Abstract
The freezing tolerance of seven olive cultivars, including Amphisis, Conservallia, Koroneiki, Manzanilla, Gorgan, Shengeh, and Rashid, was compared, and its correlation with some biochemical and physiological factors was investigated. From each cultivar, leaf and stem samples were collected and sorted into two groups: the first was exposed to various freezing temperatures to indicate its freezing tolerance in terms of lethal temperature (LT50) values by several approaches (electrolyte leakage, maximum quantum yield of PSII photochemistry, and tetrazolium staining test); the second was prepared for some biochemical and physiological parameter analyses. Of all cultivars, Amphisis and Shengeh showed the highest freezing tolerance, the maximum soluble carbohydrate and proline content, DPPH (1, 1-diphenyl–2-picrylhydrazyl) scavenging capacity, the minimum malondialdehyde (MDA), and relative water content (RWC). Conservallia, Gorgan, and Manzanilla cultivars could moderately tolerate freezing temperatures, whereas Rashid and Koroneiki cultivars turned out to be freezing-susceptible. In olive bark and leaf, LT50 showed a negative correlation with soluble carbohydrate, proline content, and DPPH scavenging capacity and a positive correlation with MDA and RWC. Three indicators, i.e., LT50, osmoregulant content, and DPPH scavenging capacity, can contribute to screening the freezing-tolerant olive cultivars.
Similar content being viewed by others
References
Adams GT, Perkins TD (1993) Assessing cold tolerance in Picea using chlorophyll fluorescence. Environ exper bot 33:377–382
Aparicio R, Luna G (2002) Characterisation of monovarietal virgin olive oils. Eur J Lipid Sci Technol 104:614–627
Arias NS, Bucci SJ, Scholz FG, Goldstein G (2015) Freezing avoidance by supercooling in Olea europaea cultivars: the role of apoplastic water solute content and cell wall rigidity. Plant Cell Environ 38:2061–2070
Arora R, Wisniewski ME, Scorza R (1992) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch). Plant Physiol 99:1562–1568
Azzarello E, Mugnai S, Pandolfi C, Masi E, Marone E, Mancuso S (2009) Comparing image (fractal analysis) and electrochemical (impedance spectroscopy and electrolyte leakage) techniques for the assessment of the freezing tolerance in olive. Trees 23:159–167
Ball MC, Canny MJ, Huang CX, Heady RD (2004) Structural changes in acclimated and unacclimated leaves during freezing and thawing. Funct Plant Biol 31:29–40
Barranco D, Ruiz N, Gomez-del-Campo M (2005) Frost tolerance of eight olive cultivars. HortScience 40:558–560
Bartolozzi F, Fontanazza G (1999) Assessment of frost tolerance in olive (Olea europaea L.). Sci Hortic 81:309–319
Bartolozzi F, Mencuccini M, Fontanazza G (2001) Enhancement of frost tolerance in olive shoots in vitro by cold acclimation and sucrose increase in the culture medium. Plant Cell Tissue Organ Cult 67:299–302
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207
Cai Q, Wang S, Cui Z, Sun J, Ishii Y (2004) Changes in freezing tolerance and its relationship with the contents of carbohydrates and proline in overwintering centipedegrass (Eremochloa ophiuroides (Munro) Hack.). Plant prod sci 7:421–426
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. J Agric Sci 147:51–61
Cheung LM, Cheung PCK, Ooi VEC (2003) Antioxidant activity and total phenolics of edible mushroom extracts. Food Chem 81:249–255
Clement JMAM, Van Hasselt PR (1996) Chlorophyll fluorescence as a parameter for frost hardiness in winter wheat. A comparison with other hardiness parameters. Phyton Ann Rei Bot Austria 36:29–41
Couée I, Sulmon C, Gouesbet G, ElAmrani A (2006) Involvement of solubles ugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459
Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638
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 Sci 41:443–451
