Melatonin treatment induces chilling tolerance by regulating the contents of polyamine, γ-aminobutyric acid, and proline in cucumber fruit

doi:10.1016/S2095-3119(20)63485-2

摘要/Abstract

摘要：

以商业成熟期黄瓜果实为材料，研究褪黑素(melatonin，MT)诱导黄瓜果实耐冷性的机制。本研究中，施用100 µmol L^-1 MT处理黄瓜果实，然后在4°C、90%相对湿度条件下贮藏15 d。与对照相比，MT处理减轻了黄瓜的冷害，电解质泄漏减少，硬度增强。在贮藏期间MT处理抑制了黄瓜果实中叶绿素酶的活性，提高了叶绿素的含量。MT处理增强了精氨酸脱羧酶(arginine decarboxylase，ADC)和鸟氨酸脱羧酶(ornithine decarboxylase，ODC)的活性，而且上调了CsADC (Cucumis sativus ADC)和CsODC (C. sativus ODC) 基因的表达，导致多胺含量的积累。类似的，处理后的黄瓜果实含有较高的脯氨酸水平。与此同时脯氨酸合成酶△¹-吡咯啉-5-羧酸合成酶(△¹-pyrroline-5-carboxylate synthetase，P5CS)和鸟氨酸转氨酶(ornithine aminotransferase，OAT)的活性显著提高，而脯氨酸降解酶脯氨酸脱氢酶(proline dehydrogenase，PDH)的活性受到抑制。MT也诱导了CsOAT (C. sativus OAT)和CsP5CS (C. sativus P5CS)基因的表达。此外，MT处理通过增强黄瓜果实中GABA转氨酶(GABA transaminase，GABA-T)和谷氨酸脱羧酶(glutamate decarboxylase，GAD)的活性，上调了CsGAD(C. sativus GAD)基因的表达，从而提高γ-氨基丁酸(γ-aminobutyric acid，GABA)的含量。综上所述，结果表明MT处理提高耐冷性，与调节多胺、脯氨酸和γ-氨基丁酸有关。

Abstract:

The mechanism of melatonin (MT) induced chilling tolerance in harvested cucumber fruit was investigated at commercial maturity. In this study, cucumber fruits were treated with 100 μmol L–1 MT at 4°C and 90% relative humidity for 15 d of storage. In comparison with the control, cucumber treatment with MT resulted in reduced chilling injury (CI), decreased electrolyte leakage and enhanced firmness. The fruits treated with MT showed higher chlorophyll contents in storage conditions with suppressed chlorophyllase enzyme activity. MT treatment increased arginine decarboxylase (ADC) and ornithine decarboxylase (ODC) enzyme activities. Moreover, enhanced expression of the Cucumis sativus ADC (CsADC) and C. sativus ODC (CsODC) genes resulted in the accumulation of polyamine contents. Similarly, proline levels exhibited higher levels among treated fruits. Meanwhile, the proline synthesizing enzymes △¹-pyrroline-5-carboxylate syntheses (P5CS) and ornithine aminotransferase (OAT) were significantly increased, while a catabolic enzyme of proline dehydrogenase (PDH) activity was inhibited by treatment. In addition, MT induced expression of C. sativus OAT (CsOAT) and C. sativus P5CS (CsP5CS) genes. Cucumber fruits treated with MT also exhibited higher γ-aminobutyric acid (GABA) content by enhanced GABA transaminase (GABA-T) and glutamate decarboxylase (GAD) enzyme activities and a higher C. sativus GAD (CsGAD) gene expression. To sum up, the results show that MT treatment enhanced chilling tolerance, which was associated with the regulation of polyamines, as well as proline and γ-aminobutyric acid.

Key words: cucumber , melatonin , polyamine , proline , GABA , chilling injury

. [J]. Journal of Integrative Agriculture, 2021, 20(11): 3060-3074.

Miilion P MADEBO, LUO Si-ming, WANG Li, ZHENG Yong-hua, JIN Peng. Melatonin treatment induces chilling tolerance by regulating the contents of polyamine, γ-aminobutyric acid, and proline in cucumber fruit[J]. Journal of Integrative Agriculture, 2021, 20(11): 3060-3074.

