Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Plants can avoid freezing damage by preventing extracellular ice formation below the equilibrium freezing temperature (supercooling). We used Olea europaea cultivars to assess which traits contribute to avoid ice nucleation at sub-zero temperatures. Seasonal leaf water relations, non-structural carbohydrates, nitrogen and tissue damage and ice nucleation temperatures in different plant parts were determined in five cultivars growing in the Patagonian cold desert. Ice seeding in roots occurred at higher temperatures than in stems and leaves. Leaves of cold acclimated cultivars supercooled down to -13°C, substantially lower than the minimum air temperatures observed in the study site. During winter, leaf ice nucleation and leaf freezing damage (LT50) occurred at similar temperatures, typical of plant tissues that supercool. Higher leaf density and cell wall rigidity were observed during winter, consistent with a substantial acclimation to sub-zero temperatures. Larger supercooling capacity and lower LT50 were observed in cold-acclimated cultivars with higher osmotically active solute content, higher tissue elastic adjustments and lower apoplastic water. Irreversible leaf damage was only observed in laboratory experiments at very low temperatures, but not in the field. A comparative analysis of closely related plants avoids phylogenetic independence bias in a comparative study of adaptations to survive low temperatures. © 2015 John Wiley & Sons Ltd.

Registro:

Documento: Artículo
Título:Freezing avoidance by supercooling in Olea europaea cultivars: The role of apoplastic water, solute content and cell wall rigidity
Autor:Arias, N.S.; Bucci, S.J.; Scholz, F.G.; Goldstein, G.
Filiación:Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, C1033AAJ, Argentina
Grupo de Estudios Biofísicos y Eco-fisiológicos (GEBEF), Departamento de Biología, Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco, Comodoro Rivadavia, 9000, Argentina
Laboratorio de Ecología Funcional (LEF), Departamento de Ecología, Genética y Evolución, FCEyN, Universidad de Buenos Aires, Buenos Aires, 1425, Argentina
Department of Biology, University of Miami, Coral Gables, 33124, United States
Palabras clave:Freezing resistance; Ice nucleation; LT50; Non-structural carbohydrate; Olive; acclimation; carbohydrate; cultivar; evergreen tree; freezing; nucleation; solute; Patagonia; Olea europaea; water; acclimatization; cell membrane; cell wall; cold; freezing; metabolism; olive tree; osmosis; physiology; season; transport at the cellular level; Acclimatization; Biological Transport; Cell Membrane; Cell Wall; Cold Temperature; Freezing; Olea; Osmosis; Seasons; Water
Año:2015
Volumen:38
Número:10
Página de inicio:2061
Página de fin:2070
DOI: http://dx.doi.org/10.1111/pce.12529
Título revista:Plant, Cell and Environment
Título revista abreviado:Plant Cell Environ.
ISSN:01407791
CODEN:PLCED
CAS:water, 7732-18-5; Water
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01407791_v38_n10_p2061_Arias

Referencias:

  • Anchordoguy, T.J., Rudolph, A.S., Carpenter, J.F., Crowe, J.H., Modes of interaction of cryoprotectant and phospholipids during freezing (1987) Cryobiology, 24, pp. 324-331
  • Ashworth, E.N., Abeles, F.B., Freezing behavior of water in small pores and the possible role in the freezing of plant tissues (1984) Plant Physiology, 72, pp. 201-204
  • Baldwin, L., Domon, J.M., Klimek, J.F., Fournet, F., Sellier, H., Gillet, F., Rayon, C., Structural alteration of cell wall pectins accompanies pea development in response to cold (2014) Phytochemistry, 104, pp. 37-47
