Skip to main content
Log in

Melatonin enhances thermotolerance of maize seedlings (Zea mays L.) by modulating antioxidant defense, methylglyoxal detoxification, and osmoregulation systems

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Melatonin (MT), derived from tryptophan, is an amazing signaling molecule with multiple functions in plants. Heat stress (HS) induced by high temperature is a major stress factor that limits metabolism, growth, development, and productivity of plants. However, whether MT could enhance the thermotolerance of maize seedlings and the underlying mechanisms is not completely known. In this study, treatment of maize seedlings with MT enhanced the survival percentage of maize seedlings under HS conditions, mitigated an increase in malondialdehyde (MDA, product of membrane lipid peroxidation) and electrolyte leakage, and improved tissue vitality compared with the control without MT treatment, indicating that MT treatment could enhance the theromotolerance of maize seedlings. To understand the mechanisms underlying MT-enhanced thermotolerance of maize seedlings, the antioxidant defense (guaiacol peroxidease: GPX; glutathione reductase: GR; catalase: CAT; ascorbic acid: AsA; and glutathione: GSH), methylglyoxal (MG) detoxification (glyoxalase I: Gly I; and glyoxalase II: Gly II), and osmoregulation (proline: Pro; trehalose: Tre; and total soluble sugar: TSS) systems were assayed. The results showed that MT treatment stimulated the activities of antioxidant enzymes (GPX, GR, and CAT) and MG detoxification enzymes (Gly I and Gly II), increased the contents of nonenzyme antioxidants (AsA and GSH) and osmolytes (Pro, Tre, and TSS) in maize seedlings under normal culture conditions, and maintained a higher abovementioned enzyme activity and antioxidant and osmolyte contents under HS conditions compared with the control. This work reported that MT could enhance the thermotolerance of maize seedlings by modulating the antioxidant defense, MG detoxification, and osmoregulation systems.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

Abbreviations

AsA:

Ascorbic acid

CAT:

Catalase

DHA:

Oxidized ascorbic acid

FW:

Fresh weight

Gly I:

Glyoxalase I

Gly II:

Glyoxalase II

GPX:

Guaiacol peroxidase

GR:

Glutathione reductase

GSH:

Glutathione

GSSG:

Oxidized glutathione

HS:

Heat stress

HSF:

Heat shock factor

HSP:

Heat shock protein

MDA:

Malondialdehyde

MG:

Methylglyoxal

MT:

Melatonin

Pro:

Proline

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TSS:

Total soluble sugar

Tre:

Trehalose

Trp:

Tryptophan

References

  • Ahammed GJ, Xu W, Liu A, Chen S (2018a) COMT1 silencing aggravates heat stress-induced reduction in photosynthesis by decreasing chlorophyll content, photosystem II activity and electron transport efficiency in tomato. Front Plant Sci 9 (in press)

  • Ahammed GJ, Xu W, Liu A, Chen S (2018b) Endogenous melatonin deficiency aggravates high temperature-induced oxidative stress in Solanum lycopersicum L. Environ Exp Bot 155 (in press)

  • Antoniou C, Chatzimichail G, Xenofontos R, Pavlou JJ, Panagiotou E, Christou A, Fotopoulos V (2017) Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. J Pineal Res 62:e12401

    Article  CAS  Google Scholar 

  • Arnao MB, Hernández-Ruiz J (2009) Protective effect of melatonin against chlorophyll degradation during the senescence of barley leaves. J Pineal Res 46:58–63

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Arnao MB, Hernández-Ruiz J (2015) Functions of melatonin in plants: a review. J Pineal Res 59:133–150

    Article  PubMed  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Back K, Tan DX, Reiter RJ (2016) Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J Pineal Res 61:426–437

    Article  PubMed  CAS  Google Scholar 

  • Bajwa VS, Shukla MR, Sherif SM, Murch SJ, Saxena PK (2014) Role of melatonin in alleviating cold stress in Arabidopsis thaliana. J Pineal Res 56:238–245

    Article  PubMed  CAS  Google Scholar 

  • Bechtold U, Field B (2018) Molecular mechanisms controlling plant growth during abiotic stress. J Exp Bot 69:2753–2758

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dubbels R, Reiter RJ, Klenke E, Goebel E, Schnakenberg E, Ehlers C, Schiwara HW, Schloot W (1995) Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry. J Pineal Res 18:28–31

    Article  PubMed  CAS  Google Scholar 

  • Erland LAE, Saxena PK (2018) Melatonin in plant morphogenesis. In Vitro Cell Devel Biol-Plant 54:3–24