参考文献

Aghdam M S, Bodbodak S. 2013. Physiological and biochemical mechanisms regulating chilling tolerance in fruits and vegetables under postharvest salicylates and jasmonates treatments. Scientia Horticulturae, 156, 73–85.
Aghdam M S, Luo Z, Jannatizadeh A, Sheikh-Assadi M, Sharafi Y, Farmani B, Fard J R, Razavi F. 2019. Employing exogenous melatonin applying confers chilling tolerance in tomato fruits by upregulating ZAT2/6/12 giving rise to promoting endogenous polyamines, proline, and nitric oxide accumulation by triggering arginine pathway activity. Food Chemistry, 275, 549–556.
Aghdam M S, Naderi R, Jannatizadeh A, Babalar M, Sarcheshmeh M A A, Faradonbe M Z. 2016. Impact of exogenous GABA treatments on endogenous GABA metabolism in anthurium cut flowers in response to postharvest chilling temperature. Plant Physiology and Biochemistry, 106, 11–15.
Alcázar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio A F. 2010. Polyamines: Molecules with regulatory functions in plant abiotic stress tolerance. Planta, 231, 1237–1249.
Anwar A, Bai L, Miao L, Liu Y, Li S, Yu X, Li Y. 2018. 24-Epibrassinolide ameliorates endogenous hormone levels to enhance low-temperature stress tolerance in cucumber seedlings. International Journal of Molecular Sciences, 19, 1–17.
Arnao M B, Hernández-Ruiz J. 2015. Functions of melatonin in plants: A review. Journal of Pineal Research, 59, 133–150.
Cai J H, Cheng S C, Luo F, Zhao Y B, Wei B D, Zhou Q, Zhou X, Ji S J. 2019. Influence of ethylene on morphology and pigment changes in harvested broccoli. Food and Bioprocess Technology, 12, 883–897.
Cao S, Bian K, Shi L, Chung H H, Chen W, Yang Z. 2018a. Role of melatonin in cell-wall disassembly and chilling tolerance in cold-stored peach fruit. Journal of Agricultural and Food Chemistry, 66, 5663–5670.
Cao S, Cai Y, Yang Z, Zheng Y. 2012. MeJA induces chilling tolerance in loquat fruit by regulating proline and γ-aminobutyric acid contents. Food Chemistry, 133, 1466–1470.
Cao S, Shao J, Shi L, Xu L, Shen Z, Chen W, Yang Z. 2018b. Melatonin increases chilling tolerance in postharvest peach fruit by alleviating oxidative damage. Scientific Reports, 8, 1–11.
Cao S, Song C, Shao J, Bian K, Chen W, Yang Z. 2016. Exogenous melatonin treatment increases chilling tolerance and induces defense response in harvested peach fruit during cold storage. Journal of Agricultural and Food Chemistry, 64, 5215–5222.
Deewatthanawong R, Nock J F, Watkins C B. 2010a. γ-Aminobutyric acid (GABA) accumulation in four strawberry cultivars in response to elevated CO2 storage. Postharvest Biology and Technology, 57, 92–96.
Deewatthanawong R, Rowell P, Watkins C B. 2010b. γ-Aminobutyric acid (GABA) metabolism in CO2 treated tomatoes. Postharvest Biology and Technology, 57, 97–105.
Fait A, Fromm H, Walter D, Galili G, Fernie A R. 2008. Highway or byway: The metabolic role of the GABA shunt in plants. Trends in Plant Science, 13, 14–19.
Gao H, Zhang Z K, Chai H K, Cheng N, Yang Y, Wang D N, Yang T, Cao W. 2016. Melatonin treatment delays postharvest senescence and regulates reactive oxygen species metabolism in peach fruit. Postharvest Biology and Technology, 118, 103–110.
Groppa M, Benavides M. 2008. Polyamines and abiotic stress: Recent advances. Amino Acids, 34, 1–22.
Gupta K, Dey A, Gupta B. 2013. Plant polyamines in abiotic stress responses. Acta Physiologiae Plantarum, 35, 2015–2036.
Hakim A, Purvis A C, Mullinix B G. 1999. Differences in chilling sensitivity of cucumber varieties depends on storage temperature and the physiological dysfunction evaluated. Postharvest Biology and Technology, 17, 97–104.
