Preconditioning treatment induces chilling tolerance in zucchini fruit improving different physiological mechanisms against cold injury

Annals of Applied BiologyVolume 166, Issue 2 p. 340-354 RESEARCH ARTICLE Preconditioning treatment induces chilling tolerance in zucchini fruit improving different physiological mechanisms against cold injury F. Carvajal, F. Carvajal Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, SpainSearch for more papers by this authorF. Palma, F. Palma Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, SpainSearch for more papers by this authorM. Jamilena, M. Jamilena Department of Biology and Geology, Escuela Superior de Ingeniería, University of Almería, Almería, SpainSearch for more papers by this authorD. Garrido, Corresponding Author D. Garrido Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain Correspondence Dr. Dolores Garrido, Department of Plant Physiology, Facultad de Ciencias, University of Granada, Fuentenueva s/n, 18071 Granada, Spain. Email: [email protected] .Search for more papers by this author F. Carvajal, F. Carvajal Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, SpainSearch for more papers by this authorF. Palma, F. Palma Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, SpainSearch for more papers by this authorM. Jamilena, M. Jamilena Department of Biology and Geology, Escuela Superior de Ingeniería, University of Almería, Almería, SpainSearch for more papers by this authorD. Garrido, Corresponding Author D. Garrido Department of Plant Physiology, Facultad de Ciencias, University of Granada, Granada, Spain Correspondence Dr. Dolores Garrido, Department of Plant Physiology, Facultad de Ciencias, University of Granada, Fuentenueva s/n, 18071 Granada, Spain. Email: [email protected] .Search for more papers by this author First published: 16 December 2014 https://doi.org/10.1111/aab.12189Citations: 53Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract Zucchini fruit is susceptible to develop chilling injuries (CI) when stored at low temperature. In this study, the effects of a preconditioning treatment during cold storage and its relation with the physiological response to chilling tolerance have been investigated. The commercial variety Sinatra, whose fruit are very sensitive to cold storage, has been used. After harvest, fruit were kept at 4°C or preconditioned during 48 h at 15°C before cold storage. Weight loss, electrolyte leakage and lipid peroxidation were lower in preconditioned at the end of storage time, and CI index was significantly reduced in preconditioned compared to control fruit. The preconditioning treatment improved the energy status of the fruit increasing the pool of ATP, and maintaining the energy charge. The preconditioned fruit improved their antioxidant status with lower H2O2 content and induction of ascorbate peroxidase (APX) and catalase (CAT) activities. A reduction in putrescine was detected in preconditioned fruit along with a lower expression of arginine decarboxylase (ADC) and ornithine decarboxylase (ODC) and a rise in activity of diamine oxidase (DAO). The concentrations of glutamate and γ-aminobutyrate (GABA) were lower during preconditioning, while that of proline was higher. In summary, preconditioning treatment induces chilling tolerance in zucchini fruit triggering a defence-response against oxidative stress and increasing ATP pool and proline content. References Alexieva V., Sergiev I., Mapelli S., Karanov E. (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell & Environment, 24, 1337– 1344. Alós E., Rodrigo M.J., Zacarías L. (2013) Transcriptomic analysis of genes involved in the biosynthesis, recycling and degradation of L-ascorbic acid in pepper fruits (Capsicum annuum L.). Plant Science, 207, 2– 11. Arbona V., Hossain Z., López-Climent M.F., Pérez-Clemente R.M., Gómez-Cadenas A. (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiologia Plantarum, 132, 452– 466. Bates L., Waldren R., Teare I. (1973) Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205– 207. Beyer W.F.J., Fridovich I. (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical Biochemistry, 161, 559– 566. 