Eris A, Gulen H, Barut E, Cansev A (2007) Annual patterns of total soluble sugars and proteins related to cold–hardiness in olive (Olea europaea L. ‘Gemlik’). J Hort Sci Biotechnol 82:597–604
Ershadi A, Karimi R, Naderi Mahdei K (2016) Freezing tolerance and its relationship with soluble carbohydrates proline and water content in 12 grapevine cultivars. Acta Physiol Plant 38:2–10
Fiorino P, Mancuso S (2000) Differential thermal analysis supercooling and cell viability in organs of Olea europaea at subzero temperatures. Adv Hort Sci 14:23–27
Ghasemi Soloklui AA, Ershadi A, Fallahi E (2012) Evaluation of cold hardiness in seven Iranian commercial pomegranates (Punica granatum L.) cultivars. HortScience 47:1821–1825
Gilmore AM, Matsubara S, Ball MC, Barker DH, Itoh S (2003) Excitation energy flow at 77 K in the photosynthetic apparatus of overwintering evergreens. Plant Cell Environ 26:1021–1034
Gomez–del–Campo M, Barranco D (2005) Field evaluation of frost tolerance in 10 olive cultivars. Plant Genet Resour 3:385–390
Guerra D, Lamontanara A, Bagnaresi P, Orrù L, Rizza F, Zelasco S, Beghè D, Ganino T, Pagani D, Cattivelli L, Mazzucotelli E (2015) Transcriptome changes associated with cold acclimation in leaves of olive tree (Olea europaea L.). Tree Genet Genomes 11:113
Gulcin I, Alici HA, Cesur M (2005) Determination of in vitro antioxidant and radical scavenging activities of propofol. Chem Pharm Bull 53:281–285
Gulen H, Cansev A, Eris A (2009) Cold hardiness of olive (Olea europaea L.) cultivars in cold-acclimated and non-acclimated stages: seasonal alteration of soluble sugars and phospholipids. J Agric Sci 147:459–467
Gusta LV, Wisniewski M (2013) Understanding plant cold hardiness: an opinion. Physiol Plan 147:4–14
Gusta LV, Wisniewski M, Nesbitt NT, Gusta ML (2004) The effect of water, sugars, and proteins on the pattern of ice nucleation and propagation in acclimated and non-acclimated canola leaves. Plant Physiol 135:1642–1653
Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Ann Rev Plant Physiol Plant Mol Biol 41:187–223
Hashempour A, Ghasemnezhad M, FotouhiGhazvini R, Sohani MM (2014a) Olive (Olea europaea L.) freezing tolerance related to antioxidant enzymes activity during cold acclimation and non acclimation. Acta Physiol Plant 36:3231–3241
Hashempour A, Ghasemnezhad M, Ghazvini RF, Sohani MM (2014b) The physiological and biochemical responses to freezing stress of olive plants treated with salicylic acid. Russ J plant physiol 61:443–450
Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extrem 10:4–10
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts I Kinetics and stochiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Hou YD, Guo ZF, Yi Y, Li HN, Li HG, Chen LJ, Ma H, Zhang L, Lin JW, Zhong M (2010) Effects of cold acclimation and exogenous pytohormone abscisic acid treatment on physiological indicators of winterness wheat. J Plant Sci 5:125–136
Irigoyen JJ, Emerich DW, Sanchez–Diaz M (1992) Water stress induced changes in concentration of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60
Jacobsen SE, Monteros C, Christiansen JL, Bravo LA, Corcuera LJ, Mujica A (2005) Plant responses of quinoa (Chenopodium quinoa Willd.) to frost at various phonological stages. Eur J Agron 22:131–139
Kang HM, Saltveit ME (2002) Chilling tolerance of maize cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plant 115:571–576
Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574
Li J, Arkorful E, Cheng S, Zhou Q, Li H, Chen X, Sun K, Li X (2018) Alleviation of cold damage by exogenous application of melatonin in vegetatively propagated tea plant (Camellia sinensis (L.) O. Kuntze). Sci Hortic 238:356–362
Mancuso S (2000) Electrical resistance changes during exposure to low temperature measure chilling and freezing tolerance in olive tree (Olea europaea L.) plants. Plant Cell Environ 23:291–299
