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Cold hardiness of olive (Olea europaea L.) cultivars in cold-acclimated and non-acclimated stages: seasonal alteration of soluble sugars and phospholipids

Published online by Cambridge University Press:  23 March 2009

H. GULEN*
Affiliation:
Horticulture Department, Faculty of Agriculture, Uludag University, Gorukle Kampusu, 16059 Bursa, Turkey
A. CANSEV
Affiliation:
Horticulture Department, Faculty of Agriculture, Uludag University, Gorukle Kampusu, 16059 Bursa, Turkey
A. ERIS
Affiliation:
Horticulture Department, Faculty of Agriculture, Uludag University, Gorukle Kampusu, 16059 Bursa, Turkey
*
*To whom all correspondence should be addressed. Email: hsgulen@uludag.edu.tr

Summary

In many plant species, several physiological and biochemical changes occur during low-temperature-induced cold acclimation. A previous study with olive cultivars (Cansev et al.2009) demonstrated a correlation between the level of accumulation of certain leaf proteins besides antioxidative enzyme activities and cold hardiness of the cultivars. The present paper analysed soluble sugar (SS) and phospholipid (PL) contents of cold-acclimated (CA) and non-acclimated (NA) leaf tissues in order to explain the mechanism of cultivar-dependent response to cold in olive. In general, cold acclimation significantly increased total soluble sugar (TSS), reducing sugars and sucrose contents of all cultivars to various extents depending on the cold hardiness of cultivars. In addition, TSS, reducing sugars and sucrose contents in cold-tolerant cultivars were significantly increased, whereas TSS, reducing sugars and sucrose contents in cold-sensitive cultivars either did not change or increased slightly in CA stage compared with those in NA stage. Even though reducing sugars were the major soluble sugar in olive leaves, levels of sucrose accumulations in CA stage compared with those in NA stage were greater than those observed in reducing sugars accumulation. Changes in levels of total PL, as well as the three individual PL fractions phosphatidylcholine (PC), phosphatidylethanolamine (PE) and phosphatidylinositol (PI), were investigated in olive leaf tissues. Significant increases in levels of PC and PE fractions during CA compared with those in NA stage suggested that PC and PE maintained the cold hardiness of olive cultivars more effectively than did PI. Although the precise mechanisms by which olive responds to cold may still be open to discussion, soluble sugars and PL are clearly important in the ability of olive cultivars to stand against cold stress.

Type
Crops and Soils
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Antikainen, M. & Pihakaski, S. (1994). Early developments in RNA, protein, and sugar levels during cold stress in winter rye (Secale cereale) leaves. Annals of Botany 74, 335341.CrossRefGoogle Scholar
Arora, R. & Wisniewski, M. E. (1994). Cold acclimation in genetically related (Sibling) deciduous and evergreen peach (Prunus persica L. Batsch). II. A 60-kilodalton bark protein in cold-acclimated tissues of peach is heat stable and related to the dehydrin family of proteins. Plant Physiology 105, 95101.CrossRefGoogle Scholar
Barranco, D., Ruiz, N. & Gomez-del Campo, M. (2005). Frost tolerance of eight olive cultivars. HortScience 40, 558560.CrossRefGoogle Scholar
Bartolozzi, F. & Fontanazza, G. (1999). Assessment of frost tolerance in olive (Olea europaea L.). Scientia Horticulturae 81, 309319.CrossRefGoogle Scholar
