi: 10.1016/j.jplph.2009.04.013
  • Li H, He J, Yang X, Li X, Luo D, Wei C. 2015. Glutathione-dependent induction of local and systemic defense against oxidative stress by exogenous melatonin in cucumber (Cucumis sativus L.). J Pineal Res. 60:206–216. doi: 10.1111/jpi.12304
  • Li C, Liang B, Chang C, Wei Z, Zhou S, Ma F. 2016a. Exogenous melatonin improved potassium content in Malus under different stress conditions. J Pineal Res. 61:218–229. doi: 10.1111/jpi.12342
  • Li X, Tan D, Jiang D, Liu F. 2016b. Melatonin enhances cold tolerance in drought-primed wild type and abscisic acid-deficient mutant barley. J Pineal Res. 61:328–339. doi: 10.1111/jpi.12350
  • Li C, Wang P, Wei Z, Liang D, Liu C, Yin L. 2012. The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J Pineal Res. 53:298–306. doi: 10.1111/j.1600-079X.2012.00999.x
  • Lin ZH, Chen LS, Chen RB, Zhang FZ, Jiang HX, Ning T. 2009. CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport probed by the JIP-test, of tea leaves in response to phosphorus supply. BMC Plant Biol. 9:43. doi: 10.1186/1471-2229-9-43
  • Lin YH, Pan KY, Hung CH, Huang HE, Chen CL, Feng TY, Huang LF. 2013. Overexpression of ferredoxin, PETF, enhances tolerance to heat stress in Chlamydomonas reinhardtii. Int J Mol Sci. 14:20913–20929. doi: 10.3390/ijms141020913
  • Manchester LC, Coto-Montes A, Boga JA, Andersen LP, Zhou Z, Galano A. 2015. Melatonin: an ancient molecule that makes oxygen metabolically tolerable. J Pineal Res. 59:403. doi: 10.1111/jpi.12267
  • Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Ann Rev Plant Biology. 59:651–681. doi: 10.1146/annurev.arplant.59.032607.092911
  • Palma JM, Río LAD. 2006. Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. J Exp Bot. 57:1747. doi: 10.1093/jxb/erj191
  • Park S, Back K. 2012. Melatonin promotes seminal root elongation and root growth in transgenic rice after germination. J Pineal Res. 53:385–389. doi: 10.1111/j.1600-079X.2012.01008.x
  • Pelagio-Flores R, Muñozparra E, Ortizcastro R, López-Bucio J. 2012. Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling. J Pineal Res. 53:279–288. doi: 10.1111/j.1600-079X.2012.00996.x
  • Porra RJ. 2002. The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res. 73:149–156. doi: 10.1023/A:1020470224740
  • Posmyk MM, Kuran H, Marciniak K, Janas KM. 2008. Presowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations. J Pineal Res. 45:24. doi: 10.1111/j.1600-079X.2007.00552.x
  • Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL. 2007. Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ. 30:1035–1040. doi: 10.1111/j.1365-3040.2007.01710.x
  • Shi H, Chan Z. 2014. The cysteine2/histidine2-type transcription factor ZINC FINGER OF Arabidopsis Thaliana 6-activated C-REPEAT-BINDING FACTOR pathway is essential for melatonin-mediated freezing stress resistance in Arabidopsis. J Pineal Res. 57:185–191. doi: 10.1111/jpi.12155
  • Shi H, Wang X, Tan DX, Reiter RJ, Chan Z. 2015. Comparative physiological and proteomic analyses reveal the actions of melatonin in the reduction of oxidative stress in Bermuda grass (cynodon dactylon (l). pers. J Pineal Res. 59:120–131. doi: 10.1111/jpi.12246
  • Siddiqui MH, Alamri S, Al-Khaishany MY. 2019. Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. Int J Mol Sci. 20(2):353. doi: 10.3390/ijms20020353
  • Srivastava A, Guissé B, Greppin H, Strasser RJ. 1997. Regulation of antenna structure and electron transport in photosystem II of Pisum sativum, under elevated temperature probed by the fast polyphasic chlorophyll a, fluorescence transient: OKJIP. BBA-Bioenergetics. 1320:95–106. doi: 10.1016/S0005-2728(97)00017-0
  • Strasser BJ. 1997. Donor side capacity of Photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res. 52(2):147–155. doi: 10.1023/A:1005896029778
  • Strasser RJ, Srivastava A. 1995. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem. Photobiol. 61:32–42. doi: 10.1111/j.1751-1097.1995.tb09240.x
  • Strasser BJ, Strasser RJ. 1995. Measuring fast fluorescence transients to address environmental questions: the JIP-test. In: P Mathis, editor. Photosynthesis: from light to biosphere. Dordrecht: Kluwer Academic Publishers; p. 977–980.
