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Articles

Study of physiological and biochemical responses to freezing stress in pomegranate (Punica granatum L.) trees during acclimation and deaclimation cycle

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Pages 341-355 | Accepted 25 Sep 2019, Published online: 12 Oct 2019

References

  • Aebi, H. (1984). Catalase in vitro. Methods in Enzymology, 105, 121–126.
  • Agricultural Statistics. (2017). Executive committee on management of environmental stresses for horticultural products. Tehran, Iran: Iran Ministry of Agriculture.
  • Ahmad, P., Jaleel, C.A., Salem, M.A., Nabi, G., & Sharma, S. (2010). Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Critical Reviews in Biotechnology, 30, 161–175. doi:10.3109/07388550903524243
  • Ali, M.B., Hahn, E.J., & Paek, K.Y. (2005). Effects of light intensities on antioxidant enzymes and malondialdehyde content during short-term acclimatization on micropropagated Phalaenopsis plantlet. Environmental and Experimental Botany, 54, 109–120. doi:10.1016/j.envexpbot.2004.06.005
  • An, F., Li, G., Li, Q.X., Li, K., Carvalho, L.J., Ou, W., & Chen, S. (2016). The comparatively proteomic analysis in response to cold stress in cassava plantlets. Plant Molecular Biology Reporter, 34, 1095–1110. doi:10.1007/s11105-016-0987-x
  • Angelcheva, L., Mishra, Y., Antti, H., Kjellsen, T.D., Funk, C., Strimbeck, R.G., & Schroder, W.P. (2014). Metabolomic analysis of extreme freezing tolerance in Siberian spruce (Picea obovata). New Phytologist, 204, 545–555. doi:10.1111/nph.12950
  • Anonymous. (2015). Iran statistical year book, area under cultivation and production of selected perennial crops. Statistical Center of Iran Press. Retrieved from https://www.amar.org.ir
  • Arnon, D.I. (1949). Copper enzymes in isolated chloroplasts: Polyphenoloxidases in Beta vulgaris. Plant Physiology, 24, 1–15. doi:10.1104/pp.24.1.1
  • Aslamarz, A.A., Vahdati, K., Hassani, D., Rahemi, M., Mohammadi, N., & Leslie, C. (2011). Cold hardiness and its relationship with proline content in Persian walnut. European Journal of Horticutural Science, 76, 84–90.
  • Baek, K.H., & Skinner, D.Z. (2003). Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. Plant Science, 165, 1221–1227. doi:10.1016/S0168-9452(03)00329-7
  • Bafeel, S.O., & Ibrahim, M.M. (2008). Antioxidants and accumulation of α-tocopherol induce chilling tolerance in Medicago sativa. International Journal of Agriculture and Biology, 10, 593–598.
  • Balanyan, H. (2015). The study of freezing-tolerance indexes in some pomegranate cultivars and genotypes (Doctoral dissertation of Horticultural Science). University of Tehran.
  • Bañuelos, M.L.G., Moreno, L.V., Winzerling, J., Orozco, J.A., & Gardea, A.A. (2008). Winter metabolism in deciduous trees: Mechanisms, genes and associated proteins. Revista Fitotecnia Mexicana, 31, 295–308.
  • Barranco, D., Ruiz, N., & Gómez-del Campo, M. (2005). Frost tolerance of eight olive cultivars. HortScience, 40, 558–560. doi:10.21273/HORTSCI.40.3.558
  • Bates, L.S., Waldren, R.P., & Teare, I.D. (1973). Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205–207. doi:10.1007/BF00018060
  • Berry, J., & Bjorkman, O. (1980). Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31, 491–543. doi:10.1146/annurev.pp.31.060180.002423
  • Björkman, O. (1981). Responses to different quantum flux densities. In: Lange, O.L., Nobel, P.S., Osmond, C.B. & Zeigler, H., Eds., Physiological plant ecology I., Ency in Plant Physiology, NS, 12A, Springer, New York. doi:10.1007/978-3-642-68090-8_4.
  • Cakmak, T., & Atici, Ö. (2009). Effects of putrescine and low temperature on the apoplastic antioxidant enzymes in the leaves of two wheat cultivars. Plant, Soil and Environment, 55, 320–326. doi:10.17221/PSE
  • Cansev, A., Gulen, H., Celik, G., & Eris, A. (2012). Alterations in total phenolic content and antioxidant capacity in response to low temperatures in olive (Olea europaea L.“Gemlik”). Plant Arch, 12, 489–494.