Mills LJ, Ferguson JC, Keller M (2006) Cold-hardiness evaluation of grapevine buds and cane tissues. Am J Enol Vitic 57:194–200
Nesbitt ML, Ebel RC, Findley D, Wilkins B, Woods F, Himelrick D (2002) Assays to assess freeze injury of Satsuma mandarin. HortScience 37:871–877
Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263
Ortega–Garcı´a F, Perago´n J (2009) The response of phenylalanine ammonia–lyase polyphenol oxidase and phenols to cold stress in the olive tree (Olea europaea L. cv Picual). J Sci Food 89:1565–1573
Palliotti A, Bongi G (1996) Freezing injury in the olive leaf and effects of mefluidide treatment. Sci Hortic 71:57–63
Palta JP, Levitt J, Stadelman EJ (1977) Freezing injury in onion bulbs cells II post-thawing injury or recovery. Plant Physiol 60:398–401
Proietti P, Famiani F (2002) Diurnal and seasonal changes in photosynthetic characteristics in different olive (Olea europaea L.) cultivars. Photosynthetica 40:171–176
Rihan HZ, Al–Issawi M, Fuller MP (2017) Advances in physiological and molecular aspects of plant cold tolerance. J Plant Interact 12:143–157
Roselli G, Venora G (1990) Relationship between stomatal size and winter hardiness in the olive. Acta Hort 286:89–92
Roselli G, Benelli G, Morelli D (1989) Relationship between stomatal density and winter hardiness in olive (Olea europaea L.). HortScience 64:199–203
Roselli G, La Porta N, Morelli D (1992) Valutazioni del germoplasma di olivo per la tolleranza a stress da freddo. Anti Convegno Germoplasma Frutticolo 9:107–112
Rugini E, Biasi R, Muleo R (2000) Olive (Olea europaea var sativa) transformation. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants. Springer, Dordrecht, pp 245–279
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.). J Hort Sci Biotechnol 89:141–146
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species oxidative damage and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26
Simkeshzadeh N, Mobli M, Etemadi N, Baninasab B (2011) Assessment of the frost resistance in some olive cultivars using visual injuries and chlorophyll fluorescence. J Hort Sci 4:163–169 (In Persian with English abstract)
Solecka D, Kacperska A (2003) Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiol Plant 119:253–262
Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Ann Rev Plant Physiol 35:543–584
Taylor CB (1996) Proline and water deficit: ups and downs. Plant Cell 8:1221–1224
Wang M, Li J, Rangarajan M, Shao Y, LaVoie EJ, Huang T, Ho Ch (1998) Antioxidative phenolic compounds from sage (Salvia officinalis). J Agric Food Chem 46:4869–4873
Weiser CJ (1970) Cold resistance and injury in woody plants: knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169:1269–1278
Wise RR (1995) Chilling–enhanced photooxidation: the production action and study of reactive oxygen species produced during chilling in the light. Photosynth Res 45:79–97
Xin Z, Li PH (1993) Relationship between proline and abscisic acid in the induction of chilling tolerance in maize suspension-cultured cells. Plant Physiol 103:607–613
Zhang X, Ervin EH, LaBranche AJ (2006) Metabolic defense responses of seeded bermudagrass during acclimation to freezing stress. Crop Sci 46:2598–2605
Acknowledgements
The authors wish to express their sincere gratitude to Dr. M. R. Sabzalian and Mr. R. Mohammadi for their valuable help with this experiment. This study was supported by the Research Council of Isfahan University of Technology.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by L. Bavaresco.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Saadati, S., Baninasab, B., Mobli, M. et al. Measurements of freezing tolerance and their relationship with some biochemical and physiological parameters in seven olive cultivars. Acta Physiol Plant 41, 51 (2019). https://doi.org/10.1007/s11738-019-2843-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-019-2843-8