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Plant function and evolutionary biology
RESEARCH ARTICLE

Melatonin improves the photosynthesis in Dracocephalum kotschyi under salinity stress in a Ca2+/CaM-dependent manner

Farinaz Vafadar A , Rayhaneh Amooaghaie https://orcid.org/0000-0002-8575-5407 A B * , Parviz Ehsanzadeh https://orcid.org/0000-0003-1754-6838 C and Faezeh Ghanati https://orcid.org/0000-0002-2901-0152 D
+ Author Affiliations
- Author Affiliations

A Plant Biology Department, Faculty of Science, Shahrekord University, Shahrekord, Iran.

B Biotechnology Research Institute, Shahrekord University, Shahrekord, Iran.

C Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan University of Technology, Isfahan, 84156-83111, Iran.

D Department of Plant Biology, Faculty of Biological Science, Tarbiat Modares University (TMU), POB 14115-154, Tehran, Iran.

* Correspondence to: rayhanehamooaghaie@yahoo.com

Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 49(1) 89-101 https://doi.org/10.1071/FP21233
Submitted: 7 August 2021  Accepted: 21 October 2021   Published: 19 November 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

This study investigated: (1) the effects of various concentrations of melatonin (MT) and Ca2+; and (2) the impact of crosstalk between these signal molecules on photosynthesis and salt tolerance of Dracocephalum kotschyi Boiss. Results indicated that 5 mM CaCl2, as well as 100 μM MT were the best concentrations for increasing shoot dry weight, leaf area, SPAD index, maximum quantum efficiency of photosystem II (Fv/Fm), and decreasing malondialdehyde content under salinity stress. The impact of MT on growth and photosynthesis was closely linked to its effect on enhancing antioxidant enzyme activities in leaves. Application of p-chlorophenylalanine, as an inhibitor of MT biosynthesis, negated the impacts of MT on the aforementioned attributes. Salinity and MT boosted cytosolic Ca2+ concentration. Exogenous MT, as well as Ca2+, enhanced tolerance index, membrane stability, leaf area, the content of chlorophyll (Chl) a, Chl b, and carotenoids (Car), Fv/Fm, and stomatal conductance under salinity stress. These impacts of MT were eliminated by applying a calmodulin antagonist, a Ca2+ chelator and a Ca2+ channel blocker. These novel findings indicate that the MT-induced effects on photosynthetic parameters and salt-evoked oxidative stress were mediated through calcium/calmodulin (Ca2+/CaM) signalling.

Keywords: antioxidant response, calcium/calmodulin, Dracocephalum kotschyi, melatonin, photosynthesis, relative water content, salinity stress, signaling.


References

Abdehpour Z, Ehsanzadeh P (2019) Concurrence of ionic homeostasis alteration and dry mass sustainment in emmer wheats exposed to saline water: implications for tackling irrigation water salinity. Plant and Soil 440, 427–441.
Concurrence of ionic homeostasis alteration and dry mass sustainment in emmer wheats exposed to saline water: implications for tackling irrigation water salinity.Crossref | GoogleScholarGoogle Scholar |

Alharbi BM, Elhakem AH, Alnusairi GSH, Mona H, Soliman MH, Hakeem KR, Hasan MM, Abdelhamid MT (2021) Exogenous application of melatonin alleviates salt stress-induced decline in growth and photosynthesis in Glycine max (L.) seedlings by improving mineral uptake, antioxidant and glyoxalase system. Plant, Soil and Environment 67, 208–220.
Exogenous application of melatonin alleviates salt stress-induced decline in growth and photosynthesis in Glycine max (L.) seedlings by improving mineral uptake, antioxidant and glyoxalase system.Crossref | GoogleScholarGoogle Scholar |

Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. Journal of Photochemistry and Photobiology B: Biology 104, 1–8.
Recent progress in the studies of structure and function of photosystem II.Crossref | GoogleScholarGoogle Scholar |

Allakhverdiev SI (2020) Optimising photosynthesis for environmental fitness. Functional Plant Biology 47, iii–vii.
Optimising photosynthesis for environmental fitness.Crossref | GoogleScholarGoogle Scholar | 33046183PubMed |

Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1657, 23–32.
Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage–repair cycle of photosystem II in Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar |

Allakhverdiev SI, Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynthesis Research 98, 529–539.
Salt stress inhibits photosystems II and I in cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 18670904PubMed |

Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiology 130, 1443–1453.
Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis.Crossref | GoogleScholarGoogle Scholar | 12428009PubMed |

Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiology 123, 1047–1056.
Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp.Crossref | GoogleScholarGoogle Scholar | 10889254PubMed |