  • Cansev, A., Gulen, H., & Eris, A. (2009). Cold-hardiness of olive (Olea europaea L.) cultivars in cold-acclimated and non-acclimated stages: Seasonal alteration of antioxidative enzymes and dehydrin-like proteins. The Journal of Agricultural Science, 147, 51–61. doi:10.1017/S0021859608008058
  • Chang, C.Y., Unda, F., Zubilewich, A., Mansfield, S.D., & Ensminger, I. (2015). Sensitivity of cold acclimation to elevated autumn temperature in field-grown Pinus strobus seedlings. Frontiers in Plant Science, 6, 165–184. doi:10.3389/fpls.2015.00165
  • Charrier, G., & Améglio, T. (2011). The timing of leaf fall affects cold acclimation by interactions with air temperature through water and carbohydrate contents. Environmental and Experimental Botany, 72, 351–357. doi:10.1016/j.envexpbot.2010.12.019
  • D’Angeli, S., & Altamura, M. (2016). Unsaturated lipids change in olive tree drupe and seed during fruit development and in response to cold-stress and acclimation. International Journal of Molecular Sciences, 17, 1889–1902. doi:10.3390/ijms17111889
  • da Silva, J.A.T., Rana, T.S., Narzary, D., Verma, N., Meshram, D.T., & Ranade, S.A. (2013). Pomegranate biology and biotechnology: A review. Scientia Horticulturae, 160, 85–107. doi:10.1016/j.scienta.2013.05.017
  • Degenkolbe, T., Giavalisco, P., Zuther, E., Seiwert, B., Hincha, D.K., & Willmitzer, L. (2012). Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana. The Plant Journal, 72, 972–982. doi:10.1111/tpj.12007
  • Dhindsa, R.S., Dhindsa, P.P., & Thorpe, T.A. (1980). Leaf senescence correlated with increased levels of membrane permeability and lipid-peroxidation and decreased levels of superoxide dismutase and catalase. Journal of Experimental Botany, 32, 93–101. doi:10.1093/jxb/32.1.93
  • Dionne, J., Castonguay, Y., Nadeau, P., & Desjardins, Y. (2001). Freezing tolerance and carbohydrate changes during cold acclimation of green-type annual bluegrass (Poa annua L.) ecotypes. Crop Science, 41, 443–451. doi:10.2135/cropsci2001.412443x
  • Ershadi, A., Karimi, R., & Mahdei, K.N. (2016). Freezing tolerance and its relationship with soluble carbohydrates, proline and water content in 12 grapevine cultivars. Acta Physiologiae Plantarum, 38, 2–12. doi:10.1007/s11738-015-2021-6
  • García Bañuelos, M.L., Moreno, L.V., Winzerling, J., Orozco, J.A., & Gardea, A.A. (2008). Winter metabolism in deciduous trees: Mechanisms, genes and associated proteins. Revista Fitotecnia Mexicana, 31, 295–308.
  • Ghasemi-Soloklui, A.A., & Ershadi, A. (2012). Evaluation of cold hardiness in seven Iranian commercial pomegranates (Punica granatum) cultivars. HortScience, 47, 1821–1825. doi:10.21273/HORTSCI.47.12.1821
  • González, E.M., de Ancos, B., & Cano, M.P. (1999). Partial characterization of polyphenol oxidase activity in raspberry fruits. Journal of Agricultural and Food Chemistry, 47, 4068–4072. doi:10.1021/jf981325q
  • Haque, M.S., Islam, M.M., Rakib, M.A., & Haque, M.A. (2014). A regulatory approach on low temperature induced enzymatic and anti-oxidative status in leaf of Pui vegetable (Basella alba). Saudi Journal of Biological Sciences, 21, 366–373. doi:10.1016/j.sjbs.2013.10.006
  • Hussain, S., Liu, G., Liu, D., Ahmed, M., Hussain, N., & Teng, Y. (2015). Study on the expression of dehydrin genes and activities of antioxidative enzymes in floral buds of two sand pear (Pyrus pyrifolia Nakai) cultivars requiring different chilling hours for bud break. Turkish Journal of Agriculture and Forestry, 39, 930–939. doi:10.3906/tar-1407-164
  • Ito, A., Sakamoto, D., & Moriguchi, T. (2012). Carbohydrate metabolism and its possible roles in endodormancy transition in Japanese pear. Scientia Horticulturae, 144, 187–194. doi:10.1016/j.scienta.2012.07.009
  • Junttila, O. (1989). Physiological responses to low temperature. Annals of Forest Science, 46, 604–613. doi:10.1051/forest:198905ART0137
  • Kalberer, S.R., Wisniewski, M., & Arora, R. (2006). Deacclimation and reacclimation of cold-hardy plants: Current understanding and emerging concepts. Plant Science, 171, 3–16. doi:10.1016/j.plantsci.2006.02.013
  • Kaminski, W., & Rom, R. (1974). Possible role of catalase in the rest of peach, Prunus persica, Sieb. and Zucc., flower buds. Journal of the American Society for Horticultural Science, 99, 86–94.
  • Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., & Gatzke, N. (2004). Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiology, 136, 4159–4168. doi:10.1104/pp.104.052142
  • Kavikishor, P.B., & Sreenivasulu, N. (2014). Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant, Cell & Environment, 37, 300–311. doi:10.1016/j.heliyon.2017.e00402
  • Kreyling, J., Schmid, S., & Aas, G. (2015). Cold tolerance of tree species is related to the climate of their native ranges. Journal of Biogeography, 42, 156–166. doi:10.1111/jbi.12411
  • Landry, E.J., Fuchs, S.J., Bradley, V.L., & Johnson, R.C. (2017). The effect of cold acclimation on the low molecular weight carbohydrate composition of safflower. Heliyon, 3, e00402. doi:10.1016/j.heliyon.2017.e00402
  • Lee, J.H., Yu, D.J., Kim, S.J., Choi, D., & Lee, H.J. (2012). Intraspecies differences in cold hardiness, carbohydrate content and β-amylase gene expression of Vaccinium corymbosum during cold acclimation and deacclimation. Tree Physiology, 32, 1533–1540. doi:10.1093/treephys/tps102
  • Leonardi, G.D.A., Carlos, N.A., Mazzafera, P., & Balbuena, T.S. (2015). Eucalyptus urograndis stem proteome is responsive to short-term cold stress. Genetics and Molecular Biology, 38, 191–198. doi:10.1590/S1415-475738220140235
  • Lewandowska, M., & Jarvis, P.G. (1977). Changes in chlorophyll and carotenoid content, specific leaf area and dry weight fraction in Sitka spruce, in response to shading and season. The New Phytologist, 79, 247–256. doi:10.1111/nph.1977.79.issue-2
  • Li, G., Hu, Q., Shi, Y., Cui, K., Nie, L., Huang, J., & Peng, S. (2018). Low nitrogen application enhances starch-metabolizing enzyme activity and improves accumulation and translocation of non-structural carbohydrates in rice stems. Frontiers in Plant Science, 9, 1128–1133. doi:10.3389/fpls.2018.01128
  • MacAdam, J.W., Nelson, C.J., & Sharp, R.E. (1992). Peroxidase activity in the leaf elongation zone of tall fescue: I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiology, 99, 872–878. doi:10.1104/pp.99.3.872
  • Matteucci, M., D’angeli, S., Errico, S., Lamanna, R., Perrotta, G., & Altamura, M.M. (2011. Cold affects the transcription of fatty acid desaturases and oil quality in the fruit of Olea europaea L. genotypes with) different cold hardiness.Journal of Experimental Botany, 62, 3403–3420. doi:10.1093/jxb/err013
  • McCready, R.M., Guggolz, J., Silviera, V., & Ownes, H.S. (1950). Determination of starch and amylase in vegetables. Analytical Chemistry, 22, 1156–1158. doi:10.1021/ac60045a016
  • Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405–410.
