Skip to main content
Log in

Effect of exogenous melatonin on improvement of chlorophyll content and photochemical efficiency of PSII in mallow plants (Malva parviflora L.) treated with cadmium

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Melatonin is a growth regulator that improves the growth and chlorophyll (chl) content in plants. This study aims to investigate the effect of melatonin pretreatment on chl synthesis and fluorescence parameters in Malva parviflora exposed to cadmium (Cd). The 42-day-old plants were transferred to nutrient solutions containing 50 μM melatonin. After two days, some plants were exposed to 50 μM Cd. Eight days after Cd treatment, some indicators related to chl fluorescence and some biochemical parameters were measured. In this study, melatonin increased chl content and chl a/pheophytin a (pheo a) ratio, chlorophyllide a (chlide a), porphyrin compounds, and 5-aminolevulinic acid (5-ALA) in the presence of Cd. However, it decreased chl a/chlide a ratio under these conditions. Whereas Cd treatment resulted in significant reductions in photochemical activity and electron transfer rate in PSII, melatonin improved photochemical efficiency of PSII by reducing the toxic effect of Cd on the activity of the oxygen evolving complex (OEC) on the electron donor site and reducing non-photochemical quenching (NPQ). Based on the results, it appears that melatonin can maintain the chl content of plants exposed to Cd by increasing the precursors of the chl biosynthesis pathway and reducing its degradation rate. These results may, at least in our experimental conditions, partly explain the reason for the improved yield and growth of Cd-exposed plants when pretreated with melatonin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

5-ALA:

5-Aminolevulinic acid

Cd:

Cadmium

Chl:

Chlorophyll

Chlide:

Chlorophyllide

ETR:

The relative electron transfer rate

Pheo:

Pheophytin

Proto:

Protoporphyrin

Pchlide:

Protochlorophyllide

FW:

Fresh weight

Mg-Proto:

Magnesium-protoporphyrin

NPQ:

Non-photochemical quenching

NBT:

Nitroblue tetrazolium

OEC:

Oxygen evolving complex

ROS:

Reactive oxygen species

qP:

Photochemical quenching

ΦPSII:

The effective quantum yield of PSII photochemistry

References

  • Arnao MB, Hernández-Ruiz J (2014) Melatonin: plant growth regulator and/or biostimulator during stress? Trends Plant Sci 19(12):789–797

    Article  CAS  Google Scholar 

  • Ayyaz A, Amir M, Umer S, Iqbal M, Bano H et al (2020) Melatonin induced changes in photosynthetic efficiency as probed by OJIP associated with improved chromium stress tolerance in canola (Brassica napus L.). Heliyon 6(7):e04364

    Article  Google Scholar 

  • Blankenship RE (2002) Photosynthetic pigments: Structure and spectroscopy. In: Blankenship RE (ed) Molecular mechanisms of photosynthesis. Blackwell Publishing, Oxford, pp 42–60

    Chapter  Google Scholar 

  • Bose SK, Howlader P (2020) Melatonin plays multifunctional role in horticultural crops against environmental stresses: a review. Environ Exp Bot 176:104063

    Article  CAS  Google Scholar 

  • Ding F, Liu B, Zhang S (2017) Exogenous melatonin ameliorates cold-induced damage in tomato plants. Sci Hortic 219:264–271

    Article  CAS  Google Scholar 

  • Dobrikova AG, Apostolova EL, Hanć A, Yotsova E, Borisova P et al (2021) Cadmium toxicity in Salvia sclarea L.: An integrative response of element uptake, oxidative stress markers, leaf structure, and photosynthesis. Ecotoxicol Environ Saf 209:111851

    Article  CAS  Google Scholar 

  • Dong Y, Chen W, Xu L, Kong J, Liu S, He Z (2016) Nitric oxide can induce tolerance to oxidative stress of peanut seedling under cadmium toxicity. Plant Growth Regul 79(1):19–28

    Article  CAS  Google Scholar 

  • Farouk S, Al-Amri SM (2019) Exogenous melatonin-mediated modulation of arsenic tolerance with improved accretion of secondary metabolite production, activating antioxidant capacity and improved chloroplast ultrastructure in rosemary herb. Ecotoxicol Environ Saf 180:333–347

    Article  CAS  Google Scholar 

  • Gill SS, Khan NA, Tuteja N (2012) Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.). Plant Sci 182:112–120