Heidarvand L, Amiri R M. 2010. What happens in plant molecular responses to cold stress? Acta Physiologiae Plantarum, 32, 419–431.
Hu W, Yang H, Tie W, Yan Y, Ding Z, Liu Y, Wu C, Wang J, Reiter R J, Tan D X. 2017. Natural variation in banana varieties highlights the role of melatonin in postharvest ripening and quality. Journal of Agricultural and Food Chemistry, 65, 9987–9994.
Hu X, Zhang Y, Shi Y, Zhang Z, Zou Z, Zhang H, Zhao J. 2012. Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiology and Biochemistry, 57, 200–209.
Hyun T K, Eom S H, Jeun Y C, Han S H, Kim J S. 2013. Identification of glutamate decarboxylases as a γ-aminobutyric acid (GABA) biosynthetic enzyme in soybean. Industrial Crops and Products, 49, 864–870.
Jahan M S, Shu S, Wang Y, Chen Z, He M, Tao M, Sun J, Guo S. 2019. Melatonin alleviates heat-induced damage of tomato seedlings by balancing redox homeostasis and modulating polyamine and nitric oxide biosynthesis. BMC Plant Biology, 19, 1–16.
Koushesh Saba M, Arzani K, Barzegar M. 2012. Postharvest polyamine application alleviates chilling injury and affects apricot storage ability. Journal of Agricultural and Food Chemistry, 60, 8947–8953.
Li X, Kim Y B, Uddin M R, Lee S, Kim S J, Park S U. 2013. Influence of light on the free amino acid content and γ-aminobutyric acid synthesis in Brassica juncea seedlings. Journal of Agricultural and Food Chemistry, 61, 8624–8631.
Liu C, Zheng H, Sheng K, Liu W, Zheng L. 2018. Effects of melatonin treatment on the postharvest quality of strawberry fruit. Postharvest Biology and Technology, 139, 47–55.
Liu J, Yang J, Zhang H, Cong L, Zhai R, Yang C, Wang Z, Ma F, Xu L. 2019. Melatonin inhibits ethylene synthesis via nitric oxide regulation to delay postharvest senescence in pears. Journal of Agricultural and Food Chemistry, 67, 2279–2288.
Maftoonazad N, Ramaswamy H. 2005. Postharvest shelf-life extension of avocados using methyl cellulose-based coating. LWT - Food Science and Technology, 38, 617–624.
Malekzadeh P, Khosravi-Nejad F, Hatamnia A A, Mehr R S. 2017. Impact of postharvest exogenous γ-aminobutyric acid treatment on cucumber fruit in response to chilling tolerance. Physiology and Molecular Biology of Plants, 23, 827–836.
Mfnguez-Mosquera M I, Gandul-Rojas B, Gallardo-Guerrero L. 1994. Measurement of chlorophyllase activity in olive fruit Olea europaea. The Journal of Biochemistry, 116, 263–268.
Mirdehghan S, Rahemi M, Martínez-Romero D, Guillén F, Valverde J, Zapata P, Serrano M, Valero D. 2007. Reduction of pomegranate chilling injury during storage after heat treatment: Role of polyamines. Postharvest Biology and Technology, 44, 19–25.
Mohammadi A, Hashemi M, Hosseini S M. 2016. Postharvest treatment of nanochitosan-based coating loaded with Zataria multiflora essential oil improves antioxidant activity and extends shelf-life of cucumber. Innovative Food Science & Emerging Technologies, 33, 580–588.
Palma F, Carvajal F, Jamilena M, Garrido D. 2014. Contribution of polyamines and other related metabolites to the maintenance of zucchini fruit quality during cold storage. Plant Physiology and Biochemistry, 82, 161–171.
Ruiz J M, Sanchez E, Garc?a P C, Lopez-Lefebre L R, Rivero R M, Romero L. 2002. Proline metabolism and NAD kinase activity in greenbean plants subjected to cold-shock. Phytochemistry, 59, 473–478.
Shan T, Jin P, Zhang Y, Huang Y, Wang X, Zheng Y. 2016. Exogenous glycine betaine treatment enhances chilling tolerance of peach fruit during cold storage. Postharvest Biology and Technology, 114, 104–110.