  • Morin, X., Améglio, T., Ahas, R., Kurz-Besson, C., Lanta, V., Lebourgeois, F., … Chuine, I. (2007). Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiology, 27, 817–825. doi:10.1093/treephys/27.6.817
  • Muller, O., Hikosaka, K., & Hirose, T. (2005). Seasonal changes in light and temperature affect the balance between light harvesting and light utilization components of photosynthesis in an evergreen understory shrub. Oecologia, 143, 501–508. doi:10.1007/s00442-005-0024-5
  • Murshed, R., Lopez-Lauri, F., & Sallanon, H. (2013). Effect of water stress on antioxidant systems and oxidative parameters in fruits of tomato (Solanum lycopersicon L, cv. Micro-tom). Physiology and Molecular Biology of Plants, 19, 363–378. doi:10.1007/s12298-013-0173-7
  • Nasrabadi, M., Ramezanian, A., Eshghi, S., Kamgar-Haghighi, A.A., Vazifeshenas, M.R., & Valero, D. (2019). Biochemical changes and winter hardiness in pomegranate (Punica granatum L.) trees grown under deficit irrigation. Scientia Horticulturae, 251, 39–47. doi:10.1016/j.scienta.2019.03.005
  • Nir, G., Shulman, Y., Fanberstein, L., & Lavee, S. (1986). Changes in the activity of catalase (EC 1.11. 1.6) in relation to the dormancy of grapevine (Vitis vinifera L.) buds. Plant Physiology, 81, 1140–1142. doi:10.1104/pp.81.4.1140
  • Noctor, G., & Foyer, C.H. (1998). Ascorbate and glutathione: Keeping active oxygen under control. Annual Review of Plant Physiology, 49, 249–279. doi:10.1146/annurev.arplant.49.1.249
  • Palta, J.P., & Li, P.H. (1980). Alterations in membrane transport properties by freezing injury in herbaceous plants: Evidence against rupture theory. Physiologia Plantarum, 50, 169–175. doi:10.1111/ppl.1980.50.issue-2
  • Pennycooke, J.C., Cox, S., & Stushnoff, C. (2005). Relationship of cold acclimation, total phenolic content and antioxidant capacity with chilling tolerance in petunia (Petunia× hybrida). Environmental and Experimental Botany, 53, 225–232. doi:10.1016/j.envexpbot.2004.04.002
  • Pommerrenig, B., Ludewig, F., Cvetkovic1, J., Trentmann, O., Klemens, P.A.M., & Neuhaus, H.E. (2018). In concert: Orchestrated changes in carbohydrate homeostasis are critical for plant abiotic stress tolerance. Plant & Cell Physiology, 59, 1290–1299. doi:10.1093/pcp/pcy063
  • Pourghayoumi, M., Rahemi, M., Bakhshi, D., Aalami, A., & Kamgar-Haghighi, A.A. (2017). Responses of pomegranate cultivars to severe water stress and recovery: Changes on antioxidant enzyme activities, gene expression patterns and water stress responsive metabolites. Physiology and Molecular Biology of Plants, 23, 321–330. doi:10.1007/s12298-017-0435-x
  • Rossi, S., Deslauriers, A., Griçar, J., Seo, J.-W., Rathgeber, C.B., Anfodillo, T., … Jalkanen, R. (2008). Critical temperatures for xylogenesis in conifers of cold climates Global Ecology and Biogeography, 17, 696–707. doi:10.1111/geb.2008.17.issue-6
  • Saadati, S., Baninasab, B., Mobli, M., & Gholami, M. (2019). Measurements of freezing tolerance and their relationship with some biochemical and physiological parameters in seven olive cultivars. Acta Physiologiae Plantarum, 41, 51. doi:10.1007/s11738-019-2843-8
  • Sakai, A. (1983). Comparative study on freezing resistance of conifers with special reference to cold adaptation and its evolutive aspects. Canadian Journal of Botany, 61, 2323–2332. doi:10.1139/b83-255
  • Sakai, A., & Larcher, W. (1987). Frost survival of plants: Responses and adaptation to freezing stress. (Vol. 62, p. 321), Berlin Heidelberg: Springer-Verlag.
  • Sakai, A., & Weiser, C.J. (1973). Freezing resistance of trees in North America with reference to tree regions. Ecology, 54, 118–126. doi:10.2307/1934380
  • Sarikhani, H., Haghi, H., Ershadi, A., Esna-Ashari, M., & Pouya, M. (2014). Foliar application of potassium sulphate enhances the cold-hardiness of grapevine (Vitis vinifera L.). The Journal of Horticultural Science and Biotechnology, 89, 141–146. doi:10.1080/14620316.2014.11513060
  • Schulze, W.X., Schneider, T., Starck, S., Martinoia, E., & Trentmann, O. (2012). Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. The Plant Journal, 69, 529–541. doi:10.1111/j.1365-313X.2011.04812.x
  • Sekozawa, Y., Sugaya, S., Gemma, H., & Iwahori, S. (2003). Cold tolerance in ‘Kousui’ Japanese pear and possibility for avoiding frost injury by treatment with n-propyl dihydrojasmonate. HortScience, 38, 288–292. doi:10.21273/HORTSCI.38.2.288
  • Selahvarzi, Y., Davarinejad, G.H.M., Tehranifar, A., Nemati, H., & Nezami, A. (2010). Study of physiological responses of six Khorasan Razavi pomegranate cultivars to freezing stress. International Journal of Horticultural Science and Technology, 11, 197–208. (In Farsi).
  • Simmonds, N.W. (Ed) (1976). Evolution of crop plants. Longman Group Ltd, London. pp. 339.
  • Singleton, V.L., & Rossi, J.A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16, 144–158.