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. Carvajal F., Martinez C., Jamilena M., Garrido D. (2011) Differential response of zucchini varieties to low storage temperature. Scientia Horticulturae, 130, 90– 96. Corpas F., Barroso J., Sandalio L., Distefano S., Palma J., Lupiáñez J., Del Río L. (1998) A dehydrogenase-mediated recycling system of NADPH in plant peroxisomes. Biochemical Journal, 330, 777– 784. Chance B., Maehly A. (1955) Assay of catalases and peroxidases. Methods in Enzymology, 2, 764– 775. Chaudhary P.R., Jayaprakasha G., Porat R., Patil B.S. (2014) Low temperature conditioning reduces chilling injury while maintaining quality and certain bioactive compounds of ‘Star Ruby’ grapefruit. Food Chemistry, 153, 243– 249. Chen B., Yang H. (2013) 6-Benzylaminopurine alleviates chilling injury of postharvest cucumber fruit through modulating antioxidant system and energy status. Journal of the Science of Food and Agriculture, 93, 1915– 1921. Cheeseman J.M. (2006) Hydrogen peroxide concentrations in leaves under natural conditions. Journal of Experimental Botany, 57, 2435– 2444. Edwards E.A., Rawsthorne S., Mullineaux P. (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta, 180, 278– 284. Esaka M., Yamada N., Kitabayashi M., Setoguchi Y., Tsugeki R., Kondo M., Nishimura M. (1997) cDNA cloning and differential gene expression of three catalases in pumpkin. Plant Molecular Biology, 33, 141– 155. Flores H.E., Galston A.W. (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiology, 69, 701– 706. Gupta K., Dey A., Gupta B. (2013) Plant polyamines in abiotic stress responses. Acta Physiologiae Plantarum, 35, 2015– 2036. Hariyadi P., Parkin K.L. (1991) Chilling-induced oxidative stress in cucumber fruits. Postharvest Biology and Technology, 1, 33– 45. Havelda Z., Maule A.J. (2000) Complex spatial responses to cucumber mosaic virus infection in susceptible Cucurbita pepo cotyledons. The Plant Cell Online, 12, 1975– 1985. Heath R.L., Packer L. (1968) Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 189– 198. Hossain M.A., Asada K. (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant and Cell Physiology, 25, 1285– 1295. Hossain M.A., Nakano Y., Asada K. (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant and Cell Physiology, 25, 385– 395. Irigoyen J.J., Einerich D.W., Sánchez-Díaz M. (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiologia Plantarum, 84, 55– 60. Jin P., Wang K., Shang H., Tong J., Zheng Y. (2009) Low-temperature conditioning combined with methyl jasmonate treatment reduces chilling injury of peach fruit. Journal of the Science of Food and Agriculture, 89, 1690– 1696. Kishor P.K., 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. Kuk Y.I., Lee J.H., Kim H.Y., Chung S.J., Chung G.C., Guh J.O., Lee H.J., Burgos N.R. (2003) Relationships of cold acclimation and antioxidative enzymes with chilling tolerance in cucumber (Cucumis sativus L.). Journal of the American Society for Horticultural Science, 128, 661– 666. Lafuente M.T., Belver A., Guye M.G., Saltveit M.E. (1991) Effect of temperature conditioning on chilling injury of cucumber cotyledons: possible role of abscisic acid and heat shock proteins. Plant Physiology, 95, 443– 449. Li P., Zheng X., Liu Y., Zhu Y. (2014) Pre-storage application of oxalic acid alleviates chilling injury in mango fruit by modulating proline metabolism and energy status under chilling stress. Food Chemistry, 142, 72– 78. Livak K.J., Schmittgen T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods, 25, 402– 408. Lyons J.M. (1973) Chilling injury in plants. Annual Review of Plant Physiology, 24, 455– 466. Lyons J.M., Raison J.K. (1970) Oxidative activity of mitochondria isolated from plant tissues sensitive and resistant to chilling injury. Plant Physiology, 45, 386– 389. Mao L.C., Pang H., Wang G., Zhu C. (2007) Phospholipase D and lipoxygenase activity of cucumber fruit in response to chilling stress. Postharvest Biology and Technology, 44, 42– 47. Martínez-Téllez M., Ramos-Clamont M., Gardea A., Vargas-Arispuro I. (2002) Effect of infiltrated polyamines on polygalacturonase activity and chilling injury responses in zucchini squash (Cucurbita pepo L.). Biochemical and Biophysical Research Communications, 295, 98– 101. Maul P., McCollum G., Guy C.L., Porat R. (2011) Temperature conditioning alters transcript abundance of genes related to chilling stress in ‘Marsh’ grapefruit flavedo. Postharvest Biology and Technology, 60, 177– 185. McDonald R.E., Kushad M.M. (1986) Accumulation of putrescine during chilling injury of fruits. Plant Physiology, 82, 324– 326. Mhamdi A., Queval G., Chaouch S., Vanderauwera S., Van Breusegem F., Noctor G. (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. Journal