Skip to main content
Log in

Dopamine Alleviates Chilling Stress in Watermelon Seedlings via Modulation of Proline Content, Antioxidant Enzyme Activity, and Polyamine Metabolism

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Dopamine acts as a strong water-soluble antioxidant that mediates many physiological processes in plants. In the present study, we utilized two cultivars to investigate the effect of dopamine in mitigating chilling stress in watermelon (Citrullus lanatus) seedlings. Under chilling stress, exogenous application of dopamine (100 μM) increased seedling health index by 23.32% (cv. Xi Nong NO. 8) and 35.19% (cv. Jing Xin NO. 1) compared to chilling-stressed seedlings alone. As the stress was prolonged, chilling treatment caused a significant reduction in net rates of photosynthesis and chlorophyll contents. Dopamine supplementation significantly mitigated these adverse effects caused by chilling stress. After 8 days of chilling stress, supplementation of dopamine to chilling treatment seedlings further increases in levels of proline in cv. Xi Nong NO. 8 and cv. Jing Xin NO. 1 by 45.24% and 58.28%, respectively. Our results indicated that application of dopamine further enhanced antioxidant enzymes, which contributed to alleviate oxidative stress-induced chilling treatment. In addition, application of dopamine significantly improved polyamine levels by stimulating enzymes involved in the polyamine metabolism. From these outcomes, it is clear that supplementation of dopamine mitigates the harmful effects of chilling stress in watermelon seedlings through modulation of osmolytes, antioxidant enzymes, and polyamine metabolism.

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

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    CAS  PubMed  Google Scholar 

  • Ahmad P, Prasad MNV (2011) Abiotic stress responses in plants. Springer, New York

    Google Scholar 

  • Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175

    CAS  PubMed  Google Scholar 

  • Ahmad P, Nabi G, Ashraf M (2011) Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. S Afr J Bot 77:36–44

    CAS  Google Scholar 

  • Ahmad P, Abdel Latef AA, Abd Allah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (2016) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:513

    PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Alyemeni MN, Ahanger MA, Egamberdieva D, Wijaya L, Alam P (2018) Salicylic acid (SA) induced alterations in growth, biochemical attributes and antioxidant enzyme activity in faba bean (Vicia faba L.) seedlings under NaCl toxicity. Russ J Plant Physiol 65:104–114

    CAS  Google Scholar 

  • Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    PubMed  Google Scholar 

  • Alyemeni MN, Ahanger MA, Wijaya L, Alam P, Bhardwaj R, Ahmad P (2018) Selenium mitigates cadmium-induced oxidative stress in tomato (Solanum lycopersicum L.) plants by modulating chlorophyll fluorescence, osmolyte accumulation, and antioxidant system. Protoplasma 255:459–469

    CAS  PubMed  Google Scholar 

  • Ashraf M, Akram NA, Al-Qurainy F, Foolad MR (2011) Chapter five: drought tolerance: roles of organic osmolytes, growth regulators, and mineral nutrients. Adv Agron 111:249–296

    CAS  Google Scholar 

  • Bach CE, Warnock DD, Horn DJV, Weintraub MN, Sinsabaugh RL, Allison SD, German DP (2013) Measuring phenol oxidase and peroxidase activities with pyrogallol, l-DOPA, and ABTS: effect of assay conditions and soil type. Soil Biol Biochem 67:183–191

    CAS  Google Scholar 

  • Bai Y, Shi WH, Xing XJ, Wang Y, Jin YR, Zhang L, Song YF, Dong LH, Liu HB (2014) Study on tobacco vigorous seedling indexes model. Sci Agric Sin 47:1086–1098

    CAS  Google Scholar 

  • Basra SMA (2010) Role of proline and glycinebetaine in improving chilling stress tolerance in sugarcane buds at sprouting. Int J Agric Biol 12:1560–8530

    Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Cao YY, Yang MT, Li X, Zhou ZQ, Wang XJ, Bai JG, Cao YY, Yang MT, Li X, Zhou ZQ (2014) Exogenous sucrose increases chilling tolerance in cucumber seedlings by modulating antioxidant enzyme activity and regulating proline and soluble sugar contents. Sci Hortic 179:67–77

    CAS  Google Scholar 

  • Cao S, Shao J, Shi L, Xu L, Shen Z, Chen W, Yang Z (2018) Melatonin increases chilling tolerance in postharvest peach fruit by alleviating oxidative damage. Sci Rep 8:806