    Article  CAS  Google Scholar 

  • Grajek H, Rydzyński D, Piotrowicz-Cieślak A, Herman A, Maciejczyk M, Wieczorek Z (2020) Cadmium ion-chlorophyll interaction-Examination of spectral properties and structure of the cadmium chlorophyll complex and their relevance to photosynthesis inhibition. Chemosphere 261:127434

    Article  CAS  Google Scholar 

  • Harpaz-Saad S, Azoulay T, Arazi T, Ben-Yaakov E, Mett A et al (2007) Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 19(3):1007–1022

    Article  CAS  Google Scholar 

  • Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta Bioenerg 1807(8):977–988

    Article  Google Scholar 

  • Huihui Z, Xin L, Zisong X, Yue W, Zhiyuan T et al (2020) Toxic effects of heavy metals Pb and Cd on mulberry (Morus alba L.) seedling leaves: photosynthetic function and reactive oxygen species (ROS) metabolism responses. Ecotoxicol Environ Saf 195:110469

    Article  Google Scholar 

  • Kim S, Schlicke H, Van Ree K, Karvonen K, Subramaniam A et al (2013) Arabidopsis chlorophyll biosynthesis: an essential balance between the methylerythritol phosphate and tetrapyrrole pathways. Plant Cell 25(12):4984–4993

    Article  CAS  Google Scholar 

  • Janas KM, Posmyk MM (2013) Melatonin, an underestimated natural substance with great potential for agriculture application. Acta Physiol Plant 35:3285–3292

    Article  CAS  Google Scholar 

  • Kaya C, Okant M, Ugurlar F, Alyemeni MN, Ashraf M, Ahmad P (2019) Melatonin-mediated nitric oxide improves tolerance to cadmium toxicity by reducing oxidative stress in wheat plants. Chemosphere 225:627–638

    Article  CAS  Google Scholar 

  • Lerner AB, Case JD, Takahashi Y, Lee TH, Mori W (1958) Isolation of melatonin, the pineal gland factor that lightens melanocytes. J Am Chem 80:2587–2592

    Article  CAS  Google Scholar 

  • Li J, Ding D, Li N, Xie J, Yu J et al (2022) Melatonin enhances the low-temperature combined low-light tolerance of pepper (Capsicum annuum L.) seedlings by regulating photosynthesis, carotenoid, and hormone metabolism. Environ Exp Bot 199:104868

    Article  CAS  Google Scholar 

  • Li X, Li MH, Deng WW, Ahammed GJ, Wei JP et al (2020) Exogenous melatonin improves tea quality under moderate high temperatures by increasing epigallocatechin-3-gallate and theanine biosynthesis in Camellia sinensis L. J Plant Physiol 253:153273

    Article  CAS  Google Scholar 

  • Liang D, Shen Y, Ni Z, Wang Q, Lei Z et al (2018) Exogenous Melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids. Front Plant Sci 9:426

    Article  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protoc Food Anal Chem. https://doi.org/10.1002/0471142913.faf0403s01

    Article  Google Scholar 

  • Lin S, Song XF, Mao HT, Li SQ, Gan JY et al (2022) Exogenous melatonin improved photosynthetic efficiency of photosystem II by reversible phosphorylation of thylakoid proteins in wheat under osmotic stress. Front Plant Sci 13:966181. https://doi.org/10.3389/fpls.2022.966181

    Article  Google Scholar 

  • Liu K, Jing T, Wang Y, Ai X, Bi H (2022a) Melatonin delays leaf senescence and improves cucumber yield by modulating chlorophyll degradation and photoinhibition of PSII and PSI. Environ Exp Bot 200:104915

    Article  CAS  Google Scholar 

  • Liu L, Wang Z, Gai Z, Wang Y, Wang B et al (2022b) Exogenous application of melatonin improves salt tolerance of sugar beet (Beta vulgaris L.) seedlings. Acta Physiol Plant 44:57. https://doi.org/10.1007/s11738-022-03389-4

    Article  CAS  Google Scholar 

  • Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55(1):64–69

    Article  CAS  Google Scholar 

  • Mandal R, Dutta G (2020) From photosynthesis to biosensing: chlorophyll proves to be a versatile molecule. Sens Int 1:100058

    Article  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence- a practical guide. J Exp Bot 51:659–668

    Article  CAS  Google Scholar 

  • Moustakas M, Bayçu G, Sperdouli I, Eroğlu H, Eleftheriou EP (2020) Arbuscular mycorrhizal symbiosis enhances photosynthesis in the medicinal herb Salvia fruticosa by improving photosystem II photochemistry. Plants 9(8):962

