Abstract
Effect of low temperature and low oxygen concentration on biochemical attributes, antioxidant enzyme activities, phenolics profile and expression of phenylpropanoid pathway-related genes was investigated in crabapple (Malus profusion) fruit. Crabapple fruit were kept at room temperature (RT, 20 ± 2 °C and 25 ± 2 °C alternatively at 12 h cycle) or low temperature (LT, 10 ± 2 °C and 25 ± 2 °C alternatively at 12 h cycle) and supplemented with either normal oxygen (21%) or low oxygen levels (5%) for 9 days. Results revealed higher concentrations of soluble solids, titratable acids, and ascorbic acid in fruit stored at LT + 5% O2. Likewise, total phenolics, peroxidase activity, and 2,2´-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid)-radical scavenging activity were observed to be significantly higher in fruit stored at low temperature (LT + 5% O2 > LT + 21% O2), followed by those stored at room temperature (RT + 5% O2 > RT + 21% O2). In contrast, H2O2 and malondialdehyde contents were significantly enhanced in fruit stored at room temperature (RT + 21% O2 and RT + 5% O2), whereas fruit stored at low temperature showed minimum inhibition in superoxide dismutase, catalase and ascorbate peroxidase activities. In addition, low temperature induced biosynthesis of phenolic acids, whereas no considerable changes were observed in flavanols and dihydrochalcones during storage. Low temperature and oxygen conditions (LT + 5% O2) significantly enhanced the biosynthesis of flavonols (glycosylated quercetin derivatives) and cyanidin 3-galactoside, compared to LT + 21% O2, RT + 5% O2 and RT + 21% O2 conditions. In addition, low temperature also up-regulated the expression of MpFLS and MpUFGT in fruit tissues. Moreover, correlation analysis suggested positive association of antioxidant capacity with the biosynthesis of flavonols and anthocyanins in fruit stored at LT + 5% O2.
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References
Ali S, Khan AS, Malik AU, Shahid M (2016) Effect of controlled atmosphere storage on pericarp browning, bioactive compounds and antioxidant enzymes of litchi fruits. Food Chem 206:18–29. https://doi.org/10.1016/j.foodchem.2016.03.021
Ali S, Khan AS, Malik AU, Nawaz A, Shahid M (2019) Postharvest application of antibrowning chemicals modulates oxidative stress and delays pericarp browning of controlled atmosphere stored litchi fruit. J Food Biochem 43:e12746. https://doi.org/10.1111/jfbc.12746
Antika LD, Lee EJ, Kim YH, Kang MK, Park SH, Kim DY, Oh H, Choi YJ, Kang YH (2017) Dietary phlorizin enhances osteoblastogenic bone formation through enhancing β-catenin activity via GSK-3β inhibition in a model of senile osteoporosis. J Nutr Biochem 49:42–52. https://doi.org/10.1016/j.jnutbio.2017.07.014
Azuma A, Yakushiji H, Koshita Y, Kobayashi S (2012) Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236:1067–1080. https://doi.org/10.1007/s00425-012-1650-x
Becker C, Kläring HP, Kroh LW, Krumbein A (2013) Temporary reduction of radiation does not permanently reduce flavonoid glycosides and phenolic acids in red lettuce. Plant Physiol Biochem 72:154–160. https://doi.org/10.1016/j.plaphy.2013.05.006
Brar JK, Rai DR, Singh A, Kaur N (2013) Biochemical and physiological changes in Fenugreek (Trigonella foenum-graecum L.) leaves during storage under modified atmosphere packaging. J Food Sci Technol 50:696–704. https://doi.org/10.1007/s13197-011-0390-4
Fang L, Meng W, Min W (2018) Phenolic compounds and antioxidant activities of flowers, leaves and fruits of five crabapple cultivars (Malus Mill. species). Sci Hort 235:460–467. https://doi.org/10.1016/j.scienta.2018.02.051
Feng F, Li M, Ma F, Cheng L (2013) Phenylpropanoid metabolites and expression of key genes involved in anthocyanin biosynthesis in the shaded peel of apple fruit in response to sun exposure. Plant Physiol Biochem 69:54–61. https://doi.org/10.1016/j.plaphy.2013.04.020