Shang H, Cao S, Yang Z, Cai Y, Zheng Y. 2011. Effect of exogenous γ-aminobutyric acid treatment on proline accumulation and chilling injury in peach fruit after long-term cold storage. Journal of Agricultural and Food Chemistry, 59, 1264–1268.
Shelp B J, Bown A W, McLean M D. 1999. Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science, 4, 446–452.
Shu S, Tang Y, Yuan Y, Sun J, Zhong M, Guo S. 2016. The role of 24-epibrassinolide in the regulation of photosynthetic characteristics and nitrogen metabolism of tomato seedlings under a combined low temperature and weak light stress. Plant Physiology and Biochemistry, 107, 344–353.
Tan X L, Fan Z Q, Kuang J F, Lu W J, Reiter R J, Lakshmanan P, Su X G, Zhou J, Chen J Y, Shan W. 2019. Melatonin delays leaf senescence of Chinese flowering cabbage by suppressing ABFs-mediated abscisic acid biosynthesis and chlorophyll degradation. Journal of Pineal Research, 67, 1–15.
Verbruggen N, Hermans C. 2008. Proline accumulation in plants: A review. Amino Acids, 35, 753–759.
Wang D, Li L, Xu Y, Limwachiranon J, Li D, Ban Z, Luo Z. 2017. Effect of exogenous nitro oxide on chilling tolerance, polyamine, proline, and γ-aminobutyric acid in bamboo shoots (Phyllostachys praecox f. prevernalis). Journal of Agricultural and Food Chemistry, 65, 5607–5613.
Wang Y, Luo Z, Du R, Liu Y, Ying T, Mao L. 2013. Effect of nitric oxide on antioxidative response and proline metabolism in banana during cold storage. Journal of Agricultural and Food Chemistry, 61, 8880–8887.
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 Chemistry, 197, 333–339.
Wu X, He J, Zhu Z, Yang S, Zha D. 2014. Protection of photosynthesis and antioxidative system by 24-epibrassinolide in Solanum melongena under cold stress. Biologia Plantarum, 58, 185–188.
Xu L, Yue Q, Xiang G, Bian F E, Yao Y. 2018. Melatonin promotes ripening of grape berry via increasing the levels of ABA, H2O2, and particularly ethylene. Horticulture Research, 5, 1–11.
Yang C M, Chang F, Lin S J, Chou C H. 2004. Effects of three allelopathic phenolics on chlorophyll accumulation of rice (Oryza sativa) seedlings: II. Stimulation of consumption-orientation. Botanical Bulletin of Academia Sinica, 45, 119–125.
Yang H, Wu F, Cheng J. 2011. Reduced chilling injury in cucumber by nitric oxide and the antioxidant response. Food Chemistry, 127, 1237–1242.
Yuan L, Shu S, Sun J, Guo S, Tezuka T. 2012. Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. under Ca(NO3)2 stress. Photosynthesis Research, 112, 205–214.
Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo Y D. 2014. Roles of melatonin in abiotic stress resistance in plants. Journal of Experimental Botany, 66, 647–656.
Zhang W, Jiang B, Li W, Song H, Yu Y, Chen J. 2009. Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Scientia Horticulturae, 122, 200–208.
Zhang X, Shen L, Li F, Meng D, Sheng J. 2011. Methyl salicylate-induced arginine catabolism is associated with up-regulation of polyamine and nitric oxide levels and improves chilling tolerance in cherry tomato fruit. Journal of Agricultural and Food Chemistry, 59, 9351–9357.
Zhang Y, Hube D J, Hu M, Jiang G, Gao Z, Xu X, Jiang Y, Zhang Z. 2018. Delay of postharvest browning in litchi fruit by melatonin via the enhancing of antioxidative processes and oxidation repair. Journal of Agricultural and Food Chemistry, 66, 7475–7484.
Zhao D, Shen L, Fan B, Liu K, Yu M, Zheng Y, Ding Y, Sheng J. 2009. Physiological and genetic properties of tomato fruits from 2 cultivars differing in chilling tolerance at cold storage. Journal of Food Science, 74, C348–C352.
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. Scientific Reports, 7, 1–12.