Amooaghaie R, Tabatabaie F (2017) Osmopriming-induced salt tolerance during seed germination of alfalfa most likely mediates through H2O2 signaling and upregulation of heme oxygenase. Protoplasma 254, 1791–1803.
Osmopriming-induced salt tolerance during seed germination of alfalfa most likely mediates through H2O2 signaling and upregulation of heme oxygenase.Crossref | GoogleScholarGoogle Scholar | 28093607PubMed |

Arnao MB, Hernández-Ruiz J (2019) Melatonin and reactive oxygen and nitrogen species: a model for the plant redox network. Melatonin Research 2, 152–168.
Melatonin and reactive oxygen and nitrogen species: a model for the plant redox network.Crossref | GoogleScholarGoogle Scholar |

Białasek M, Górecka M, Mittler R, Karpiński S (2017) Evidence for the involvement of electrical, calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis. Plant Cell Physiology 58, 207–215.
Evidence for the involvement of electrical, calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 28184891PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |

Cha-um S, Singh HP, Samphumphuang T, Kirdmanee C (2012) Calcium-alleviated salt tolerance in indica rice (Oryza sativa L. spp. indica): physiological and morphological changes. Australian Journal of Crop Science 6, 176–182.

Chen Y-E, Mao J-J, Sun L-Q, Huang B, Ding C-B, Gu Y, Liao J-Q, Hu C, Zhang Z-W, Yuan S, Yuan M (2018) Plant Physiology 164, 349–363.
Crossref | GoogleScholarGoogle Scholar |

Demidchik V, Shabala S (2017) Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ Hub’. Functional Plant Biology 45, 9–27.
Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ Hub’.Crossref | GoogleScholarGoogle Scholar |

Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Science 135, 1–9.
Antioxidant responses of rice seedlings to salinity stress.Crossref | GoogleScholarGoogle Scholar |

Erland LAE, Saxena PK, Murch SJ (2017) Melatonin in plant signalling and behavior. Functional Plant Biology 45, 58–69.
Melatonin in plant signalling and behavior.Crossref | GoogleScholarGoogle Scholar |

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |

Hu W, Kong H, Guo Y, Zhang Y, Ding Z, Tie W, Yan Y, Huang Q, Peng M, Shi H, Guo A (2016) Comparative physiological and transcriptomic analyses reveal the actions of melatonin in the delay of postharvest physiological deterioration of cassava. Frontiers in Plant Science 7, 736
Comparative physiological and transcriptomic analyses reveal the actions of melatonin in the delay of postharvest physiological deterioration of cassava.Crossref | GoogleScholarGoogle Scholar | 27303428PubMed |

Huang L, Li Z, Pan S, Liu Q, Pu G, Zhang Y, Li J (2019) Ameliorating effects of exogenous calcium on the photosynthetic physiology of honeysuckle (Lonicera japonica) under salt stress. Functional Plant Biology 46, 1103–1113.
Ameliorating effects of exogenous calcium on the photosynthetic physiology of honeysuckle (Lonicera japonica) under salt stress.Crossref | GoogleScholarGoogle Scholar | 31581977PubMed |

Jabs T, Dietrich RA, Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853–1856.
Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide.Crossref | GoogleScholarGoogle Scholar | 8791589PubMed |

Johnson Jr H (1980) ‘Hydroponics: a guide to soilless culture, Leaflet 2947’. (Division of agriculture and natural resources, University of California)

Kabiri R, Hatami A, Oloumi H, Naghizadeh M, Nasibi F, Tahmasebi Z (2018) Foliar application of melatonin induces tolerance to drought stress in Moldavian balm plants (Dracocephalum moldavica) through regulating the antioxidant system. Folia Horticulturae 30, 155–167.
Foliar application of melatonin induces tolerance to drought stress in Moldavian balm plants (Dracocephalum moldavica) through regulating the antioxidant system.Crossref | GoogleScholarGoogle Scholar |

Kader MA, Lindberg S, Seidel T, Golldack D, Yemelyanov V (2007) Sodium sensing induces different changes in free cytosolic calcium concentration and pH in salt-tolerant and-sensitive rice (Oryza sativa) cultivars. Physiologiae Plantarum 130, 99–111.
Sodium sensing induces different changes in free cytosolic calcium concentration and pH in salt-tolerant and-sensitive rice (Oryza sativa) cultivars.Crossref | GoogleScholarGoogle Scholar |

Khanjani F, Sajedi RH, Hasannia S (2018) Rapid screening of drug candidates against EGFR/HER2 signaling pathway using fluorescence assay. Analytical and Bioanalytical Chemistry 410, 7827–7835.
Rapid screening of drug candidates against EGFR/HER2 signaling pathway using fluorescence assay.Crossref | GoogleScholarGoogle Scholar | 30338368PubMed |

Khodabakhsh F, Amooaghaie R, Mostajeran A (2014) Effect of hydro- and osmo-priming on membrane deterioration, proline accumulation and H2O2 scavenging enzymes in two salt stressed chickpea cultivars. Environmental Engineering and Management Journal (EEMJ) 13, 619–626.