    Article  CAS  Google Scholar 

  • Erland LAE, Saxena PK, Murch SJ (2017) Melatonin in plant signalling and behaviour. Funct Plant Biol 45:58–69

    Article  CAS  Google Scholar 

  • Erland LAE, Shukla MR, Singh AS, Murch SJ, Saxena PK (2018) Melatonin and serotonin: mediators in the symphony of plant morphogenesis. J Pineal Res 64:e12452

    Article  CAS  Google Scholar 

  • Fan J, Xie Y, Zhang Z, Chen L (2018) Melatonin: a multifunctional factor in plants. Int J Mol Sci 19:1528

    Article  PubMed Central  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M, Oku H, Fujita M (2017) Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int J Mol Sci 18:200

    Article  PubMed Central  CAS  Google Scholar 

  • Hattori A, Migitaka H, Iigo M, Itoh M, Yamamoto K, Ohtani-Kaneko R, Hara M, Suzuki T, Reiter RJ (1995) Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochem Mol Biol Int 35:627–634

    PubMed  CAS  Google Scholar 

  • Iqbal N, Nazar R, Khan NA (2016) Osmolytes and plants acclimation to changing environment: emerging omics technologies. Springer, London

    Book  Google Scholar 

  • Ishikawa M, Robertson AJ, Gusta LV (1995) Comparison of viability tests for assessing cross-adaptation to freezing, heat and salt stresses induced by abscisic acid in bromegrass (Bromus inermis Leyss) suspension cultured cells. Plant Sci 107:83–93

    Article  CAS  Google Scholar 

  • Jambunathan N (2010) Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. In: Sunkar R (ed) Plant abiotic tolerance: methods and protocols. Springer, London, pp 291–297

    Chapter  Google Scholar 

  • Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. BMC Genome Biol 18:124

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li ZG (2016) Methylglyoxal and glyoxalase system in plants: old players, new concepts. Bot Rev 82:183–203

    Article  Google Scholar 

  • Li ZG, Duan XQ, Min X, Zhou ZH (2017) Methylglyoxal as a novel signal molecule induces the salt tolerance of wheat by regulating the glyoxalase system, the antioxidant system, and osmolytes. Protoplasma 254:1995–2006

    Article  PubMed  CAS  Google Scholar 

  • Li ZG, Ding XJ, Du PF (2013a) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:41–747

    Article  CAS  Google Scholar 

  • Li ZG, Gong M, Xie H, Yang L, Li J (2012) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185(/186):185–189

    Article  PubMed  CAS  Google Scholar 

  • Li ZG, Luo LJ, Zhu LP (2014a) Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings. Bot Stud 55:20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li ZG, Nie Q, Yang CL, Wang Y, Zhou ZH (2018) Signaling molecule methylglyoxal ameliorates cadmium injury in wheat (Triticum aestivum L) by a coordinated induction of glutathione pool and glyoxalase system. Ecotoxicol Environ Saf 149:101–107

    Article  PubMed  CAS  Google Scholar 

  • Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b) Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:564–1572

    Google Scholar 

  • Li ZG, Yi XY, Li YT (2014b) Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia 69:1001–1009

    CAS  Google Scholar 

  • Li ZG, Yuan LX, Wang QL, Ding ZL, Dong CY (2013c) Combined action of antioxidant defense system and osmolytes in chilling shock-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:2127–2136

    Article  CAS  Google Scholar 

  • Mostofa MG, Ghosh A, Li ZG, Siddiqui MN, Fujita M, Tran LSP (2018) Methylglyoxal—a signaling molecule in plant abiotic stress responses. Free Rad Biol Med 125, in press

  • Mostofa MG, Yoshida N, Fujita M (2014) Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul 73:31–44

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Mahmud JA, Suzuki T, Fujita M (2017) Insights into spermine-induced combined high temperature and drought tolerance in mung bean: osmoregulation and roles of antioxidant and glyoxalase system. Protoplasma 254:445–460

    Article  PubMed  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata, L.) by modulating antioxidant defense and methylglyoxal detoxification system. Environ Exp Bot 112:44–54

    Article  CAS  Google Scholar 

  • Shi H, Tan DX, Reiter RJ, Ye T, Yang F, Chan Z (2015) Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis. J Pineal Res 58:335–342

    Article  PubMed  CAS  Google Scholar 

  • Strable J, Scanlon MJ (2009) Maize (Zea mays): a model organism for basic and applied research in plant biology. Cold Spring Harb Protoc 10(2009):pdb.emo132

