Abstract
Melatonin mediates many physiological processes in animals and plants. To examine the potential roles of melatonin in salinity tolerance, we investigated the effects of exogenous melatonin on growth and antioxidant system in cucumber under 200 mM NaCl stress conditions. The results showed that the melatonin-treated plants significantly increased growth mass and antioxidant protection. Under salinity stress, the addition of melatonin effectively alleviated the decrease in the net photosynthetic rate, the maximum quantum efficiency of PSII, and the total chlorophyll content. Our data also suggested that melatonin and the resistance of plants exhibited a concentration effect. The application of 50–150 μM melatonin significantly improved the photosynthetic capacity. Additionally, the pretreatment with melatonin reduced the oxidative damage under salinity stress by scavenging directly H2O2 or enhancing activity of antioxidant enzymes (including superoxide dismutase, peroxidase, catalase, ascorbate peroxidase) and concentrations of antioxidants (ascorbic acid and glutathione). Therefore, the melatonin-treated plants could effectively enhance their salinity tolerance.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- AsA:
-
ascorbate
- CAT:
-
catalase
- Chl:
-
chlorophyll
- DAT:
-
days after treatment
- DM:
-
dry mass
- DTNB:
-
5,5′-dithio-bis-2-nitrobenzoic acid
- F0 :
-
minimal fluorescence yield of the dark-adapted state
- Fm :
-
maximal fluorescence yield of the dark-adapted state
- Fv :
-
variable fluorescence
- Fv/Fm :
-
maximal quantum yield of PSII photochemistry
- FM:
-
fresh mass
- GR:
-
glutathion reductase
- GSH:
-
reduced glutathione
- GSSH:
-
oxidized glutathione
- IAA:
-
indole acetic acid
- MDA:
-
malondialdehyde
- MT:
-
melatonin
- NSC:
-
unstressed control group
- P N :
-
net photosynthetic rate
- POD:
-
peroxidase
- ROS:
-
reactive oxygen species
- SOD:
-
superoxide dismutase
- ST:
-
salt treatment
References
Aebi H.: Catalase in vitro. — Methods Enzymol. 105: 121–126, 1984.
Afreen F., Zobayed S.M., Kozai T.: Melatonin in Glycyrrhiza uralensis: response of plant roots to spectral quality of light and UV-B radiation. — J. Pineal Res. 41: 108–115, 2006.
Arnao M.B.: Phytomelatonin: discovery, content, and role in plants. — Adv. Bot. 2014:1–11, 2014.
Arnao M.B., Hernández-Ruiz J.: Melatonin promotes adventitious and lateral root regeneration in etiolated hypocotyls of Lupinus albus L. — J. Pineal Res. 42: 147–152, 2007.
Arnao M.B., Hernández-Ruiz J.: Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. — J. Pineal Res. 46: 58–63, 2009.
Arnao M.B., Hernández-Ruiz J.: Growth conditions determine different melatonin levels in Lupinus albus L. — J. Pineal Res. 55: 149–155, 2013a.
Arnao M.B., Hernández-Ruiz J.: Growth conditions influence the melatonin content of tomato plants. — Food Chem. 138: 1212–1214, 2013b.
Arnao M.B., Hernández-Ruiz J.: Melatonin: plant growth regulator and/or biostimulator during stress? — Trends Plant Sci. 19: 789–797, 2014.
Choi S., Dadakhujaev S., Ryu H. et al.: Melatonin protects against oxidative stress in granular corneal dystrophy type 2 corneal fibroblasts by mechanisms that involve membrane melatonin receptors. — J. Pineal Res. 51: 94–103, 2011.
Dionisio-Sese M.L., Tobita S.: Antioxidant responses of rice seedlings to salinity stress. — Plant Sci. 135: 1–9, 1998.
Foyer C., Noctor G.: Oxygen processing in photosynthesis: regulation and signalling. — New Phytol. 146: 359–388, 2000.
Gómez-Pando L.R., Álvarez-Castro R., Eguiluz-de la Barra A.: Effect of salt stress on peruvian germplasm of Chenopodium quinoa Willd.: A promising crop. — J. Agron. Crop Sci. 196: 391–396, 2010.
Galano A., Tan D.X., Reiter R.J.: Melatonin as a natural ally against oxidative stress: a physicochemical examination. — J. Pineal Res. 51: 1–16, 2011.
Griffith O.W.: Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. — Anal. Biochem. 106: 207–212, 1980.
Hardeland R., Cardinali D.P., Srinivasan V. et al.: Melatonin — a pleiotropic, orchestrating regulator molecule. — Prog. Neurobiol. 93: 350–384, 2011.
Hernández-Ruiz J., Arnao M.B.: Melatonin stimulates the expansion of etiolated lupin cotyledons. — Plant Growth Regul. 55: 29–34, 2008.
Hernandez-Ruiz J., Cano A., Arnao M.B.: Melatonin: a growthstimulating compound present in lupin tissues. — Planta 220: 140–144, 2004.
Hodges D.M., DeLong J.M., Forney C.F., Prange R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. — Planta 207: 604–611, 1999.
Jampeetong A., Brix H.: Effects of NaCl salinity on growth, morphology, photosynthesis and proline accumulation of Salvinia natans. — Aquat. Bot. 91: 181–186, 2009.
Jung-Hynes B., Reiter R.J., Ahmad N.: Sirtuins, melatonin and circadian rhythms: building a bridge between aging and cancer. — J. Pineal Res. 48: 9–19, 2010.