    PubMed  PubMed Central  Google Scholar 

  • Diao Q, Song Y, Qi H (2015) Exogenous spermidine enhances chilling tolerance of tomato (Solanum lycopersicum L.) seedlings via involvement in polyamines metabolism and physiological parameter levels. Acta Physiol Plant 37:230

    Google Scholar 

  • Diao Q, Song Y, Shi D, Qi H (2016) Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum Mill.) seedling. J Zhejiang Univ Sci B 17:916–930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding F, Wang M, Zhang S (2017) Overexpression of a calvin cycle enzyme SBPase improves tolerance to chilling-induced oxidative stress in tomato plants. Sci Hortic 214:27–33

    CAS  Google Scholar 

  • Duncan DR, Widholm JM (1991) Proline is not the primary determinant of chilling tolerance induced by mannitol or abscisic acid in regenerable maize callus cultures. Plant Physiol 95:1284–1287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elstner EF, Konze JRR, Selman BR, Stoffer C (1976) Ethylene formation in sugar beet leaves. Plant Physiol 58:163–168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Esim N, Atici Ö (2015) Effects of exogenous nitric oxide and salicylic acid on chilling-induced oxidative stress in wheat (Triticum aestivum). Front Life Sci 8:124–130

    CAS  Google Scholar 

  • Fan H, Du C, Xu Y, Xue W (2014) Exogenous nitric oxide improves chilling tolerance of Chinese cabbage seedlings by affecting antioxidant enzymes in leaves. Hortic Environ Biotechnol 55:159–165

    CAS  Google Scholar 

  • Feng Z, Guo A, Feng Z (2003) Amelioration of chilling stress by triadimefon in cucumber seedlings. Plant Growth Regul 39:277–283

    CAS  Google Scholar 

  • Ferguson IB, Watkins CB, Harman JE (1983) Inhibition by calcium of senescence of detached cucumber cotyledons. Plant Physiol 71:182–186

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flores HE, Filner P (1985) Polyamine catabolism in higher plants: characterization of pyrroline dehydrogenase. Plant Growth Regul 3:277–291

    CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occrrence in higher plants. Plant Physiol 59:309–314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gomes BR, Siqueira-Soares RDC, Santos WDD, Marchiosi R, Soares AR, Ferrarese-Filho O (2014) The effects of dopamine on antioxidant enzymes activities and reactive oxygen species levels in soybean roots. Plant Signal Behav 9:e977704

    PubMed  PubMed Central  Google Scholar 

  • Gulzar SS, Shabir HW, WasimSingh HNB (2011) Engineering cold stress tolerance in crop plants. Curr Genom 12:30–43

    Google Scholar 

  • Hawrylak-Nowak B, Matraszek R, Szymańska M (2010) Selenium modifies the effect of short-term chilling stress on cucumber plants. Biol Trace Elem Res 138:307

    CAS  PubMed  Google Scholar 

  • Heidarvand L, Amiri RM (2010) What happens in plant molecular responses to cold stress? Acta Physiol Plant 32:419–431

    CAS  Google Scholar 

  • Hu WH, Song XS, Shi K, Xia XJ, Zhou YH, Yu JQ (2008) Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46:581–588

    CAS  Google Scholar 

  • Kader DZA, Saleh AAH, Elmeleigy SA, Dosoky NS (2011) Chilling-induced oxidative stress and polyamines regulatory role in two wheat varieties. J Taibah Univ Sci 5:14–24

    Google Scholar 

  • Kanazawa K, Sakakibara H (2000) High content of dopamine, a strong antioxidant, in Cavendish banana. J Agric Food Chem 48:844–848

    CAS  PubMed  Google Scholar 

  • Kanda HO (1998) Studies on nucleic acid and protein metabolism in roots relating to low temperature-tolerant elongation ability of figleaf gourd [Cucurbita ficifolia] for root stock. Bull Prefect Coll Agric 24:29–62

    Google Scholar 

  • Kao CH (1981) Senescence of rice leaves VI. Comparative study of the metabolic changes of senescing turgid and water-stressed excised leaves. Plant Cell Physiol 22:683–688

    CAS  Google Scholar 

  • Kaur G, Asthir B (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plantarum 59:609–619

    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

    CAS  PubMed  Google Scholar 

  • Kim TE, Kim SK, Han TJ, Lee JS, Chang SC (2010) ABA and polyamines act independently in primary leaves of cold-stressed tomato (Lycopersicon esculentum). Physiol Plant 115:370–376

