Abstract
The beneficial roles of melatonin in plants have been widely reported, but its effect on photosynthesis under drought stress is not clear. In the study, correlated tests were performed to discover melatonin part on photosynthesis in maize (Zea mays L.) seedlings leaves during drought stress. The results showed that melatonin application can mitigate the drought stress-induced damage by protecting chloroplast membrane structure and physiological function. Under drought stress condition, melatonin-treated plants maintained higher photosynthetic rate (Pn), stomatal conductance (gs), intercellular CO2 concentration (Ci) and transpiration rate (Tr). The photosystem I (PSI) reaction central proteins-encoding genes (psaA/psaB), cytochrome b6/f complex subunits-encoding genes (petA/petB), photosystem II (PSII) reaction central proteins-encoding genes (psbA/psbB), PSII antenna proteins-encoding genes (psbC/psbD) and photosynthetic enzymes (phosphoenolpyruvate carboxylase (PEPC), pyruvate phosphate dikinase (PPDK), NADP-malic enzyme (NADP-ME) and ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco)) activity were enhanced. These evidences suggested that exogenous melatonin significantly increased the effective quantum yield and electron transport rate on PSII and PSI, but also decreased energy dissipation and donor and acceptor side impairment on PSI. To sum up, our study provides new insights to further investigate melatonin regulation mechanism on enhancement maize seedings drought tolerance.






Similar content being viewed by others
REFERENCES
Daryanto, S., Wang, L.X., and Jacinthe, P.A., Global synthesis of drought effects on maize and wheat production, PLoS One, 2016, vol. 11, p. e0156362. https://doi.org/10.1371/journal.pone.0156362
Zhang, N., Sun, Q.Q., Zhang, H.J., Cao, Y.J., Weeda, S., Ren, S.X., and Guo, Y.D., Roles of melatonin in abiotic stress resistance in plants, J. Exp. Bot., 2015, vol. 66, p. 647. https://doi.org/10.1093/jxb/eru336
Campos, H., Trejo, C., Peña-Valdivia, C.B., García-Nava, R., Conde-Martínez, F.V., and Cruz-Ortega, M.R., Stomatal and non-stomatal limitations of bell pepper (Capsicum annuum L.) plants under water stress and re-watering: delayed restoration of photosynthesis during recovery, Environ. Exp. Bot., 2014, vol. 98, p. 56. https://doi.org/10.1016/j.envexpbot.2013.10.015
Lara, M.V., Chuong, S.D.X., Akhani, H., Andreo, C.S., and Edwards, G.E., Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species, Plant Physiol., 2006, vol. 142, p. 673. https://doi.org/10.1104/pp.106.085829
Arnao, M.B. and Hernández-Ruiz, J., Functions of melatonin in plants: a review, J. Pineal Res., 2015, vol. 59, p. 133. https://doi.org/10.1111/jpi.12253
Cui, G.B., Zhao, X.X., Liu, S.D., Sun, F.L., Zhang, C., and Xi, Y.J., Beneficial effects of melatonin in overcoming drought stress in wheat seedlings, Plant Physiol. Biochem., 2017, vol. 118, p. 138. https://doi.org/10.1016/j.plaphy.2017.06.014
Liu, J.L., Wang, W.X., Wang, L.Y., and Sun, Y., Exogenous melatonin improves seedling health index and drought tolerance in tomato, Plant Growth Regul., 2015, vol. 77, p. 317. https://doi.org/10.1007/s10725-015-0066-6
Yang, X.L., Xu, H., Li, D., Gao, X., Li, T.L., and Wang, R., Effect of melatonin priming on photosynthetic capacity of tomato leaves under low-temperature stress, Photosynthetica, 2018, vol. 56, p. 884. https://doi.org/10.1007/s11099-017-0748-6