  • Strasser RJ, Tsimilli-Micheal M, Srivastava A. 2004. Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou, GC Govindjee, editor. Chlorophyll a fluorescence: a signature of photosynthesis. Dordrecht: Springer; p. 321–362.
  • Suo J, Qi Z, Zhang Z, Chen S, Cao J, Liu G. 2015. Cytological and proteomic analyses of Osmunda cinnamomea germinating spores reveal characteristics of fern spore germination and rhizoid tip growth. Mol Cell Proteomics. 14(9):2510–2534. doi: 10.1074/mcp.M114.047225
  • Takahashi S, Murata N. 2008. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 13:178–182. doi: 10.1016/j.tplants.2008.01.005
  • Tal O, Haim A, Harel O, Gerchman Y. 2011. Melatonin as an antioxidant and its semi-lunar rhythm in green macroalga Ulva sp. J Exp Bot. 62:1903. doi: 10.1093/jxb/erq378
  • Tan DX, Manchester LC, Terron MP, Flores LJ, Reiter RJ. 2007. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res. 42:28–42. doi: 10.1111/j.1600-079X.2006.00407.x
  • Tiryaki I, Keles H. 2012. Reversal of the inhibitory effect of light and high temperature on germination of Phacelia tanacetifolia seeds by melatonin. J Pineal Res. 52:332–339. doi: 10.1111/j.1600-079X.2011.00947.x
  • TóTh SZ, Schansker G, Kissimon J, Ková CL, Garab G, Strasser RJ. 2005. Biophysical studies of photosystem ii-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.). J Plant Physiol. 162:181–194. doi: 10.1016/j.jplph.2004.06.010
  • Venkatesh J, Upadhyaya CP, Yu JW, Hemavathi A, Kim DH, Strasser RJ. 2012. Chlorophyll a fluorescence transient analysis of transgenic potato overexpressing D-galacturonic acid reductase gene for salinity stress tolerance. Hortic Environ Biotechnol. 53:320–328. doi: 10.1007/s13580-012-0035-1
  • Wang X, Chen S, Zhang H, Shi L, Cao F, Guo L. 2010. Desiccation tolerance mechanism in resurrection fern-ally Selaginella tamariscina revealed by physiological and proteomic analysis. J Proteome Res. 9:6561–6577. doi: 10.1021/pr100767k
  • Wang LY, Liu JL, Wang WX, Sun Y. 2016. Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica. 54:19–27. doi: 10.1007/s11099-015-0140-3
  • Wang P, Sun X, Chang C, Feng F, Liang D, Cheng L. 2013a. Delay in leaf senescence of Malus hupehensis by long-term melatonin application is associated with its regulation of metabolic status and protein degradation. J Pineal Res. 55:424–434. doi: 10.1111/jpi.12069
  • Wang P, Sun X, Li C, Wei Z, Liang D, Ma F. 2013b. Long term exogenous application of melatonin delays drought induced leaf senescence in apple. J Pineal Res. 54:292–302. doi: 10.1111/jpi.12017
  • Wang P, Yin L, Liang D, Li C, Ma F, Yue Z. 2012. Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate-glutathione cycle. J Pineal Res. 53:11. doi: 10.1111/j.1600-079X.2011.00966.x
  • Wang L, Zhao Y, Reiter RJ, He C, Liu G, Lei Q. 2014. Changes in melatonin levels in transgenic ‘Micro-Tom’ tomato overexpressing ovine AANAT and ovine HIOMT genes. J Pineal Res. 56:134–142. doi: 10.1111/jpi.12105
  • Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS. 2015. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot. 66:695–707. doi: 10.1093/jxb/eru392
  • Wilhelm C, Selmar D. 2011. Energy dissipation is an essential mechanism to sustain the viability of plants: The physiological limits of improved photosynthesis. J Plant Physiol. 168:79–87. doi: 10.1016/j.jplph.2010.07.012
  • Yan B, Dai Q, Liu X, Huang S, Wang Z. 1996. Flooding-inducedmembrane damage, lipid oxidation and activated oxygengeneration in corn leaves. Plant Soil. 179:261–268. doi:10.1007/bf00009336.