    Google Scholar 

  • Kohli SK, Handa N, Sharma A, Gautam V, Arora S, Bhardwaj R, Wijaya L, Alyemeni MN, Ahmad P (2018) Interaction of 24-epibrassinolide and salicylic acid regulates pigment contents, antioxidative defense responses, and gene expression in Brassica juncea L. seedlings under Pb stress. Environ Sci Pollut R 25:15159–15173

    CAS  Google Scholar 

  • Kohli SK, Bali S, Tejpal R, Bhalla V, Verma V, Bhardwaj R, Alqarawi AA, Abd Allah EF, Ahmad P (2019) In-situ localization and biochemical analysis of bio-molecules reveals Pb-stress amelioration in Brassica juncea L. by co-application of 24-epibrassinolide and salicylic acid. Sci Rep 9:3524

    PubMed  PubMed Central  Google Scholar 

  • Korkmaz A, Dufault RJ (2004) Differential cold stress duration and frequency treatment effects on muskmelon seedling and field growth and yield. Eur J Hortic Sci 69:12–20

    Google Scholar 

  • Korkmaz A, Korkmaz Y, Demirkıran AR (2010) Enhancing chilling stress tolerance of pepper seedlings by exogenous application of 5-aminolevulinic acid. Environ Exp Bot 67:495–501

    CAS  Google Scholar 

  • Kotzabasis K, Christakis-Hampsas MD, Roubelakis-Angelakis KA (1993) A narrow-bore HPLC method for the identification and quantitation of free, conjugated, and bound polyamines. Anal Biochem 214:484

    CAS  PubMed  Google Scholar 

  • Kubien DS, Rt VCS, Sage RF (2003) C-4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. Plant Physiol 132:1577–1585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kulma A, Szopa J (2007) Catecholamines are active compounds in plants. Plant Sci 172:433–440

    CAS  Google Scholar 

  • Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Planta 228:367–381

    CAS  PubMed  Google Scholar 

  • Li C, Sun X, Chang C, Jia D, Wei Z, Li C, Ma F (2015) Dopamine alleviates salt-induced stress in Malus hupehensis. Physiol Plant 153:584–602

    CAS  PubMed  Google Scholar 

  • Liang C, Zheng G, Li W, Wang Y, Hu B, Wang H, Wu H, Qian Y, Zhu XG, Tan DX (2015) Melatonin delays leaf senescence and enhances salt stress tolerance in rice. J Pineal Res 59:91–101

    CAS  PubMed  Google Scholar 

  • Liang B, Li C, Ma C, Wei Z, Wang Q, Huang D, Chen Q, Li C, Ma F (2017) Dopamine alleviates nutrient deficiency-induced stress in Malus hupehensis. Plant Physiology & Biochemistry Ppb 119:346

    CAS  Google Scholar 

  • Liang B, Gao T, Zhao Q, Ma C, Chen Q, Wei Z, Li C, Li C, Ma F (2018) Effects of exogenous dopamine on the uptake, transport, and resorption of apple ionome under moderate drought. Front Plant Sci 9:755

    PubMed  PubMed Central  Google Scholar 

  • Liu BR (2008) Influences of boron on the acitivity of superoxide dismutase (SOD), production rate of superoxide anion radical and content of malondialdehyde in turfgrasses. J Huazhong Agric Univ 27:378–381

    CAS  Google Scholar 

  • Liu A, Chen S, Wang M, Liu D, Chang R, Wang Z, Lin X, Bai B, Ahammed GJ (2016) Arbuscular mycorrhizal fungus alleviates chilling stress by boosting redox poise and antioxidant potential of tomato seedlings. J Plant Growth Regul 35:109–120

    CAS  Google Scholar 

  • Lukatkin AS (2002a) Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 1. Reactive oxygen species formation during plant chilling. Russ J Plant Phys 49:622–627

    CAS  Google Scholar 

  • Lukatkin AS (2002b) Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 2. The activity of antioxidant enzymes during plant chilling. Russ J Plant Phys 49:782–788

    CAS  Google Scholar 

  • Lukatkin AS, Brazaitytė A, Bobinas C, Duchovskis P (2012) Chilling injury in chilling-sensitive plants: a review. Zemdirbyste 99:111–124

    Google Scholar 

  • Ni J, Wang Q, Shah FA, Liu W, Wang D, Huang S, Fu S, Wu L (2018) Exogenous melatonin confers cadmium tolerance by counterbalancing the hydrogen peroxide homeostasis in wheat seedlings. Molecules 23:799