  • Soloklui, A.A.G., Gharaghani, A., Oraguzie, N., Eshghi, S., & Vazifeshenas, M. (2017). Chilling and heat requirements of 20 Iranian pomegranate cultivars and their correlations with geographical and climatic parameters, as well as tree and fruit characteristics. HortScience, 52, 560–565. doi:10.21273/HORTSCI11614-16
  • Soluklui, G., Akbar, A., Ershadi, A., & Fallahi, E. (2014). Paclobutrazol-induced biochemical changes in pomegranate (Punica granatum L.) cv.‘Malas Saveh’ under freezing stress. Journal of Horticultural Science and Technology, 1, 181–190.
  • Steponkus, P.L. (1984). Role of the plasma membrane in freezing injury and cold acclimation. Annual Review of Plant Physiology, 35, 543–584. doi:10.1146/annurev.pp.35.060184.002551
  • Strimbeck, G.R., Kjellsen, T.D., Schaberg, P.G., & Murakami, P.F. (2007). Cold in the common garden: Comparative low-temperature tolerance of boreal and temperate conifer foliage. Trees, 21, 557–567. doi:10.1007/s00468-007-0151-1
  • Strimbeck, G.R., Schaberg, P.G., Fossdal, C.G., Schröder, W.P., & Kjellsen, T.D. (2015). Extreme low temperature tolerance in woody plants. Frontiers in Plant Science, 6, 884–898. doi:10.3389/fpls.2015.00884
  • Thirugnanasambantham, K., Senthilkumar, P., Sureshramraj, S.C.B., & Mandal, A.K.A. (2013). Differential activity of antioxidative enzymes in active and temporarily dormant buds of tea (Camellia sinensis). American-Eurasian Journal of Agricultural & Environmental Sciences, 13, 1400–1406.
  • Thomson, G. (1989). Membrane acclimation by unicellular organisms in response to temperature change. Journal of Bioenergetics and Biomembranes, 21, 43–60. doi:10.1007/BF00762211
  • Tsikas, D. (2017). Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples. Analytical Biochemistry, 524, 13–30. doi:10.1016/j.ab.2016.10.021
  • Viuda‐Martos, M., Fernández‐López, J., & Pérez‐Álvarez, J. (2010). Pomegranate and its many functional components as related to human health: A review. Comprehensive Reviews in Food Science and Food Safety, 9, 635–654. doi:10.1111/crfs.2010.9.issue-6
  • Wang, S.Y., Jiao, H.J., & Faust, M. (1991). Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron‐induced bud break of apple. Physiologia Plantarum, 82, 231–236. doi:10.1111/ppl.1991.82.issue-2
  • Wang, W.B., Kim, Y.H., Lee, H.S., Deng, X.P., & Kwak, S.S. (2009). Differential antioxidation activities in two alfalfa cultivars under chilling stress. Plant Biotechnology Reports, 3, 301–307. doi:10.1007/s11816-009-0102-y
  • Wang, Y., Hu, Y., Chen, B., Zhu, Y., Dawuda, M.M., & Svetla, S. (2018). Physiological mechanisms of resistance to cold stress associated with 10 elite apple rootstocks. Journal of Integrative Agriculture, 17, 857–866. doi:10.1016/S2095-3119(17)61760-X
  • Wisniewski, M., Close, T.J., Artlip, T., & Arora, R. (1996). Seasonal patterns of dehydrins and 70‐kDa heat‐shock proteins in bark tissues of eight species of woody plants. Physiologia Plantarum, 96, 496–505. doi:10.1111/ppl.1996.96.issue-3
  • Yemm, E.W., & Willis., A.J. (1954). The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal, 57, 508–514. doi:10.1042/bj0570508
  • Yun, S.K., Bae, H., Chung, K.H., Yoon, I.K., Nam, E.Y., Kwon, J.H., & Jun, J.H. (2014). Sugar, starch, and proline in peach trees exposed to freezing temperatures during dehardening. Journal of Agricultural Sciences, 5, 913–921.
  • Zeng, X., Xu, Y., Jiang, J., Zhang, F., Ma, L., Wu, D., … Sun, W. (2018). Identification of cold stress responsive microRNAs in two winter turnip rape (Brassica rapa L.) by high throughput sequencing. BMC Plant Biology, 18, 18–52. doi:10.1186/s12870-018-1232-6
  • Zhang, Z.Q., Pang, X.Q., Xuewu, X.., Ji, Z., & Jiang, Y. (2005). Role of peroxidase in anthocyanin degradation in litchi fruit pericarp. Food Chemistry, 90, 47–52. doi:10.1016/j.foodchem.2004.03.023

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