  • Yang Y, Chang D, Wang Y, Zhang FC. 2015. Effects of exogenous JA and MeJA on seed germination and seeding physiological characteristics of Gossypium hirsutum under salt stress. Seed. 34:8–18.
  • Yin ZP, Li S, Ren J, Song XS. 2014. Role of spermidine and spermine in alleviation of drought-induced oxidative stress and photosynthetic inhibition in Chinese dwarf cherry (Cerasus humilis) seedlings. Plant Growth Regul. 74:209–218. doi: 10.1007/s10725-014-9912-1
  • Yin Z, Ren J, Zhou L, Sun L, Wang J, Liu Y. 2017. Water deficit mechanisms in perennial shrubs Cerasus humilis leaves revealed by physiological and proteomic analyses. Proteome Sci. 15:9. doi: 10.1186/s12953-017-0117-1
  • Zhan GM, Li RJ, Hu ZY, Liu J, Deng LB, Lu SY. 2014. Cosuppression of RBCS3B, in Arabidopsis, leads to severe photoinhibition caused by ROS accumulation. Plant Cell Rep. 33:1091. doi: 10.1007/s00299-014-1597-4
  • Zhang Z, Li G, Gao H, Zhang L, Yang C, Liu P. 2012. Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence, Zea mays, L. inbred lines. Plos One. 7:e42936. doi: 10.1371/journal.pone.0042936
  • Zhang HH, Li X, Zhang SB, Yin ZP, Zhu WX, Li JB, Meng L, Zhong HX, Wu YN, Xu N, Sun GY. 2018. Rootstock alleviates salt stress in grafted mulberry seedlings: physiological and PSII function responses. Front Plant Sci. 9:1806. doi: 10.3389/fpls.2018.01806
  • Zhang D, Ren L, Chen GQ, Zhang J, Reed BM, Shen XH. 2015a. ROS-induced oxidative stress and apoptosis-like event directly affect the cell viability of cryopreserved embryogenic callus in Agapanthus praecox. Plant Cell Rep. 34:1499–1513. doi: 10.1007/s00299-015-1802-0
  • Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S. 2015b. Roles of melatonin in abiotic stress resistance in plants. J Exp Bot. 66:647. doi: 10.1093/jxb/eru336
  • Zhang HH, Xu N, Li X, Jin WW, Tian Q, Gu SY. 2017. Overexpression of 2-Cys Prx increased salt tolerance of photosystem II in tobacco. Int J Agric Biol. 19:735–745. doi: 10.17957/IJAB/15.0348
  • Zhang HH, Xu N, Teng ZY, Wang JR, Ma SL, Wu XY, Li X, Sun GY. 2019. 2-Cys Prx plays a critical role in scavenging H2O2 and protecting photosynthetic function in leaves of tobacco seedlings under drought stress. Journal of Plant Interaction. 14(1):119–128. doi: 10.1080/17429145.2018.1562111
  • Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC. 2013. Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L). J Pineal Res. 54:15–23. doi: 10.1111/j.1600-079X.2012.01015.x
  • Zhao H, Ye L, Wang Y, Zhou X, Yang J, Wang J. 2016. Melatonin increases the chilling tolerance of chloroplast in cucumber seedlings by regulating photosynthetic electron flux and the ascorbate-glutathione cycle. Front Plant Sci. 7:e85996.
  • Zheng Q, Liu J, Liu R, Wu H, Jiang C, Wang C. 2015. Temporal and spatial distributions of sodium and polyamines regulated by brassinosteroids in enhancing tomato salt resistance. Plant & Soil. 400:147–164. doi: 10.1007/s11104-015-2712-1
  • Zhou X, Zhao H, Cao K, Hu L, Du T, Baluška F, Zou Z. 2016. Beneficial roles of melatonin on redox regulation of photosynthetic electron transport and synthesis of d1 protein in tomato seedlings under salt stress. Front Plant Sci. 7. doi:10.3389/fpls.2016.01823.
  • Zhu JK. 2002. Salt and drought stress signal transduction in plants. Annu Rev Plant Biol. 53:247. doi: 10.1146/annurev.arplant.53.091401.143329