Biologia plantarum 65:307-315, 2021 | DOI: 10.32615/bp.2021.039
Melatonin alleviates photoinhibition in cucumber seedlings by modulating partitioning of absorbed excitation energy in photosystem Ⅱ
- 1 College of Horticulture, Shanxi Agricultural University, Taigu, 030801, Shanxi, P.R. China
- 2 Shanxi protected vegetable quality improvement and Synergetic Innovation Center, Taigu, 030801, Shanxi, P.R. China
- 3 Shanxi Key Laboratory of Facility Horticulture, Taigu, 030801,Shanxi, P.R. China
The aim of this study was to evaluate the effects of melatonin on photoinhibition under chilling stress in cucumber seedlings and to inquire into any mechanisms of mitigation. Under chilling stress, the net photosynthetic rate declined dramatically but the decline was significantly mitigated by irrigation with a melatonin solution. Possible mechanisms for this mitigation are that melatonin accelerates xanthophyll de-epoxidation by upregulating the transcription of the violaxanthin de-epoxidase gene (CsVDE) and down-regulating that of the zeaxanthin cyclase gene (CsZE) during chilling. There was also a rise in non-photochemical quenching (NPQ) if seedlings were pretreated with melatonin before chilling. The efficient operation of the xanthophyll cycle helped consume excessive excitation energy in photosystem (PS) Ⅱ and so protected the photosynthetic system. Melatonin also modulated the partitioning of absorbed excitation energy in PS Ⅱ as evidenced by alleviation of the decrease in quantum yield of photochemical energy conversion in PS Ⅱ under chilling stress, by alleviation of the rise in quantum yield of non-regulated, non-photochemical energy loss in PS II and by increasing the regulated non-photochemical energy loss in PS II. This study presents a new understanding of the mechanisms through which melatonin mitigates photoinhibition by modulating the partitioning of absorption energy in PS Ⅱ based on the xanthophyll cycle.
Keywords: chilling, Cucumis sativus, excitation energy, melatonin, photoinhibition, xanthophyll cycle.
Received: October 11, 2020; Revised: June 7, 2021; Accepted: June 30, 2021; Published online: November 12, 2021 Show citation
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References
- Al-Huqail, A., Khan, M., Ali, H., Siddiqui, D.M.H., Al-Huqail, A., Al-Zuaibr, F., Al-Muwayhi, M., Marraiki, N., Al-Humaid, L.A.: Exogenous melatonin mitigates boron toxicity in wheat. - Ecotoxicol. Environ. Safety 201: 110822, 2020.
Go to original source... - Allen, D.J., Ort, D.R.: Impacts of chilling temperatures on photosynthesis in warm-climate plants. - Trends Plant Sci. 6: 36-42, 2001.
Go to original source... - Arms, E.M., Bloom, A.J., St. Clair, D.A.: High-resolution mapping of a major effect QTL from wild tomato Solanum habrochaites that influences water relations under root chilling. - Theor. appl. Genet. 128: 1713-1724, 2015.
Go to original source... - Baker, N.R.: Chlorophyll fluorescence: a probe of photosynthesis in vivo. - Annu. Rev. Plant Biol. 59: 89-113, 2008.
Go to original source... - Butler, W.L.: Energy distribution in the photochemical apparatus of photosynthesis. - Annu. Rev. Plant Biol. 29: 345-378, 1978.
Go to original source... - Cooper, J.W., Hu, Y., Beyyoudh, L., Yildiz Dasgan, H., Kunert, K., Beveridge, C.A., Foyer, C.H.: Strigolactones positively regulate chilling tolerance in pea and in Arabidopsis. - Plant Cell Physiol. 41: 1298-1310, 2018.
Go to original source... - Gan, P., Liu, F., Li, R., Wang, S., Luo, J.: Molecular sciences chloroplasts-beyond energy capture and carbon fixation: tuning of photosynthesis in response to chilling stress. - Int. J. mol. Sci. 20: 5046-5060, 2019.