Bartolozzi, F., Rocchi, P., Camerini, F. & Fontanazza, G. (1999). Changes of biochemical parameters in olive (Olea europaea L.) leaves during an entire vegetative season, and their correlation with frost resistance. Acta Horticulturae 474, 435440.CrossRefGoogle Scholar
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 and Organ Culture 67, 299302.CrossRefGoogle Scholar
Borovskii, G. B., Stupnikova, I. V., Peshkova, A. A., Dorofeev, N. V. & Voinikov, V. K. (1999). Heat-stable proteins of winter wheat seedlings and crowns. Russian Journal of Plant Physiology 46, 678683.Google Scholar
Burak, M. & Eris, A. (1992). Relationships between frost resistance and carbohydrate, protein and lipid contents in buds of some peach cultivars. Acta Horticulturae 315, 6170.CrossRefGoogle Scholar
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. Journal of Agricultural Science, Cambridge 147, 5161.CrossRefGoogle Scholar
Caffrey, M., Fonseca, V. & Leopold, A. C. (1988). Lipid–sugar interactions. Relevance to anhydrous biology. Plant Physiology 86, 754758.CrossRefGoogle ScholarPubMed
Cyril, J., Powell, G. L., Duncan, R. R. & Baird, W. V. (2002). Changes in membrane polar lipid fatty acids of seashore paspalum in response to low temperature exposure. Crop Science 42, 20312037.CrossRefGoogle Scholar
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, 623638.CrossRefGoogle ScholarPubMed
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’). Journal of Horticultural Science and Biotechnology 82, 597604.CrossRefGoogle Scholar
Fiorino, P. & Mancuso, S. (2000). Differential thermal analysis, supercooling and cell viability in organs of Olea europaea at subzero temperatures. Advances in Horticultural Science 14, 2327.Google Scholar
Folch, J., Lees, M. & Sloane-Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry 226, 497509.CrossRefGoogle ScholarPubMed
Fontanazza, G. (1985). II dopo gelo: rinnovamento dell'olivicoltura su basi moderne. Informatore Agrario 24, 5360.Google Scholar
Galiba, G. (1994). In vitro adaptation for drought and cold hardiness in wheat. In Plant Breeding Reviews (Ed. Janick, J.), Vol. 12, pp. 115162. New York: John Wiley and Sons.CrossRefGoogle Scholar
Galiba, G., Kerepesi, I., Snape, J. W. & Sutka, J. (1997). Location of a gene regulating cold-induced carbohydrate production on chromosome 5A of wheat. Theoretical and Applied Genetics 95, 265270.CrossRefGoogle Scholar
Guy, C. L. (1990). Cold acclimation and freezing stress tolerance: role of protein metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 41, 187223.CrossRefGoogle Scholar
Guy, C. L., Huber, J. L. & Huber, S. C. (1992). Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiology 100, 502508.CrossRefGoogle ScholarPubMed
Jacobsen, S. E., Monteros, C., Christiansen, J. L., Bravo, L. A., Corcuera, L. J. & Mujica, A. (2005). Plant responses of quinoa (Chenopodium quinoa Willd.) to frost at various phonological stages. European Journal of Agronomy 22, 131139.CrossRefGoogle Scholar
Kameli, A. & Lösel, D. M. (1993). Charbohydrates and water status in wheat plants under water stress. New Phytologist 125, 609614.CrossRefGoogle Scholar
Knowles, L., Trimble, M. R. & Knowles, N. R. (2001). Phosphorus status affects postharvest respiration, membrane permeability and lipid chemistry of European seedless cucumber fruit (Cucumis sativus L.). Postharvest Biology and Technology 21, 179188.CrossRefGoogle Scholar
Lavee, S. (1989). Involvement of plant growth regulators and endogenous growth substances in the control of alternate bearing. Acta Horticulturae 239, 311322.CrossRefGoogle Scholar
Lavee, S. (1996). Biology and physiology of the olive. In World Olive Encyclopedia (Ed. International Olive Oil Council), pp. 59106. Madrid, Spain: International Olive Oil Council Press.Google Scholar