    Article  CAS  Google Scholar 

  • Nawaz MA, Jiao Y, Chen C, Shireen F, Zheng Z et al (2018) Melatonin pretreatment improves vanadium stress tolerance of watermelon seedlings by reducing vanadium concentration in the leaves and regulating melatonin biosynthesis and antioxidant-related gene expression. J Plant Physiol 220:115–127

    Article  CAS  Google Scholar 

  • Özfidan-Konakcia C, Yildiztugay E, Bahtiyar M, Kucukoduk M (2018) The humic acid-induced changes in the water status, chlorophyll fluorescence and antioxidant defense systems of wheat leaves with cadmium stress. Ecotoxicol Environ Saf 155:66–75

    Article  Google Scholar 

  • Radojevič M, Bashkin VN (1999) Water analysis (chapter 4). In: Radojevič M, Bashkin VN (eds) Practical environmental analysis, 2nd edn. RSC Publishing, UK, Cambridge, pp 138–273

    Chapter  Google Scholar 

  • Roy M, Niu J, Irshad A, AbdulKareem H, UlHassan M et al (2021) Exogenous melatonin protects alfalfa (Medicago sativa L.) seedlings from drought-induced damage by modulating reactive oxygen species metabolism, mineral balance and photosynthetic efficiency. Plant Stress 2:100044

    Article  CAS  Google Scholar 

  • Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hortic 103(1):93–99

    Article  CAS  Google Scholar 

  • Sarropoulou V, Dimassi-Theriou K, Therios I, Koukourikou-Petridou M (2012) Melatonin enhances root regeneration, photosynthetic pigments, biomass, total carbohydrates, and proline content in the cherry rootstock PHL-C (Prunus avium× Prunus cerasus). Plant Physiol Biochem 61:162–168

    Article  CAS  Google Scholar 

  • Schelbert S, Aubry S, Burla B, Agne B, Kessler F et al (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21(3):767–785

    Article  CAS  Google Scholar 

  • Sherin G, Raj Aswathi KP, Puthur JT (2022) Photosynthetic functions in plants subjected to stresses are positively influenced by priming. Plant Stress 4:100079

    Article  CAS  Google Scholar 

  • Shahabivand S, Parvaneh A, Aliloo AA (2017) Root endophytic fungus Piriformospora indica affected growth, cadmium partitioning and chlorophyll fluorescence of sunflower under cadmium toxicity. Ecotoxicol Environ Saf 145:496–502

    Article  CAS  Google Scholar 

  • Shah Jahan MS, Guo S, Baloch AR, Sun J, Shu S et al (2020) Melatonin alleviates nickel phytotoxicity by improving photosynthesis, secondary metabolism and oxidative stress tolerance in tomato seedlings. Ecotoxicol Environ Saf 197:110593

    Article  Google Scholar 

  • Sharma A, Wang J, Xu D, Tao S, Chong S et al (2020) Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants. Sci Total Environ 713:136675

    Article  CAS  Google Scholar 

  • Siddiqi MY, Glass ADM, Ruth TJ, Rufty TW (1990) Studies of the uptake of nitrate in barley: I. Kinetics of 13NO3 influx. Plant Physiol 93(4):1426–1432

    Article  CAS  Google Scholar 

  • Su Y, Qin C, Begum N, Ashraf M, Zhang L (2020) Acetylcholine ameliorates the adverse effects of cadmium stress through mediating growth, photosynthetic activity and subcellular distribution of cadmium in tobacco (Nicotiana benthamiana). Ecotoxicol Environ Saf 198:110671

    Article  CAS  Google Scholar 

  • Szafrańska K, Reiter RJ, Posmyk MM (2017) Melatonin improves the photosynthetic apparatus in pea leaves stressed by paraquat via chlorophyll breakdown regulation and its accelerated de novo synthesis. Front Plant Sci 8:878

    Article  Google Scholar 

  • Tang L, Yang RR, Jiang D, Zeng XW, Morel JL et al (2013) Impaired leaf CO2 diffusion mediates Cd induced inhibition of photosynthesis in the Zn/Cd hyperaccumulator Picris divaricata. Plant Physiol Biochem 73:70–76

    Article  CAS  Google Scholar 

  • Tousi S, Zoufan P, Rahnama Ghahfarrokhie A (2020) Alleviation of cadmium-induced phytotoxicity and growth improvement by exogenous melatonin pretreatment in mallow (Malva parviflora) plants. Ecotoxicol Environ Saf 206:111403

    Article  CAS  Google Scholar 

  • Turan S, Tripathy BC (2015) Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiol Plant 153(3):477–491