Go to original source... - Gilmore, A.M.: Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. - Physiol. Plant. 99: 197-209, 1997.
Go to original source... - Goss, R., Jakob, T.: Regulation and function of xanthophyll cycle-dependent photoprotection in algae. - Photosynth. Res. 106: 103-122, 2010.
Go to original source... - Heidarvand, L., Amiri, R.M.: What happens in plant molecular responses to cold stress? - Acta Physiol. Plant. 32: 419-431, 2010.
Go to original source... - Hendrickson, L., Furbank, R.T., Chow, W.S.: A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. - Photosynth. Res. 82: 73-81, 2004.
Go to original source... - Hu, L., Xiang, L., Li, Z., Zhou, X., Zou, Z., Hu, X., Wu, K.: The photoprotective role of spermidine in tomato seedlings under salinity-alkalinity stress. - Plos ONE 9: e110855, 2014.
Go to original source... - Hu, W.H., Wu, Y., Zeng, J.Z., He, L., Zeng, Q.M.: Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. - Photosynthetica 48: 537-544, 2010.
Go to original source... - Jahns, P., Holzwarth, A.: The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. - Biochim. biophys. Acta 1817: 182-193, 2011.
Go to original source... - Kalisz, A., Jezdinský, A., Pokluda, R., Sękara, A., Grabowska, A., Gil, J.: Impacts of chilling on photosynthesis and chlorophyll pigment content in juvenile basil cultivars. - Hort. Environ. Biotechnol. 57: 330-339, 2016.
Go to original source... - Karashima, Y., Talavera Perez, K., Everaerts, W., Janssens, A., Kwan, K., Vennekens, R., Nilius, B., Voets, T.: TRPA1 acts as a cold sensor in vitro and in vivo. - Proc. nat. Acad. Sci. USA 106: 1273-1278, 2009.
Go to original source... - Kasamo, K., Kagita, F., Yamanishi, H., Sakaki, T.: Low temperature-induced changes in the thermotropic properties and fatty acid composition of the plasma membrane and tonoplast of cultured rice (Oryza sativa L.) cells. - Plant Cell Physiol. 33: 609-616, 1992.
- Kaya, C., Okant, M., Ugurlar, F., Alyemeni, M.N., Ashraf, M., Ahmad, P.: Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. - Chemosphere 225: 627-638, 2019.
Go to original source... - Klughammer, C., Schreiber, U.: Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. - PAN Appl. Notes 1: 27-35, 2008.
- Kromdijk, J., Glowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K., Long, S.P.: Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. - Science 354: 857-861, 2016.
Go to original source... - Kusaba, M., Ito, H., Morita, R., Iida, S., Sato, Y., Fujimoto, M., Kawasaki, S., Tanaka, R., Hirochika, H., Nishimura, M.: Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. - Plant Cell 19: 1362-1375, 2007.
Go to original source... - Lavergne, J., Trissl, H.W.: Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. - Biophys. J. 68: 2474-2492, 1995.
Go to original source... - Li, C., Wang, P., Wei, Z., Liang, D., Ma, F.: The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. - J. Pineal Res. 53: 298-306, 2012.
Go to original source... - Liu, J., Wang, W., Wang, L., Sun, Y.: Exogenous melatonin improves seedling health index and drought tolerance in tomato. - Plant Growth Regul. 77: 317-326, 2015.
Go to original source... - López-Bernal, Á., García-Tejera, O., Vega, V.A., Hidalgo, J.C., Testi, L., Orgaz, F., Villalobos, F.J.: Using sap flow measurements to estimate net assimilation in olive trees under different irrigation regimes. - Irrig. Sci. 33: 357-366, 2015.
Go to original source... - Pu, Y.-J., Cisse, E.H.M., Zhang, L.-J., Miao, L.-F., Nawaz, M., Yang, F.: Coupling exogenous melatonin with Ca2+ alleviated chilling stress in Dalbergia odorifera T. Chen. - Trees 2021: 1-14, 2021.