  • Ball, M.C., Canny, M.J., Huang, C.X., Heady, R.D., Structural changes in acclimated and unacclimated leaves during freezing and thawing (2004) Functional Plant Biology, 31, pp. 29-40
  • Bartolozzi, F., Fontanazza, G., Assessment of frost tolerance in olive (Olea europaea L.) (1999) Scientia Horticulturae, 81, pp. 309-319
  • Bartolozzi, F., Mencuccini, M., Fontanazza, G., Enhancement of frost tolerance in olive shoots in vitro by cold acclimation and sucrose increase in the culture medium (2001) Plant Cell, Tissue and Organ Culture, 67, pp. 299-302
  • Boyer, J.S., Plant productivity and environment (1982) Science, 218, pp. 443-448
  • D'Angeli, S., Altamura, M., Osmotin induces cold protection in olive trees by affecting programmed cell death and cytoskeleton organization (2007) Planta, 225, pp. 1147-1163
  • Eris, A., Gulen, H., Barut, E., Cansev, A., Annual patterns of total soluble sugars and proteins related to cold-hardiness in olive (Olea europaea L. 'Gemlik') (2007) The Journal of Horticultural Science and Biotechnology, 82, pp. 597-604
  • Evans, R.D., Black, R.A., Link, S.O., Rehydration-induced changes in pressure-volume relationships of Artemisia tridentutu Nutt. ssp. tridentutu (1990) Plant, Cell & Environment, 13, pp. 455-461
  • Fernández-Escobar, R., García-Novelo, J., Restrepo-Díaz, H., Mobilization of nitrogen in the olive bearing shoots after foliar application of urea (2011) Scientia Horticulturae, 127, pp. 452-454
  • Fiorino, P., Mancuso, S., Differential thermal analysis, supercooling and cell viability in organs of Olea europaea at subzero temperatures (2000) Advances in Horticultural Science, 14, pp. 23-27
  • George, M.F., Burke, M.J., Pellett, H.M., Johnson, A.G., Low temperature exotherms and woody plant distribution (1974) Horticultural Science, 9, pp. 519-522
  • Goldstein, G., Meinzer, F.C., Influence of insulation of dead leaves and low temperatures on water balance in an Andean giant rosette plant (1984) Plant, Cell & Environment, 6, pp. 649-656
  • Goldstein, G., Nobel, P.S., Changes in osmotic pressure and mucilage during low-temperature acclimation of Opuntia ficus-indica (1991) Plant Physiology, 97, pp. 954-961
  • Goldstein, G., Rada, F., Azocar, A., Cold hardiness and supercooling along an altitudinal gradient in Andean giant rosette species (1985) Oecologia, 68, pp. 147-152
  • Griffith, M., Brown, G., Cell wall deposits in winter rye Secale cereale L. 'Puma' during cold acclimation (1982) Botanical Gazette, 143, pp. 486-490
  • Gulen, H., Cansev, A., Eris, A., Cold hardiness of olive (Olea europaea L.) cultivars in cold-acclimated and non-acclimated stages: seasonal alteration of soluble sugars and phospholipids (2009) The Journal of Agricultural Science, 147, pp. 459-467
  • Gusta, L.V., Wisniewski, M., Understanding plant cold hardiness: an opinion (2013) Physiologia Plantarum, 147, pp. 4-14
  • Gusta, L.V., Wisniewski, M., Nesbitt, N.T., Gusta, M.L., The effect of water, sugars, and proteins on the pattern of ice nucleation and propagation in acclimated and non-acclimated canola leaves (2004) Plant Physiology, 135, pp. 1642-1653
  • Hong, S.G., Sucoff, E., Lee-Stadelmann, O., Effect of freezing deep supercooled water on the viability of ray cells (1980) Botanical Gazette, 141, pp. 464-468
  • Janská, A., Maršík, P., Zelenková, S., Ovesná, J., Cold stress and acclimation - what is important for metabolic adjustment? (2009) Plant Biology (Stuttgart, Germany), 12, pp. 395-405