Arnao, M.B. and Hernández-Ruiz, J., Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves, J. Pineal Res., 2009, vol. 46, p. 58. https://doi.org/10.1111/j.1600-079X.2008.00625.x
Lu, H.D., Xue, J.Q., and Guo, D.W., Efficacy of planting date adjustment as a cultivation strategy to cope with drought stress and increase rainfed maize yield and water-use efficiency, Agric. Water Manage., 2017, vol. 179, p. 227. https://doi.org/10.1016/j.agwat.2016.09.001
Song, H., Li, Y.B., Zhou, L., Xu, Z.Z., and Zhou, G.S., Maize leaf functional responses to drought episode and re-watering, Agric. For. Meteorol., 2018, vol. 249, p. 57. https://doi.org/10.1016/j.agrformet.2017.11.023
Wang, D., Heckathorn, S.A., Barua, D., Joshi, P., Hamilton, E.W., and Lacroix, J.J., Effects of elevated CO2 on the tolerance of photosynthesis to acute heat stress in C3, C4, and CAM species, Am. J. Bot., 2008, vol. 95, p. 165. https://doi.org/10.3732/ajb.95.2.165
Meng, J.F., Xu, T.F., Wang, Z.Z., Fang, Y.L., Xi, Z.M., and Zhang, Z.W., The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology, J. Pineal Res., 2015, vol. 57, p. 200. https://doi.org/10.1111/jpi.12159
Markwell, J., Osterman, J.C., and Mitchell, J.L., Calibration of the Minolta SPAD-502 leaf chlorophyll meter, Photosynth. Res., 1995, vol. 46, p. 467. https://doi.org/10.1007/BF00032301
Zhou, R.H., Kan, X., Chen, J.J., Hua, H.L., Li, Y., Ren, J.J., Feng, K., Liu, H.H., Deng, D.X., and Yin, Z.T., Drought-induced changes in photosynthetic electron transport in maize probed by prompt fluorescence, delayed, P700 and cyclic electron flow signals, Environ. Exp. Bot., 2019, vol. 158, p. 51. https://doi.org/10.1016/j.envexpbot.2018.11.005
Wang, P., Sun, X., Li, C., Wei, Z.W., Liang, D., and Ma, F.W., Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple, J. Pineal Res., 2013, vol. 54, p. 292. https://doi.org/10.1111/jpi.12017
Fan, J.B., Hu, Z.G., Xie, Y., Chan Z.L., Chen, K., Amombo, E., Chen, L., and Fu, J.M., Alleviation of cold damage to photosystem II and metabolisms by melatonin in bermudagrass, Front. Plant Sci., 2015, vol. 6, p. 925. https://doi.org/10.3389/fpls.2015.00925
Huang, B., Chen, Y. E., Zhao, Y.Q., Ding, C.B., Liao, J.Q., Hu, C., Zhou, L.J., Zhang, Z.W., Yuan, S., and Yuan, M., Exogenous melatonin alleviates oxidative damages and protects photosystem II in maize seedlings under drought stress, Front. Plant Sci., 2019, vol. 10, p. 677. https://doi.org/10.3389/fpls.2019.00677
Tomar, R.S. and Jajoo, A. PSI becomes more tolerant to fluoranthene through the initiation of cyclic electron flow, Funct. Plant Biol., 2017, vol. 44, p.978. https://doi.org/10.1071/FP17121
Nishiyama, Y., Allakhverdiev, S.I., and Murata, N., Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II, Physiol. Plant., 2011, vol. 142, p. 35. https://doi.org/10.1111/j.1399-3054.2011.01457.x
Seki, M., Umezawa, T., Urano, K., and Shinozaki, K., Regulatory metabolic networks in drought stress responses, Curr. Opin. Plant Biol., 2007, vol. 10, p. 296. https://doi.org/10.1016/j.pbi.2007.04.014
Taylor, L., Nunes-Nesi, A., Parsley, K., Leiss, A., Leach, G., Coates, S., Wingler, A., Fernie, A.R., and Hibberd, J.M., Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content, Plant J., 2010, vol. 62, p. 641. https://doi.org/10.1111/j.1365-313X.2010.04179.x