    Google Scholar 

  • Sun Q, Zhang N, Wang J, Zhang H, Li D, Shi J, Li R, Weeda S, Zhao B, Ren S, Guo YD (2015) Melatonin promotes ripening and improves quality of tomato fruit during postharvest life. J Exp Bot 66:657–668

    Article  PubMed  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  PubMed  CAS  Google Scholar 

  • Tan DX, Hardeland R, Back K, Manchester LC, Alatorre-Jimenez MA, Reiter RJ (2016) On the significance of an alternate pathway of melatonin synthesis via 5-methoxytryptamine: comparisons across species. J Pineal Res 61:27–40

    Article  PubMed  CAS  Google Scholar 

  • Tassel DV, Roberts N, Lewy A, O'Neill SD (2001) Melatonin in plant organs. J Pineal Res 31:8–15

    Article  PubMed  Google Scholar 

  • Turk H, Erdal S, Genisel M (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74:139–152

    Article  CAS  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google 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. Int J Mol Sci 18:991

    Article  PubMed Central  CAS  Google Scholar 

  • Wang Y, Reiter RJ, Chan Z (2018) Phytomelatonin: a universal abiotic stress regulator. J Exp Bot 69:963–974

    Article  PubMed  CAS  Google Scholar 

  • Wang P, Yin L, Liang D, Li C, Ma F, Yue Z (2012) Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate–glutathione cycle. J Pineal Res 53:11–20

    Article  PubMed  CAS  Google Scholar 

  • Waszczak C, Carmody M, Kangasjärvi J (2018) Reactive oxygen species in plant signaling. Annu Rev Plant Biol 69:209–236

    Article  PubMed  CAS  Google Scholar 

  • Wei Z, Gao T, Liang B, Zhao Q, Ma F, Li C (2018) Effects of exogenous melatonin on methyl viologen-mediated oxidative stress in apple leaf. Int J Mol Sci 19:316

    Article  PubMed Central  CAS  Google Scholar 

  • Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707

    Article  PubMed  CAS  Google Scholar 

  • Xu W, Cai SY, Zhang Y, Wang Y, Ahammed GJ, Xia XJ, Shi K, Zhou HY, Yu JQ, Reiter RJ, Zhou J (2016) Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J Pineal Res 61:457–469

    Article  PubMed  CAS  Google Scholar 

  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi Y, Furutera A, Seki K, Toyoda Y, Tanaka K, Sugimoto Y (2008) Malondialdehyde generated from peroxidized linolenic acid causes protein modification in heat-stressed plants. Plant Physiol Biochem 46:786–793

    Article  PubMed  CAS  Google Scholar 

  • Zandalinas SI, Mittler R, Balfagón D, Arbona V, Gómez-Cadenas A (2018) Plant adaptations to the combination of drought and high temperatures. Physiol Plant 162:2–12

    Article  PubMed  CAS  Google Scholar 

  • Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo YD (2015) Roles of melatonin in abiotic stress resistance in plants. J Exp Bot 66:647–656

    Article  PubMed  CAS  Google Scholar 

  • Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Cao YY, Weeda S, Zhao B, Ren S, Guo YD (2014) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J Pineal Res 57:269–279

    Article  PubMed  CAS  Google Scholar 

  • Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC, Ren S, Guo YD (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativusL.). J Pineal Res 54:15–23

    Article  PubMed  CAS  Google Scholar 

  • Zhou ZH, Wang Y, Ye XY, Li ZG (2018) Signaling molecule hydrogen sulfide improves seed germination and seedling growth of maize (Zea mays L.) under high temperature by inducing antioxidant system and osmolyte biosynthesis. Front Plant Sci 9:1288

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research is supported by the National Natural Science Foundation of China (31760069, 31360057).

Author information

Authors and Affiliations

Authors

Contributions

ZGL designed the experiments; YX, LKB, and SYZ performed the experiments; YW carried out the data analysis; and ZGL and YW wrote and revised the manuscript. All authors have approved the final version of the manuscript.

Corresponding author

Correspondence to Zhong-Guang Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, ZG., Xu, Y., Bai, LK. et al. Melatonin enhances thermotolerance of maize seedlings (Zea mays L.) by modulating antioxidant defense, methylglyoxal detoxification, and osmoregulation systems. Protoplasma 256, 471–490 (2019). https://doi.org/10.1007/s00709-018-1311-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-1311-4

Keywords

Navigation