of Experimental Botany, 61, 4197– 4220. Mittler R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405– 410. O'Kane D., Gill V., Boyd P., Burdon R. (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta, 198, 371– 377. Obrero A., Die J.V., Román B., Gómez P., Nadal S., González-Verdejo C.I. (2011) Selection of reference genes for gene expression studies in zucchini (Cucurbita pepo) using qPCR. Journal of Agricultural and Food Chemistry, 59, 5402– 5411. Okuda T., Matsuda Y., Yamanaka A., Sagisaka S. (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiology, 97, 1265– 1267. Palma F., Carvajal F., Lluch C., Jamilena M., Garrido D. (2014a) Changes in carbohydrate content in zucchini fruit (Cucurbita pepo L.) under low temperature stress. Plant Science, 217-218, 78– 86. Palma F., Carvajal F., Jamilena M., Garrido D. (2014b) Contribution of polyamines and other related metabolites to the maintenance of zucchini fruit quality during cold storage. Plant Physiology and Biochemistry, 82, 161– 171. Park E.-J., Jeknic Z., Chen T.H.H. (2006) Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant and Cell Physiology, 47, 706– 714. Pradet A., Raymond P. (1983) Adenine nucleotide ratios and adenylate energy charge in energy metabolism. Annual Review of Plant Physiology, 34, 199– 224. Queval G., Hager J., Gakiére B., Noctor G. (2008) Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts. Journal of Experimental Botany, 59, 135– 146. Sala J.M., Lafuente M.T. (1999) Catalase in the heat-induced chilling tolerance of cold-stored hybrid fortune mandarin fruits. Journal of Agricultural and Food Chemistry, 47, 2410– 2414. Saquet A.A., Streif J., Bangerth F. (2003) Energy metabolism and membrane lipid alterations in relation to brown heart development in ‘Conference’ pears during delayed controlled atmosphere storage. Postharvest Biology and Technology, 30, 123– 132. Shelp B.J., Bozzo G.G., Trobacher C.P., Zarei A., Deyman K.L., Brikis C.J. (2012) Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Science, 193, 130– 135. Shigeoka S., Ishikawa T., Tamoi M., Miyagawa Y., Takeda T., Yabuta Y., Yoshimura K. (2002) Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany, 53, 1305– 1319. Shigeoka S., Nakano Y., Kitaoka S. (1980) Metabolism of hydrogen peroxide in Euglena gracilis Z. by L-ascorbic acid peroxidase. Biochemical Journal, 186, 377– 380. Su G., An Z., Zhang W., Liu Y. (2005) Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls. Journal of Plant Physiology, 162, 1297– 1303. Su G., Bai X. (2008) Contribution of putrescine degradation to proline accumulation in soybean leaves under salinity. Biologia Plantarum, 52, 796– 799. Szabados L., Savouré A. (2010) Proline: a multifunctional amino acid? Trends in Plant Science, 15, 89– 97. Verwoerd T.C., Dekker B.M.M., Hoekema A. (1989) A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Research, 17, 2362. Wang C.Y. (1994) Combined treatment of heat shock and low temperature conditioning reduces chilling injury in zucchini squash. Postharvest Biology and Technology, 4, 65– 73. Wang C.Y. (1995) Effect of temperature preconditioning on catalase, peroxidase, and superoxide dismutase in chilled zucchini squash. Postharvest Biology and Technology, 5, 67– 76. Wang C.Y. (1996) Temperature preconditioning affects ascorbate antioxidant system in chilled zucchini squash. Postharvest Biology and Technology, 8, 29– 36. Wongsheree T., Ketsa S., van Doorn W.G. (2009) The relationship between chilling injury and membrane damage in lemon basil (Ocimum × citriodourum) leaves. Postharvest Biology and Technology, 51, 91– 96. Yang Q., Zhang Z., Rao J., Wang Y., Sun Z., Ma Q., Dong X. (2013) Low-temperature conditioning induces chilling tolerance in ‘Hayward’ kiwifruit by enhancing antioxidant enzyme activity and regulating endogenous hormones levels. Journal of the Science of Food and Agriculture, 93, 3691– 3699. Zhang X., Shen L., Li F., Meng D., Sheng J. (2013) Hot air treatment-induced arginine catabolism is associated with elevated polyamines and proline levels and alleviates chilling injury in postharvest tomato fruit. Journal of the Science of Food and Agriculture, 93, 3245– 3251. Zhou Q., Ma C., Cheng S., Wei B., Liu X., Ji S. (2014) Changes in antioxidative metabolism accompanying pitting development in stored blueberry fruit. Postharvest Biology and Technology, 88, 88– 95. Citing Literature Volume166, Issue2March 2015Pages 340-354 ReferencesRelatedInformation