Leprince, O., Hendry, G. A. F. & McKersie, B. D. (1993). The mechanisms of desiccation tolerance in developing seeds. Seed Science Research 3, 231246.CrossRefGoogle Scholar
Levitt, J. (1980). Responses of Plants to Environmental Stresses, Vol. 1 (2nd edn). New York: Academic Press.Google Scholar
Lynch, D. V. & Steponkus, P. L. (1987). Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv. Puma). Plant Physiology 83, 761767.CrossRefGoogle ScholarPubMed
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 and Environment 23, 291299.CrossRefGoogle Scholar
Miller, G. L. (1959). Use of dinitrosalicylic acid reagent for determination of reducing sugars. Analytical Chemistry 31, 426428.CrossRefGoogle Scholar
Ögren, E., Nilsson, T. & Sundblad, L-G. (1997). Relationship between respiratory depletion of sugars and loss of cold hardiness in coniferous seedlings over-wintering at raised temperatures: indications of different sensitivities of spuce and pine. Plant Cell and Environment 20, 247253.CrossRefGoogle Scholar
Palonen, P. (1999). Relationship of seasonal changes in carbohydrates and cold hardiness in canes and buds of three red raspberry cultivars. Journal of the American Society for Horticultural Science 124, 507513.CrossRefGoogle Scholar
Palta, J. P., Whitaker, B. D. & Weiss, L. S. (1993). Plasma membrane lipids associated with genetic variability in freezing tolerance and cold acclimation of Solanum species. Plant Physiology 103, 793803.CrossRefGoogle ScholarPubMed
Perras, M. & Sarhan, F. (1984). Energy state of spring and winter wheat during cold hardening. Soluble sugars and adenine nucleotides. Physiologia Plantarum 60, 129132.CrossRefGoogle Scholar
Proietti, P. & Famiani, F. (2002). Diurnal and seasonal changes in photosynthetic characteristics in different olive (Olea europaea L.) cultivars. Photosynthetica 40, 171176.CrossRefGoogle Scholar
Sasaki, H., Ichimura, K. & Oda, M. (1996). Changes in sugar content during cold acclimation and deacclimation of cabbage seedlings. Annals of Botany 78, 365369.CrossRefGoogle Scholar
Sasaki, H., Ichimura, K., Okada, K. & Oda, M. (1998). Freezing tolerance and soluble sugar contents affected by water stress during cold-acclimation and de-acclimation in cabbage seedlings. Scientia Horticulturae 76, 161169.CrossRefGoogle Scholar
Sasaki, H., Ichimura, K., Imada, S. & Yamaki, S. (2001). Sucrose synthase and sucrose phosphate synthase, but not acid invertase, are regulated by cold acclimation and deacclimation in cabbage seedlings. Journal of Plant Physiology 158, 847852.CrossRefGoogle Scholar
Sauter, J. J., Wisniewski, M. & Witt, W. (1996). Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus×canadensis Moench ‘robusta’) wood. Journal of Plant Physiology 149, 451461.CrossRefGoogle Scholar
Sikorska, E. & Kacperska-Palacz, A. (1979). Phospholipid involvement in frost tolerance. Physiologia Plantarum 47, 144150.CrossRefGoogle Scholar
Steponkus, P. L. & Webb, M. S. (1992). Freeze-induced dehydration and membrane destabilization in plants. In Water and Life: Comparative Analysis of Water Relationships at the Organismic, Cellular and Molecular Level (Eds Somero, G. N., Osmond, C. B. & Bolis, C. L.), pp. 338362. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Steponkus, P. L., Lynch, D. V. & Uemura, M. (1990). The influence of cold acclimation on the lipid composition and cryobehaviour of the plasma membrane of isolated rye protoplasts. Philosophical Transaction of the Royal Society of London B: Biological Sciences 326, 571583.Google Scholar