Heim K, Tagliaferro AR, Bobilya DJ (2002) Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13:572–584. https://doi.org/10.1016/S0955-2863(02)00208-5
Hoang TT, John B, Golding MAW (2011) The effect of postharvest 1-MCP treatment and storage atmosphere on ‘Cripps Pink’ apple phenolics and antioxidant activity. Food Chem 127:1249–1256. https://doi.org/10.1016/j.foodchem.2011.01.052
Jacobo-Velázquez DA, Cisneros-Zevallos L (2012) An alternative use of horticultural crops: stressed plants as biofactories of bioactive phenolic compounds. Agric 2:259–271. https://doi.org/10.3390/agriculture2030259
Jacobo-Velázquez DA, Martínez-Hernández GB, Rodríguez SC, Cao CM, Cisneros-Zevallos L (2011) Plants as biofactories: physiological role of reactive oxygen species on the accumulation of phenolic antioxidants in carrot tissue under wounding and hyperoxia stress. J Agric Food Chem 59:6583–6593. https://doi.org/10.1021/jf2006529
Külen O, Stushnoff C, Holm DG (2013) Effect of cold storage on total phenolics content, antioxidant activity and vitamin C level of selected potato clones. J Sci Food Agric 93:2437–2444. https://doi.org/10.1002/jsfa.6053
Lattanzio V, Venere DD, Linsalata V, Bertolini P, Ippolito A, Salerno M (2001) Low temperature metabolism of apple phenolics and quiescence of Phlyctaena vagabunda. J Agric Food Chem 49(12):5817–5821. https://doi.org/10.1021/jf010255b
Lee JH, Oh MM (2015) Short-term low temperature increases phenolic antioxidant levels in kale. Hortic Environ Biotechnol 56:588–596. https://doi.org/10.1007/s13580-015-0056-7
Lee KW, Kim YJ, Kim DO, Lee HJ, Lee CY (2003) Major phenolics in apple and their contribution to the total antioxidant capacity. J Agric Food Chem 51:6516–6520. https://doi.org/10.1021/jf034475w
Li PM, Du GR, Ma FW (2011) Phenolics concentration and antioxidant capacity of different fruit tissues of astringent versus non-astringent persimmons. Sci Hortic 129:710–714. https://doi.org/10.1016/j.scienta.2011.05.024
Li N, Shi J, Wang K (2014) Profile and antioxidant activity of phenolic extracts from 10 crabapples (Malus wild species). J Agric Food Chem 62:574–581. https://doi.org/10.1021/jf404542d
Li F, Zhang X, Li Y, Lu K, Yin R, Ming J (2017) Phenolics extracted from tartary (Fagopyrum tartaricum L. Gaerth) buckwheat bran exhibit antioxidant activity, and an antiproliferative effect on human breast cancer MDA-MB-231 cells through the p38/MAP kinase pathway. Food Funct 8:177–188. https://doi.org/10.1039/C6FO01230B
Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K, Michael AJ, Tohge T, Yamazaki M, Saito K (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77(3):367–379. https://doi.org/10.1111/tpj.12388
Noveroske RL, Kuæ J, Williams EB (1964) Oxidation of phloridzin and phloretin related to resistance of Malus to Venturia inaequalis. Phytopathol 54:92–97. https://doi.org/10.1007/BF01977511
Padda MS, Picha DH (2008) Effect of low temperature storage on phenolic composition and antioxidant activity of sweetpotatoes. Postharvest Biol Technol 47:176–180. https://doi.org/10.1016/j.postharvbio.2007.06.014
Park MJ, Cho JY, Ha IJ, Moon JS, Kang YH (2018) Comparison of the antioxidant properties and flavonols in various parts of Korean red onions by multivariate data analysis. Hortic Environ Biotechnol 59:919–927. https://doi.org/10.1007/s13580-018-0091-2
Punyasiri PAN, Abeysinghe ISB, Kumar V, Treutter D, Duy D, Gosch C, Martens S, Forkmann G, Fischer TC (2004) Flavonoid biosynthesis in the tea plant Camellia sinensis: properties of enzymes of the prominent epicatechin and catechin pathways. Arch Biochem Biophy 431:22–30. https://doi.org/10.1016/j.abb.2004.08.003
Rehman RNU, You Y, Zhang L, Goudia BD, Khan AR, Li P, Ma F (2017) High temperature induced anthocyanin inhibition and active degradation in Malus profusion. Front Plant Sci 8:1401. https://doi.org/10.3389/fpls.2017.01401
Rehman RNU, You Y, Ali S, Wang Y, Zhang L, Li P, Ma F (2018) Phenolic compounds as biochemical markers of senescence in woody ornamental flowers of Malus crabapple. Hort Environ Biotechnol. https://doi.org/10.1007/s13580-018-0001-7