Landau M, Zisapel N (2007) The low affinity binding of melatonin to calmodulin: use of computational methods to explain its physiological relevance. In ‘Melatonin—from molecules to therapy’. (Eds SR Pandi-Perumal, DP Cardinali) pp. 69–79. (Nova Science)

Li H, Chang J, Chen H, Wang Z, Gu X, Wei C, Zhang Y, Ma J, Yang J, Zhang X (2017) Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Frontiers in Plant Science 8, 295
Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis.Crossref | GoogleScholarGoogle Scholar | 28298921PubMed |

Li J, Yang Y, Sun K, Chen Y, Chen X, Li X (2019) Exogenous melatonin enhances cold, salt and drought stress tolerance by improving antioxidant defense in tea plant (Camellia sinensis (L.) O. Kuntze). Molecules 24, 1826
Exogenous melatonin enhances cold, salt and drought stress tolerance by improving antioxidant defense in tea plant (Camellia sinensis (L.) O. Kuntze).Crossref | GoogleScholarGoogle Scholar |

Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11, 591–592.
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.Crossref | GoogleScholarGoogle Scholar |

Liu N, Gong B, Jin Z, Wang X, Wei M, Yang F, Li Y, Shi Q (2015) Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal. Journal of Plant Physiology 186–187, 68–77.
Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal.Crossref | GoogleScholarGoogle Scholar | 26412100PubMed |

Mohammadi F, Ghanati F, Sharifi M, Chashmi NA (2018) On the mechanism of the cell cycle control of suspension-cultured tobacco cells after exposure to static magnetic field. Plant Science 277, 139–144.
On the mechanism of the cell cycle control of suspension-cultured tobacco cells after exposure to static magnetic field.Crossref | GoogleScholarGoogle Scholar | 30466579PubMed |

Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1767, 414–421.
Photoinhibition of photosystem II under environmental stress.Crossref | GoogleScholarGoogle Scholar |

Nabaei M, Amooaghaie R (2019) Nitric oxide is involved in the regulation of melatonin-induced antioxidant responses in Catharanthus roseus roots under cadmium stress. Botany 97, 681–690.
Nitric oxide is involved in the regulation of melatonin-induced antioxidant responses in Catharanthus roseus roots under cadmium stress.Crossref | GoogleScholarGoogle Scholar |

Pan T, Liu M, Kreslavski VD, Zharmukhamedov SK, Nie C, Yu M, Kuznetsov VV, Allakhverdiev SI, Shabala S (2021) Non-stomatal limitation of photosynthesis by soil salinity. Critical Reviews in Environmental Science and Technology 51, 791–825.
Non-stomatal limitation of photosynthesis by soil salinity.Crossref | GoogleScholarGoogle Scholar |

Sebastiani L, Lindberg S, Vitagliano C (1999) Cytoplasmic free Ca2+ dynamics in single tomato (Lycopersicon esculentum) protoplasts subjected to chilling temperatures. Physiologia Plantarum 105, 239–244.
Cytoplasmic free Ca2+ dynamics in single tomato (Lycopersicon esculentum) protoplasts subjected to chilling temperatures.Crossref | GoogleScholarGoogle Scholar |

Siddiqui MH, Alamri S, Nasir Khan M, Corpas FJ, Al-Amri AA, Alsubaiea QD, Alia HM, Kalajid HM, Ahmada P (2020) Melatonin and calcium function synergistically to promote the resilience through ROS metabolism under arsenic-induced stress. Journal of Hazardous Materials 398, 122882
Melatonin and calcium function synergistically to promote the resilience through ROS metabolism under arsenic-induced stress.Crossref | GoogleScholarGoogle Scholar | 32516727PubMed |

Sukhov V, Sukhova E, Vodeneev V (2019) Long-Distance electrical signals as a link between the local action of stressors and the systemic physiological responses in higher plants. Progress in Biophysics and Molecular Biology 146, 63–84.
Long-Distance electrical signals as a link between the local action of stressors and the systemic physiological responses in higher plants.Crossref | GoogleScholarGoogle Scholar | 30508537PubMed |

Sukhova E, Sukhov V (2021) Electrical signals, plant tolerance to actions of stressors, and programmed cell death: is interaction possible? Plants 10, 1704
Electrical signals, plant tolerance to actions of stressors, and programmed cell death: is interaction possible?Crossref | GoogleScholarGoogle Scholar | 34451749PubMed |