  • Kasuga, J., Arakawa, K., Fujikawa, S., High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells (2007) The New Phytologist, 174, pp. 569-579
  • Koide, R.T., Robichaux, R.H., Morse, S.R., Smith, C.M., Plant water status, hydraulic resistance and capacitance. In Plant Physiological Ecology (1989), pp. 161-179. , (eds R.W. Pearcy, J. Ehleringer, H.A. Mooney & P.W. Rundel) - Chapman & Hall, London; Kosová, K., Vitámvás, P., Prásil, I.T., The role of dehydrins in plant response to cold (2007) Biol. Plant, 51, pp. 601-617
  • Kubacka-Zebalska, M., Kacperska, A., Low temperature-induced modifications of cell wall content and polysaccharide composition in leaves of winter oilseed rape (Brassica napus L. var. oleifera L.) (1999) Plant Science, 148, pp. 59-67
  • Larcher, W., Typology of freezing phenomena among vascular plants and evolutionary trends in frost acclimation (1982) Plant Cold Hardiness and Freezing Stress, pp. 417-426. , (eds A. Sakai & P.H. Li) - Academic Press, New York
  • Lavee, S., Involvement of plant growth regulators and endogenous growth substances in the control of alternate bearing (1989) Acta Horticulturae, 239, pp. 311-322
  • Levitt, J., (1980) Responses of Plants to Environmental Stresses, 1, pp. 67-344. , Chilling, freezing and high temperature stresses. (ed. J. Levitt), 2nd edn - Academic Press Inc, New York
  • Lipp, C.C., Goldstein, G., Meinzer, F.C., Niemczura, W., Freezing tolerance and avoidance in high-elevation Hawaiian plants (1994) Plant, Cell & Environment, 17, pp. 1035-1044
  • Melcher, P.J., Cordell, S., Jones, T.J., Scowcroft, P.G., Niemczura, F.T., Giambelluca, W., Goldstein, G., Supercooling capacity increases from sea level to tree line in the Hawaiian tree species Metrosideros polymorpha (2000) International Journal of Plant Sciences, 161, pp. 369-379
  • Miller, G.L., Miller, E.E., Determination of nitrogen in biological materials (1948) Annals of Chemistry, 20, pp. 481-488
  • Neuner, G., Frost resistance in alpine woody plants (2014) Frontiers in Plant Science, 5, p. 654
  • Neuner, G., Hacker, J., Ice formation and propagation in alpine plants (2011) Plants in Alpine Regions: Cell Physiology of Adaptation and Survival Strategies, pp. 163-174. , (ed. C. Lütz) - Springer, Wien
  • Nobel, P.S., (1991) Physicochemical and Environmental Plant Physiology, p. 635. , Academic Press, San Diego, California
  • Pearce, R.S., Plant freezing and damage (2001) Annals of Botany, 87, pp. 417-424
  • Quellet, F., Charron, J.B., Cold acclimation and freezing tolerance in plants. In eLS (2013), John Wiley & Sons, Ltd, Chichester; Rada, F., Goldstein, G., Azoear, A., Meinzer, F., Daily and seasonal osmotic changes in a tropical treeline species (1985) Journal of Experimental Botany, 36, pp. 987-1000
  • Rada, F., Goldstein, G., Azocar, A., Torres, F., Supercooling along an altitudinal gradient in Espeletia schultzii, a caulescent giant rosette species (1986) Journal of Experimental Botany, 38, pp. 491-497
  • Rejskova, A., Patkova, L., Stodulkova, E., Lipavska, H., The effect of abiotic stresses on carbohydrate status of olive shoots (Olea europaea L.) under in vitro conditions (2005) Journal of Plant Physiology, 164, pp. 174-184
  • Reyes-Diaz, M., Ulloa, N., Zuñiga-Feest, A., Gutiérrez, A., Gidekel, M., Alberdi, M., Bravo, L., Arabidopsis thaliana avoids freezing by supercooling (2006) Journal of Experimental Botany, 57, pp. 3687-3696
  • Sakai, A., Freezing avoidance mechanism of primordial shoots of conifer buds (1979) Plant & Cell Physiology, 20, pp. 1381-1390
  • Sakai, A., Larcher, W., Frost survival of plants. Responses and adaptation to freezing stress (1987) Ecological Studies, 62, pp. 1-321