    PubMed Central  Google Scholar 

  • Protacio CM, Dai YR, Lewis EF, Flores HE (1992) Growth stimulation by catecholamines in plant tissue/organ cultures. Plant Physiol 98:89

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sayyari M, Ghanbari F, Fatahi S, Bavandpour F (2013) Chilling tolerance improving of watermelon seedling by salicylic acid seed and foliar application. Not Sci Biol 5:67–73

    CAS  Google Scholar 

  • Song Y, Diao Q, Qi H (2014a) Polyamine metabolism and biosynthetic genes expression in tomato (Lycopersicon esculentum Mill.) seedlings during cold acclimation. Plant Growth Regul 75:21–32

    Google Scholar 

  • Song Y, Diao Q, Qi H (2014b) Putrescine enhances chilling tolerance of tomato (Lycopersicon esculentum Mill.) through modulating antioxidant systems. Acta Physiol Plant 36:3013–3027

    CAS  Google Scholar 

  • Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584

    CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plantarum 126:45–51

    CAS  Google Scholar 

  • Świędrych A, Lorenc-Kukuła K, Skirycz A, Szopa J (2004) The catecholamine biosynthesis route in potato is affected by stress. Plant Physiol Biochem 42:593–600

    PubMed  Google Scholar 

  • Szopa J, Wilczyński G, Fiehn O, Wenczel A, Willmitzer L (2001) Identification and quantification of catecholamines in potato plants (Solanum tuberosum) by GC–MS. Phytochemistry 58:315–320

    CAS  PubMed  Google Scholar 

  • Terzi R, Kalaycıoglu E, Demiralay M, Saglam A, Kadioglu A (2015) Exogenous ascorbic acid mitigates accumulation of abscisic acid, proline and polyamine under osmotic stress in maize leaves. Acta Physiol Plant 37:43

    Google 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 Sci 151:59–66

    CAS  Google Scholar 

  • Wan YY, Zhang Y, Zhang L, Zhou ZQ, Li X, Shi Q, Wang XJ, Bai JG (2015) Caffeic acid protects cucumber against chilling stress by regulating antioxidant enzyme activity and proline and soluble sugar contents. Acta Physiol Plant 37:1–10

    CAS  Google Scholar 

  • Wang Y, Luo Z, Mao L, Ying T (2016) Contribution of polyamines metabolism and GABA shunt to chilling tolerance induced by nitric oxide in cold-stored banana fruit. Food Chem 197:333–339

    CAS  PubMed  Google Scholar 

  • Wang Y, Zhu M, Yang Y, Alam I, Cheng X, Qin T, Yunhai LU (2017) Exogenous application of abscisic acid (ABA) enhances chilling tolerance in seedlings of napier grass (Pennisetum purpureum Schum.). Agric Sci Technol 18:417–423

    Google Scholar 

  • Willekens H, Inzé D, Montagu MV, Camp WV (1995) Catalases in plants. Mol Breed 1:207–228

    CAS  Google Scholar 

  • Yadav SK (2010) Cold stress tolerance mechanisms in plants: a review. Agron Sustain Dev 30:515–527

    CAS  Google Scholar 

  • Yu BJ, Li SN, Liu YL (2002) Comparison of ion effects of salt injury in soybean seedlings. J Nanjing Agric Univ 25:5–9

    CAS  Google Scholar 

  • Zhao F, Sun C, Liu Y, Zhang W (2003) Relationship between polyamine in roots and salt tolerance of barley seedlings. Acta Bot Sin 45:295–300

    CAS  Google Scholar 

  • Zhao H, Zhang K, Zhou X, Xi L, Wang Y, Xu H, Pan T, Zou Z (2017) Melatonin alleviates chilling stress in cucumber seedlings by up-regulation of CsZat12 and modulation of polyamine and abscisic acid metabolism. Sci Rep 7:4912–4998

    Google Scholar 

Download references

Acknowledgements

This work was supported by the earmarked fund for China Agricultural Research System. The authors are grateful to Thomas A. Gavin for help in revising our English composition.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yan Sun.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts 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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiao, C., Lan, G., Sun, Y. et al. Dopamine Alleviates Chilling Stress in Watermelon Seedlings via Modulation of Proline Content, Antioxidant Enzyme Activity, and Polyamine Metabolism. J Plant Growth Regul 40, 277–292 (2021). https://doi.org/10.1007/s00344-020-10096-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-020-10096-2

Keywords

Navigation