Reyes LF, Cisneros-Zevallos L (2003) Wounding stress increases the phenolic content and antioxidant capacity of purple-flesh potatoes (Solanum tuberosum L.). J Agric Food Chem 51:5296–5300. https://doi.org/10.1021/jf034213u
Rivera-Pastrana DM, Gardea AA, Yahia EM, Martínez-Téllez MA, González-Aguilar GA (2014) Effect of UV-C irradiation and low temperature storage on bioactive compounds, antioxidant enzymes and radical scavenging activity of papaya fruit. J Food Sci Technol 51:3821–3829. https://doi.org/10.1007/s13197-013-0942-x
Rivero RC, Rodrı́guez RE, Romero CD (2003) Effects of current storage conditions on nutrient retention in several varieties of potatoes from Tenerife. Food Chem 80:445–450. https://doi.org/10.1016/S0308-8146(02)00281-9
Sekher PA, Chan TS, O’Brien PJ, Rice-Evans CA (2001) Flavonoid B-ring chemistry and antioxidant activity: fast reaction kinetics. BBRC 282:1161–1168. https://doi.org/10.1006/bbrc.2001.4705
Sharma R, Nath AK (2016) Antioxidant levels and activities of reactive oxygen-scavenging enzymes in crab apple fruits (Malus baccata). Proc Natl Acad Sci India Sect B Biol Sci 86:877–885. https://doi.org/10.1007/s40011-015-0529-6
Shin Y, Liu RH, Nock JF, Holliday D, Watkins CB (2007) Temperature and relative humidity effects on quality, total ascorbic acid, phenolics and flavonoid concentrations, and antioxidant activity of strawberry. Postharvest Biol Technol 45:349–357. https://doi.org/10.1016/j.postharvbio.2007.03.007
Sozmen AB, Canbay E, Sozmen EY, Ovez B (2018) The effect of temperature and light intensity during cultivation of Chlorella miniata on antioxidant, anti-inflammatory potentials and phenolic compound accumulation. Biocatal Agric Biotechnol 14:366–374. https://doi.org/10.1016/j.bcab.2018.03.023
Szankowski I, Flachowsky H, Li HH, Halbwirth H, Treutter D, Regos I, Hanke MV, Stich K, Fischer TC (2009) Shift in polyphenol profile and sublethal phenotype caused by silencing of anthocyanidin synthase in apple (Malus sp.). Planta 229:681e692. https://doi.org/10.1007/s00425-008-0864-4
Taulavuori K, Hyöky V, Oksanen J, Taulavuori E, Julkunen-Tiitto R (2016) Species-specific differences in synthesis of flavonoids and phenolic acids under increasing periods of enhanced blue light. Environ Exp Bot 121:145–150. https://doi.org/10.1016/j.envexpbot.2015.04.002
Tian J, Han ZY, Zhang J, Hu Y, Song T, Yao Y (2015) The balance of expression of dihydroflavonol 4-reductase and flavonol synthase regulates flavonoid biosynthesis and red foliage coloration in crabapples. Sci Rep 5:1–14. https://doi.org/10.1038/srep12228
Tsao R, Yang R, Young JC, Zhu H (2003) Polyphenolic profiles in eight apple cultivars using high-performance liquid chromatography (HPLC). J Agric Food Chem 51:6347–6353. https://doi.org/10.1021/jf0346298
Yoshizawa Y, Sakurai K, Kawaii S, Soejima J, Murofushi N (2007) Antiproliferative and antioxidant properties of crabapple juices. Food Sci Technol Res 10:278–281. https://doi.org/10.3136/fstr.10.278
Zhang M, Zhang G, You Y, Yang C, Li P, Ma F (2016) Effects of relative air humidity on the phenolic compounds contents and coloration in the ‘Fuji’ apple (Malus domestica Borkh.) peel. Sci Hortic 201:18–23. https://doi.org/10.1016/j.scienta.2016.01.017
Acknowledgements
The authors are grateful to the China Scholarship Council (CSC) for funding this study. We are also very thankful to Weiyang Tao from Utrecht University, The Netherland, for helping us to carry out Pearson correlation by Corrplot R.
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Rehman, R.N.U., Ali, S., Hasan, M.U. et al. Low temperature and hypoxic conditions induce flavonoids biosynthesis and enhances antioxidant potential of crabapple (Malus profusion) fruits. Acta Physiol Plant 43, 131 (2021). https://doi.org/10.1007/s11738-021-03302-5
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DOI: https://doi.org/10.1007/s11738-021-03302-5