  • Scarth, G.W., Levitt, J., The frost hardening mechanism of plant cells (1937) Plant Physiology, 12, pp. 51-78
  • Scholz, F.G., Bucci, S.J., Goldstein, G., Meinzer, F., Franco, A.C., Miralles-Wilhelm, F., Biophysical properties and functional significance of stem water storage tissues in Neotropical savanna trees (2007) Plant, Cell & Environment, 30, pp. 236-248
  • Scholz, F.G., Bucci, S.J., Arias, N.S., Meinzer, F.C., Goldstein, G., Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: coping with drought and subzero temperatures (2012) Oecologia, 170, pp. 885-897
  • Steponkus, P.L., Garber, M.P., Myers, S.P., Lineberger, R.D., Effects of cold acclimation and freezing on structure and function of chloroplast thylakoids (1977) Cryobiology, 14, pp. 303-321
  • Strauss, G., Hauser, H., Stabilization of lipid bilayer vesicles by sucrose during freezing (1986) Proceedings of the National Academy of Sciences of the United States of America, 83, pp. 2422-2426
  • Thomas, H., James, A.R., Freezing tolerance and solute changes in contrasting genotypes of Lolium perenne L. acclimated to cold and drought (1993) Annals of Botany, 72, pp. 249-254
  • Tyree, M.T., Cheung, Y.N., McGregor, M.E., Talbot, A.J., The characteristic of seasonal and ontogenic changes in the tissue-water relations of Acer, Populus, Tsuga and Picea (1978) Canadian Journal of Botany. Journal Canadien de Botanique, 56, pp. 635-647
  • Wanner, L.A., Junttila, O., Cold-induced freezing tolerant in Arabidopsis (1999) Plant Physiology, 120, pp. 391-399
  • Wilner, J., Relative and absolute electrolytic conductance tests for frost hardiness of apple varieties (1960) Canadian Journal of Plant Science. Revue Canadienne de Phytotechnie, 40, pp. 630-637
  • Wisniewski, M., Fuller, M., Palta, J., Carter, J., Gusta, L., Griffith, M., Duncan, J., Factors involved in ice nucleation and propagation in plants: an overview based on new insights gained from the use of infrared thermography (2001) Icelandic Agricultural Sciences, 14, pp. 41-47
  • Xin, Z., Browse, J., Cold comfort farm: the acclimation of plants to freezing temperatures (2000) Plant, Cell & Environment, 23, pp. 893-902
  • Yemm, E.W., Willis, A.J., The estimation of carbohydrates in plant extracts by Anthrone (1954) The Biochemical Journal, 57, pp. 508-514

Citas:

---------- APA ----------
Arias, N.S., Bucci, S.J., Scholz, F.G. & Goldstein, G. (2015) . Freezing avoidance by supercooling in Olea europaea cultivars: The role of apoplastic water, solute content and cell wall rigidity. Plant, Cell and Environment, 38(10), 2061-2070.
http://dx.doi.org/10.1111/pce.12529
---------- CHICAGO ----------
Arias, N.S., Bucci, S.J., Scholz, F.G., Goldstein, G. "Freezing avoidance by supercooling in Olea europaea cultivars: The role of apoplastic water, solute content and cell wall rigidity" . Plant, Cell and Environment 38, no. 10 (2015) : 2061-2070.
http://dx.doi.org/10.1111/pce.12529
---------- MLA ----------
Arias, N.S., Bucci, S.J., Scholz, F.G., Goldstein, G. "Freezing avoidance by supercooling in Olea europaea cultivars: The role of apoplastic water, solute content and cell wall rigidity" . Plant, Cell and Environment, vol. 38, no. 10, 2015, pp. 2061-2070.
http://dx.doi.org/10.1111/pce.12529
---------- VANCOUVER ----------
Arias, N.S., Bucci, S.J., Scholz, F.G., Goldstein, G. Freezing avoidance by supercooling in Olea europaea cultivars: The role of apoplastic water, solute content and cell wall rigidity. Plant Cell Environ. 2015;38(10):2061-2070.
http://dx.doi.org/10.1111/pce.12529