Steponkus, P. L., Uemura, M. & Webb, M. S. (1993). A contrast of the cryostability of the plasma membrane of winter rye and spring oat – two species that widely differ in their freezing tolerance and plasma membrane lipid composition. In Advances in Low-temperature Biology (Ed. Steponkus, P. L.), Vol. 2, pp. 211312. London: JAI Press.Google Scholar
Stitt, M. & Hurry, V. (2002). A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Current Opinion in Plant Biology 5, 199206.CrossRefGoogle ScholarPubMed
Stone, J. M., Palta, J. P., Bamberg, J. B., Weiss, L. S. & Harbage, J. F. (1993). Inheritance of freezing resistance in tuber-bearing Solanum species: evidence for independent genetic control of nonacclimated freezing tolerance and cold acclimation capacity. Proceedings of the National Academy of Sciences, USA 90, 78697873.CrossRefGoogle ScholarPubMed
Stupnikova, I. V., Borovskii, G. B., Dorofeev, N. V., Peshkova, A. A. & Voinikov, V. K. (2002). Accumulation and disappearance of dehydrins and sugars depending on freezing tolerance of winter wheat plants at different developmental phases. Journal of Thermal Biology 27, 5560.CrossRefGoogle Scholar
Svanborg, A. & Svennerholm, L. (1961). Plasma total lipids, cholesterol, triglycerides, phospholipids and free fatty acids in a healthy Scandinavian population. Acta Medica Scandinavica 169, 4349.CrossRefGoogle Scholar
Tabaei-Aghdaei, S. R., Pearce, R. S. & Harrison, P. (2003). Sugars regulate cold-induced gene expression and freezing-tolerance in barley cell cultures. Journal of Experimental Botany 54, 15651575.CrossRefGoogle ScholarPubMed
Thomashow, M. F. (1999). Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571599.CrossRefGoogle ScholarPubMed
Uemura, M. & Steponkus, P. L. (1994). A contrast of the plasma membrane lipid composition of oat and winter rye leaves in relation to freezing tolerance. Plant Physiology 104, 479496.CrossRefGoogle Scholar
Uemura, M. & Yoshida, S. (1984). Involvement of plasma membrane alterations in cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiology 75, 818826.CrossRefGoogle ScholarPubMed
Uemura, M., Joseph, R. A. & Steponkus, P. L. (1995). Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiology 109, 1530.CrossRefGoogle ScholarPubMed
Uemura, M., Warren, G. & Steponkus, P. L. (2003). Freezing sensitivity in the sfr4 mutant of Arabidopsis is due to low sugar content and is manifested by loss of osmotic responsiveness. Plant Physiology 131, 18001807.CrossRefGoogle ScholarPubMed
Uemura, M., Tomınaga, Y., Nakagawara, C., Shıgematsu, S., Mınamı, A. & Kawamura, Y. (2006). Responses of the plasma membrane to low temperatures. Physiologia Plantarum 126, 8189.CrossRefGoogle Scholar
Vagujfalvi, A., Kerepesi, I., Galiba, G., Tischner, T. & Sutka, J. (1999). Frost hardiness depending on carbohydrate changes during cold acclimation in wheat. Plant Science 144, 8592.CrossRefGoogle Scholar
Van Handel, E. (1968). Direct microdetermination of sucrose. Analytical Biochemistry 22, 280283.CrossRefGoogle ScholarPubMed
Wang, S. Y. & Lin, H-S. (2006). Effect of plant growth temperature on membrane lipids in strawberry (Fragaria×ananassa Duch.). Scientia Horticulturae 108, 3542.CrossRefGoogle Scholar
Wei, H., Dhanaraj, A. L., Arora, R., Rowland, L. J., Fu, Y. & Sun, L. (2006). Identification of cold acclimation-responsive Rhododendron genes for lipid metabolism, membrane transport and lignin biosynthesis: importance of moderately abundant ESTs in genomic studies. Plant, Cell and Environment 29, 558570.CrossRefGoogle ScholarPubMed
Yoshida, S. & Sakai, A. (1974). Phospholipid degradation in frozen plant cells associated with freezing injury. Plant Physiology 53, 509511.CrossRefGoogle ScholarPubMed