    Article  CAS  Google Scholar 

  • Wang G, Xing M, Hu T, Ji M, Li X et al (2022) Photosystem II photochemical adjustment of tall fescue against heatstress after melatonin priming. J Plant Physiol 275:153758

    Article  CAS  Google Scholar 

  • Wang P, Sun X, Li C, Wei Z, LiangD MF et al (2013) Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. J Pineal Res 54(3):292–302

    Article  CAS  Google Scholar 

  • Weeda S, Zhang N, Zhao X, Ndip G, Guo Y et al (2014) Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS ONE 9(3):e93462

    Article  Google Scholar 

  • Wei Z, Li C, Gao T, Zhang Z, Liang B et al (2019) Melatonin increases the performance of Malus hupehensis after UV-B exposure. Plant Physiol Biochem 139:630–641

    Article  CAS  Google Scholar 

  • Wu S, Wang Y, Zhang J, Gong X, Zhang Z et al (2021) Exogenous melatonin improves physiological characteristics and promotes growth of strawberry seedlings under cadmium stress. Hortic Plant J 7(1):13–22

    Article  CAS  Google Scholar 

  • Yan F, Zhang J, Li W, Ding Y, Zhong Q et al (2021) Exogenous melatonin alleviates salt stress by improving leaf photosynthesis in rice seedlings. Plant Physiolo Biochem 163:367–375

    Article  CAS  Google Scholar 

  • Yotsova E, Dobrikova A, Stefanov M, Misheva S, Bardáčová M et al (2020) Effects of cadmium on two wheat cultivars depending on different nitrogen supply. Plant Physiol Biochem 155:789–799

    Article  CAS  Google Scholar 

  • Zhang H, Xu Z, Huo Y, Guo K, Wang Y et al (2020a) Overexpression of Trx CDSP32 gene promotes chlorophyll synthesis and photosynthetic electron transfer and alleviates cadmium-induced photoinhibition of PSII and PSI in tobacco leaves. J Hazard Mater 398:122899

    Article  CAS  Google Scholar 

  • Zhang H, Xu Z, Guo K, Huo Y, He G et al (2020b) Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicol Environ Saf 202:110856

    Article  CAS  Google Scholar 

  • Zhang H, Xu N, Li X, Long J, Sui X et al (2018) Arbuscular mycorrhizal fungi (Glomus mosseae) improves growth, photosynthesis and protects photosystem II in leaves of Lolium perenne L. under cadmium contaminated soil. Front Plant Sci 9:1156

    Article  Google Scholar 

  • Zhang H, Zhong H, Wang J, Sui X, Xu N (2016) Adaptive changes in chlorophyll content and photosynthetic features to low light in Physocarpus amurensis Maxim and Physocarpus opulifolius “Diabolo. Peer J 4(3):e2125

    Article  Google Scholar 

  • Zheng X, Tan DX, Allan AC, Zuo B, Zhao Y et al (2017) Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress. Sci Rep 7:41236

    Article  CAS  Google Scholar 

  • Zoufan P, Azad Z, Rahnama Ghahfarokhie A, Kolahi M (2020) Modification of oxidative stress through changes in some indicators related to phenolic metabolism in Malva parviflora L. exposed to cadmium. Ecotoxicol Environ Saf 187:109811

    Article  CAS  Google Scholar 

  • Zoufan P, Jalali R, Hassibi P, Neisi E, Rastegarzadeh S (2018) Evaluation of antioxidant bioindicators and growth responses in Malva parviflora L. exposed to cadmium. Physiol Mol Biol Plants 24(6):1005–1016

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Research Affairs of Shahid Chamran University of Ahvaz [Grant number: SCU.SB99.746].

Author information

Authors and Affiliations

Authors

Contributions

PZ designed and conducted the research and wrote the paper original draft. MRZB helped to measure and analyze fluorescence indices. ST performed all the assessments related to growth and biochemical parameters. AR helped as consultant to carry out measurement protocols. All authors revised the manuscript and approved submission of this work.

Corresponding author

Correspondence to Parzhak Zoufan.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. The authors declare no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zoufan, P., Zare Bavani, M.R., Tousi, S. et al. Effect of exogenous melatonin on improvement of chlorophyll content and photochemical efficiency of PSII in mallow plants (Malva parviflora L.) treated with cadmium. Physiol Mol Biol Plants 29, 145–157 (2023). https://doi.org/10.1007/s12298-022-01271-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-022-01271-8

Keywords

Navigation