Go to original source... - Siddiqui, M.H., Alamri, S., Al-Khaishany, M.Y., Khan, M.N., Al-Amri, A., Ali, H.M., Alaraidh, I.A., Alsahli, A.A.: Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. - Int. J. mol. Sci. 20: 353, 2019.
Go to original source... - Siddiqui, M.H., Alamri, S., Nasir Khan, M., Corpas, F.J., Al-Amri, A.A., Alsubaie, Q.D., Ali, H.M., Kalaji, H.M., Ahmad, P.: Melatonin and calcium function synergistically to promote the resilience through ROS metabolism under arsenic-induced stress. - J. Hazard. Mater. 398: 122882, 2020.
Go to original source... - Tuzet, A., Perrier, A., Leuning, R.: A coupled model of stomatal conductance, photosynthesis and transpiration. - Plant Cell Environ. 26: 1097-1116, 2003.
Go to original source... - Wang, M., Zhang, S., Ding, F.: Melatonin mitigates chilling-induced oxidative stress and photosynthesis inhibition in tomato plants. - Antioxidants 9: 218, 2020.
Go to original source... - Wang, M., Duan, S., Zhou, Z., Chen, S., Wang, D.: Foliar spraying of melatonin confers cadmium tolerance in Nicotiana tabacum L. - Ecotox. Environ. Safety 170: 68-76, 2019a.
Go to original source... - Wang, P., Sun, X., Li, C., Wei, Z., Liang, D.: Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. - J. Pineal Res. 54: 292-302, 2012.
Go to original source... - Wang, Y., Wang, G., Zheng, Y., Zheng, Y., Xu, S.: Polyamines are involved in chilling tolerance in tobacco (Nicotiana tabacum) seedlings. - Plant Growth Regul. 89: 153-166, 2019b.
Go to original source... - Xu, P.L., Guo, Y.K., Bai, J.G., Shang, L., Wang, X.J.: Effects of long-term chilling on ultrastructure and antioxidant activity in leaves of two cucumber cultivars under low light. - Physiol. Plant. 132: 467-478, 2008.
Go to original source... - Zhang, N., Zhao, B., Zhang, H.J., Weeda, S., Guo, Y.D.: Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). - J. Pineal Res. 54: 15-23, 2012.
Go to original source... - Zhang, Z., Jia, Y., Gao, H., Zhang, L., Li, H., Meng, Q.: Characterization of PSI recovery after chilling-induced photoinhibition in cucumber (Cucumis sativus L.) leaves. - Planta 234: 883-889, 2011.
Go to original source... - Zhang, Z., Liu, M., Gao, H., Jin, L., Li, Y., Li, Q., Ai, X.: Water status related root-to-shoot communication regulates the chilling tolerance of shoot in cucumber (Cucumis sativus L.) plants. - Sci. Rep. 5: 13094, 2015.
Go to original source... - Zhao, H., Ye, L., Wang, Y., Zhou, X., Yang, J., Wang, J., Cao, K., Zou, Z.: Melatonin increases the chilling tolerance of chloroplast in cucumber seedlings by regulating photosynthetic electron flux and the ascorbate-glutathione cycle. - Front. Plant Sci. 7: 1814, 2016.
Go to original source... - Zhao, H., Zhang, K., Zhou, X., Xi, L., Wang, Y., Xu, H., Pan, T., Zou, Z.: Melatonin alleviates chilling stress in cucumber seedlings by up-regulation of CsZat12 and modulation of polyamine and abscisic acid metabolism. - Sci Rep. 7: 4998, 2017.
Go to original source... - Zou, J.N., Jin, X.J., Wang, Y.X. Effects of melatonin on photosynthesis and soybean seed growth during grain filling under drought stress. - Photosynthetica 57: 512-520, 2019.
Go to original source...