Khalid A.M., Nasim A.R., Abdulbasset M.A.: Salicylic acidmediated alleviation of cadmium toxicity in maize leaves. — J. Plant Sci. 2: 276–281, 2014.
Kolář J., Johnson C.H., Macháčková I.: Exogenously applied melatonin (N-acetyl-5-methoxytryptamine) affects flowering of the short-day plant Chenopodium rubrum. — Physiol. Plantarum 118: 605–612, 2003.
Lei X.Y., Zhu R.Y., Zhang G.Y., Dai Y.R.: Attenuation of coldinduced apoptosis by exogenous melatonin in carrot suspension cells: the possible involvement of polyamines. — J. Pineal Res. 36: 126–131, 2004.
Li C., Wang P., Wei Z. et al.: The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. — J. Pineal Res. 53: 298–306, 2012.
Lichtenthaler K., Wellburn A.: Determinations of total carotenoids and chlorophylls a and a of leaf extracts in different solvents. — Biochem. Soc. Trans. 11: 591–592, 1983.
Logan B.A., Grace S. C., Adams W. W., Demmig-Adams B.: Seasonal differences in xanthophylls cycle characteristics and antioxidants in Mahonia repens growing in different light environments. — Oecologia 116: 9–17, 1998.
McKersie B.D., Bowley S.R., Harjanto E., Leprince O.: Waterdeficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. — Plant Physiol. 111: 1177–1181, 1996.
Mittler R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.
Motilva V., García-Mauriño S., Talero E., Illanes M.: New paradigms in chronic intestinal inflammation and colon cancer: role of melatonin. — J. Pineal Res. 51: 44–60, 2011.
Munns R., Tester M.: Mechanisms of salinity tolerance. — Annu. Rev. Plant Biol. 59: 651–681, 2008.
Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. — Plant Cell Physiol. 22: 867–880, 1981.
Noctor G., Foyer C.H.: Ascorbate and glutathione: Keeping active oxygen under control. — Annu. Rev. Plant Phys. 49: 249–279, 1998.
Parida A.K., Das A.B.: Salt tolerance and salinity effects on plants: a review. — Ecotox. Environ. Safe. 60: 324–349, 2005.
Patterson B.D., Macrae E.A., Ferguson I.B.: Estimation of hydrogen peroxide in plant extracts using titanium(IV). — Anal. Biochem. 139: 487–492, 1984.
Radyukina N.L., Kartashov A.V., Ivanov Y.V. et al.: Functioning of defense systems in halophytes and glycophytes under progressing salinity. — Russ. J. Plant Physl+ 54: 806–815, 2007.
Rao M.V., Paliyath G., Ormrod D.P.: Ultraviolet-B- and ozoneinduced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. — Plant Physiol. 110: 125–136, 1996.
Reiter R.J., Tan D.X., Terron M.P. et al.: Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. — Acta. Biochim. Pol. 54: 1–9, 2007.
Roncarati F., Rijstenbil J.W., Pistocchi R.: Photosynthetic performance, oxidative damage and antioxidants in Cylindrotheca closterium in response to high irradiance, UVB radiation and salinity. — Mar. Biol. 153: 965–973, 2008.
Smirnoff N.: The role of active oxygen in the response of plants to water deficit and desiccation. — New Phytol. 125: 27–58, 1993.
Sreenivasulu N., Grimm B., Wobus U., Weschke W.: Differential response of antioxidant compounds to salinity stress in salttolerant and salt-sensitive seedlings of foxtail millet (Setaria italica). — Physiol. Plantarum 109: 435–442, 2000.
Tan D.X., Manchester L.C., Liu X. et al.: Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin’s primary function and evolution in eukaryotes. — J. Pineal Res. 54: 127–138, 2013.
Tan D.X., Manchester L.C., Terron M.P. et al.: One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? — J. Pineal Res. 42: 28–42, 2007.
Wang P., Sun X., Li C. et al.: Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. — J. Pineal Res. 54: 292–302, 2013.
Wang P., Yin L., Liang D. et al.: Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate-glutathione cycle. — J. Pineal Res. 53: 11–20, 2012.
Xu S.C., He M.D., Zhong M. et al.: Melatonin protects against Nickel-induced neurotoxicity in vitro by reducing oxidative stress and maintaining mitochondrial function. — J. Pineal Res. 49: 86–94, 2010.
Zhang N., Sun Q., Zhang H. et al.: Roles of melatonin in abiotic stress resistance in plants. — J. Exp. Bot. 66: 647–656, 2015
Zhang N., Zhao B., Zhang H.J. et al.: Melatonin promotes waterstress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). — J. Pineal Res. 54: 15–23, 2013.
Zhang N., Zhao H., Yang R.C. et al.: Advances in melatonin and its functions in plants. — Agr. Sci. Tech. 13: 1833–1837, 2012.
Zhu J.K.: Plant salt tolerance. — Trends Plant Sci. 6: 66–71, 2001.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: This work was supported by the earmarked fund for China Agricultural Research System. The authors are grateful to Priscilla Licht for help in revising our English composition and to Mr. Zhengwei Ma for management of the potted cucumber plants.
Rights and permissions
About this article
Cite this article
Wang, L.Y., Liu, J.L., Wang, W.X. et al. Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica 54, 19–27 (2016). https://doi.org/10.1007/s11099-015-0140-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-015-0140-3