Sukhova E, Mudrilov M, Vodeneev V, Sukhov V (2018) Influence of the variation potential on photosynthetic flows of light energy and electrons in pea. Photosynththesis Research 136, 215–228.
Influence of the variation potential on photosynthetic flows of light energy and electrons in pea.Crossref | GoogleScholarGoogle Scholar |

Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction. Plant Journal 11, 1187–1194.
Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction.Crossref | GoogleScholarGoogle Scholar |

Vafadar F, Amooaghaie R, Ehsanzadeh P, Ghanadian M (2020) Salinity stress alters ion homeostasis, antioxidant activities and the production of rosmarinic acid, luteolin and apigenin in Dracocephalum kotschyi Boiss. Biologia 75, 2147–2158.
Salinity stress alters ion homeostasis, antioxidant activities and the production of rosmarinic acid, luteolin and apigenin in Dracocephalum kotschyi Boiss.Crossref | GoogleScholarGoogle Scholar |

Vaghar M, Ehsanzadeh P (2018) Comparative photosynthetic attributes of emmer and modern wheats in response to water and nitrogen supply. Photosynthetica 56, 1224–1234.
Comparative photosynthetic attributes of emmer and modern wheats in response to water and nitrogen supply.Crossref | GoogleScholarGoogle Scholar |

Valivand M, Amooaghaie R, Ahadi A (2019) Interplay between hydrogen sulfide and calcium/calmodulin enhances systemic acquired acclimation and antioxidative defense against nickel toxicity in zucchini. Environmental and Experimental Botany 158, 40–50.
Interplay between hydrogen sulfide and calcium/calmodulin enhances systemic acquired acclimation and antioxidative defense against nickel toxicity in zucchini.Crossref | GoogleScholarGoogle Scholar |

Varghese N, Alyammahi O, Nasreddine S, Alhassani A, Gururani MA (2019) Melatonin positively influences the photosynthetic machinery and antioxidant system of Avena sativa during salinity stress. Plants 8, 610
Melatonin positively influences the photosynthetic machinery and antioxidant system of Avena sativa during salinity stress.Crossref | GoogleScholarGoogle Scholar |

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151, 59–66.
Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |

Wang G, Bi A, Amombo E, Li H, Zhang L, Cheng C, Hu T, Fu J (2017) Exogenous calcium enhances the photosystem II photochemistry response in salt stressed tall fescue. Frontiers in Plant Science 8, 2032
Exogenous calcium enhances the photosystem II photochemistry response in salt stressed tall fescue.Crossref | GoogleScholarGoogle Scholar | 29250091PubMed |

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.
Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress.Crossref | GoogleScholarGoogle Scholar |

Wang Q, An B, Shi H, Luo H, He C (2017) High concentration of melatonin regulates leaf development by suppressing cell proliferation and endoreduplication in Arabidopsis. International Journal of Molecular Sciences 18, 991
High concentration of melatonin regulates leaf development by suppressing cell proliferation and endoreduplication in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Wang Q, Yang S, Wan S, Li X (2019) The significance of calcium in photosynthesis. International Journal of Molecular Sciences 20, 1353
The significance of calcium in photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Wei J, Li D-X, Zhang J-R, Shan C, Rengel Z, Song Z-B, Chen Q (2018) Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. Journal of Pineal Research 65, e12500
Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 29702752PubMed |

Wungrampha S, Joshi R, Singla-Pareek SL, Pareek A (2018) Photosynthesis and salinity: are these mutually exclusive? Photosynthetica 56, 366–381.
Photosynthesis and salinity: are these mutually exclusive?Crossref | GoogleScholarGoogle Scholar |

Xu D, Wang W, Gao T, Fang X, Gao X, Li J, Bu H, Mu J (2017) Calcium alleviates decreases in photosynthesis under salt stress by enhancing antioxidant metabolism and adjusting solute accumulation in Calligonum mongolicum. Conservation Physiology 5, cox060
Calcium alleviates decreases in photosynthesis under salt stress by enhancing antioxidant metabolism and adjusting solute accumulation in Calligonum mongolicum.Crossref | GoogleScholarGoogle Scholar |

Yang Z, Li J-L, Liu L-N, Xie Q, Sui N (2020) Photosynthetic regulation under salt stress and salt-tolerance mechanism of sweet sorghum. Frontiers in Plant Science 10, 1722
Photosynthetic regulation under salt stress and salt-tolerance mechanism of sweet sorghum.Crossref | GoogleScholarGoogle Scholar | 32010174PubMed |

Zhang T, Shi Z, Zhang X, Zheng S, Wang J, Mo J (2020) Alleviating effects of exogenous melatonin on salt stress in cucumber. Scientia Horticulture 262, 109070

Zheng X, Tan DX, Allan AC, Zuo B, Zhao Y, Reiter RJ, Wang L, Wang Z, Guo Y, Zhou J (2017) Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress. Scientific Reports 7, 41236