Doubnerová, V., Müller, K., Čeřovská, N., Synková, H., Spoustová, P., and Ryšlavá, H., Effect of Potato virus Y on the NADP-malic enzyme from Nicotiana tabacum L.: mRNA, expressed protein and activity, Int. J. Mol. Sci., 2009, vol. 10, p. 3583. https://doi.org/10.3390/ijms10083583
Valderrama, R., Corpas, F.J., Carreras, A., Gomez-Rodriguez, M.V., Chaki, M., Pedrajas, J.R., Fernandez-Ocana, A., Del Rio, L.A.D., and Barroso, J.B., The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants, Plant Cell Environ., 2006, vol. 29, p. 1449. https://doi.org/10.1111/j.1365-3040.2006.01530.x
Chojak-Kozniewska, J., Kuzniak, E., Linkiewicz, A., and Sowa, S., Primary carbon metabolism-related changes in cucumber exposed to single and sequential treatments with salt stress and bacterial infection, Plant Physiol. Biochem., 2018, vol. 123, p. 160. https://doi.org/10.1016/j.plaphy.2017.12.015
Laporte, M.M., Shen, B., and Tarczynski, M.C., Engineering for drought avoidance: expression of maize NADP-malic enzyme in tobacco results in altered stomatal function, J. Exp. Bot., 2002, vol. 53, p. 699. https://doi.org/10.1093/jexbot/53.369.699
Reddy, A.R., Chaitanya, K.V., and Vivekanandan, M., Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants, J. Plant Physiol., 2004, vol. 161, p. 1189. https://doi.org/10.1016/j.jplph.2004.01.013
Weiner, H., Burnell, J.N., Woodrow, I.E., Heldt, H.W., and Hatch, M.D., Metabolite diffusion into bundle sheath cells from C4 plants: relation to C4 photosynthesis and plasmodesmatal function, Plant Physiol., 1988, vol. 88, p. 815. https://doi.org/10.1104/pp.88.3.815
ACKNOWLEDGMENTS
The authors would like to thank all members of the laboratory for their advice and technical assistance.
Funding
This study was founded by National Key Research and Development Program of China (project no. 2017YFD0300304); the Shaanxi Technology Innovation and Guide Project (project no. 2019 TG-002).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests. The authors declare that they have no conflicts of interest.
Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by any of the authors.
Additional information
Abbreviations: Chl—chloroplasts; Ci—intercellular CO2 concentration; ETR(I)—the PSI electron transport rate; ETR(II)—the PSII electron transport rate; gs—stomatal conductance; Mch—mitochondria; NADP-ME-NADP-malic enzyme; PEPC—phosphoenolpyruvate carboxylase; PPDK— pyruvate phosphate dikinase; Pn—photosynthetic rate; PSI— photosystem I; PSII—photosystem II; ROS—reactive oxygen species; Rubisco-ribulose-1,5-bisphosphate carboxylase/oxygenase; Tr—transpiration rate; V—vacuole; Y(II)—the PSII effective quantum yield; Y(NO)—the PSII quantum yield of non-regulatory energy dissipation; Y(NPQ)—the PSII quantum yield of regulatory energy dissipation; Y(I)—the PSI effective quantum yield; Y(ND)—the PSI quantum yield of non-photochemical energy dissipation due to donor side limitation; Y(NA)—the PSI quantum yield of non-photochemical energy dissipation due to accept or side limitation.
Supplementary Information
Rights and permissions
About this article
Cite this article
Wang, Y.F., Guo, Y.Y., Zhao, C.F. et al. Exogenous Melatonin Achieves Drought Tolerance by Improving Photosynthesis in Maize Seedlings Leaves. Russ J Plant Physiol 68, 718–727 (2021). https://doi.org/10.1134/S102144372104021X
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S102144372104021X


