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:

Freezing resistance through avoidance or tolerance of extracellular ice nucleation is important for plant survival in habitats with frequent subzero temperatures. However, the role of cell walls in leaf freezing resistance and the coordination between leaf and stem physiological processes under subzero temperatures are not well understood. We studied leaf and stem responses to freezing temperatures, leaf and stem supercooling, leaf bulk elastic modulus and stem xylem vessel size of six Patagonian shrub species from two sites (plateau and low elevation sites) with different elevation and minimum temperatures. Ice seeding was initiated in the stem and quickly spread to leaves, but two species from the plateau site had barriers against rapid spread of ice. Shrubs with xylem vessels smaller in diameter had greater stem supercooling capacity, i.e., ice nucleated at lower subzero temperatures. Only one species with the lowest ice nucleation temperature among all species studied exhibited freezing avoidance by substantial supercooling, while the rest were able to tolerate extracellular freezing from −11.3 to −20 °C. Leaves of species with more rigid cell walls (higher bulk elastic modulus) could survive freezing to lower subzero temperatures, suggesting that rigid cell walls potentially reduce the degree of physical injury to cell membranes during the extracellular freezing and/or thaw processes. In conclusion, our results reveal the temporal–spatial ice spreading pattern (from stem to leaves) in Patagonian shrubs, and indicate the role of xylem vessel size in determining supercooling capacity and the role of cell wall elasticity in determining leaf tolerance of extracellular ice formation. © The Author 2016. Published by Oxford University Press. All rights reserved.

Registro:

Documento: Artículo
Título:Freezing resistance in Patagonian woody shrubs: the role of cell wall elasticity and stem vessel size
Autor:Zhang, Y.-J.; Bucci, S.J.; Arias, N.S.; Scholz, F.G.; Hao, G.-Y.; Cao, K.-F.; Goldstein, G.
Filiación:Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, 666303, China
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, United States
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Grupo de Estudios Biofísicos y Eco-fisiológicos (GEBEF), Departamento de Biología, Universidad Nacional de la Patagonia San Juan Bosco, Comodoro Rivadavia, 9000, Argentina
Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110164, China
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Key Laboratory of Ministry of Education for Microbial and Plant Genetic Engineering, College of Forestry, Guangxi University, Nanning, Guangxi, 530004, China
Department of Biology, University of Miami, PO Box 249118, Coral Gables, FL 33124, United States
Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Nuñez, Buenos Aires, C1428EGA, Argentina
Palabras clave:Bulk elastic modulus; Ice nucleation temperature; Leaf lethal temperature; Patagonian steppe; Pressure–volume relationship; Supercooling.; cell; elastic modulus; freezing; nucleation; physiological response; shrub; steppe; supercooling; survival; woody plant; Atlantic Ocean; Patagonian Sea; cell wall; cold; metabolism; physiology; plant leaf; plant stem; Young modulus; Cell Wall; Cold Temperature; Elastic Modulus; Plant Leaves; Plant Stems
Año:2016
Volumen:36
Número:8
Página de inicio:1007
Página de fin:1018
DOI: http://dx.doi.org/10.1093/treephys/tpw036
Título revista:Tree Physiology
Título revista abreviado:Tree Physiol.
ISSN:0829318X
CODEN:TRPHE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0829318X_v36_n8_p1007_Zhang

Referencias:

  • Alonso-Amelot, M.E., High altitude plants, chemistry of acclimation and adaptation (2008) Studies in Natural Products Chemistry, 34, pp. 883-982. , Atta-ur-Rahman FRS (ed.) Elsevier, Oxford, UK
  • 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 (2015) Plant Cell Environ, 38, pp. 2061-2070
  • Azocar, A., Rada, F., Goldstein, G., Freezing tolerance in Draba chionophila, a ‘miniature’ caulescent rosette species (1988) Oecologia, 75, pp. 156-160
  • Arora, R., Wisniewski, M.E., Scorza, R., Cold acclimation in genetically related (Sibling) deciduous and evergreen peach (Prunus persica [L] Batsch) 1. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues (1992) Plant Physiol, 99, pp. 1562-1568
  • Ball, M.C., Wolfe, J., Canny, M., Hofmann, M., Nicotra, A.B., Hughes, D., Space and time dependence of temperature and freezing in evergreen leaves (2002) Funct Plant Biol, 29, pp. 1259-1272
  • Ball, M.C., Canny, M.J., Huang, C.X., Heady, R.D., Structural changes in acclimated and unacclimated leaves during freezing and thawing (2004) Funct Plant Biol, 31, pp. 29-40
  • Ball, M.C., Canny, M.J., Huang, C.X., Egerton, J.J.G., Wolfe, J., Freeze/thaw-induced embolism depends on nadir temperature: The heterogeneous hydration hypothesis (2006) Plant Cell Environ, 29, pp. 729-745
  • Bravo, L.A., Ulloa, N., Zuñiga, G.E., Casanova, A., Corcuera, L.J., Alberdi, M., Cold resistance in Antarctic angiosperms (2001) Physiol Plant, 111, pp. 55-65
  • Bucci, S.J., Scholz, F.G., Goldstein, G., Meinzer, F.C., Arce, M.E., Soil water availability and rooting depth as determinants of hydraulic architecture of Patagonian woody species (2009) Oecologia, 160, pp. 631-641
  • Bucci, S.J., Scholz, F.G., Peschiutta, M.L., Arias, N.S., Meinzer, F.C., Goldstein, G., The stem xylem of Patagonian shrubs operates far from the point of catastrophic dysfunction and is additionally protected from drought-induced embolism by leaves and roots (2013) Plant Cell Environ, 36, pp. 2163-2174
  • Cavender-Bares, J., Cortes, P., Rambal, S., Joffre, R., Miles, B., Rocheteau, A., Summer and winter sensitivity of leaves and xylem to minimum freezing temperatures: A comparison of co-occurring Mediterranean oaks that differ in leaf lifespan (2005) New Phytol, 168, pp. 597-612
  • Feild, T.S., Brodribb, T., Stem water transport and freeze-thaw xylem embolism in conifers and angiosperms in a Tasmanian treeline heath (2001) Oecologia, 127, pp. 314-320
  • Fuselli, S.R., Gende, L.B., García de la Rosa, S.B., Eguaras, M.J., Fritz, R., Inhibition of Paenibacillus larvae subsp. Larvae by the essential oils of two wild plants and their emulsifying agents (2005) Span J Agric Res, 3, pp. 220-224
  • George, M.F., Burke, M.J., Pellett, H.M., Johnson, A.G., Low temperature exotherms and woody plant distribution (1974) HortScience, 9, pp. 519-522
  • Goldstein, G., Meinzer, F., Influence of insulating dead leaves and low temperatures on water balance in an Andean giant rosette plant (1983) Plant Cell Environ, 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 Physiol, 97, pp. 954-961
  • Goldstein, G., Nobel, P.S., Water relations and low-temperature acclimation for cactus species varying in freezing tolerance (1994) Plant Physiol, 104, pp. 675-681
  • Goldstein, G., Rada, F., Zaocar, A., Cold hardiness and supercooling along an altitudinal gradient in Andean giant rosette species (1985) Oecologia, 68, pp. 147-152
  • Griffith, M., Antikienen, M., Extracellular ice formation in freezing-tolerant plants (1996) Adv Low Temp Biol, 3, pp. 107-139
  • Hacker, J., Neuner, G., Ice propagation in plants visualized at the tissue level by infrared differential thermal analysis (IDTA) (2007) Tree Physiol, 27, pp. 1661-1670
  • Iljin, W.S., Uber den Kaltetod der Pflanzen und seine Ursachen (1933) Protoplasma, 20, pp. 105-124
  • 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 Sci, 148, pp. 59-67
  • Kubiske, M.E., Abrams, M.D., Seasonal, diurnal and rehydration-induced variation of pressure-volume relationships in Pseudotsuga menziesii (1991) Physiol Plant, 83, pp. 107-116
  • Larcher, W., Typology of freezing phenomena among vascular plants and evolutionary trends in frost acclimation (1982) Plant Cold Hardiness and Freezing Stress: Mechanisms and Crop Implications, pp. 417-426. , Li Sakai A (eds) Academic Press, New York, NY
  • Lenné, T., Bryant, G., Hocart, C.H., Huang, C.X., Ball, M.C., Freeze avoidance: A dehydrating moss gathers no ice (2010) Plant Cell Environ, 33, pp. 1731-1741
  • Levitt, J., (1972) Responses of Plants to Environmental Stresses, , Academic Press, New York, NY
  • Lipp, C.C., Goldstein, G., Meinzer, F.C., Niemczura, W., Freezing tolerance and avoidance in high-elevation Hawaiian plants (1994) Plant Cell Environ, 17, pp. 1035-1044
  • McCully, M.E., Canny, M.J., Huang, C.X., The management of extracellular ice by petioles of frost-resistant herbaceous plants (2004) Ann Bot, 94, pp. 665-674
  • Meinzer, F.C., Moore, P.H., Effect of apoplastic solutes on water potential in elongating sugarcane leaves (1988) Plant Physiol, 86, pp. 873-879
  • Melcher, P.J., Cordell, S., Jones, T.J., Scowcroft, P.G., Niemczura, W., Giambelluca, T.W., Goldstein, G., Supercooling capacity increases from sea level to tree line in the Hawaiian tree species Metrosideros polymorpha (2000) Int J Plant Sci, 161, pp. 369-379
  • Murai, M., Yoshida, S., Evidence for the cell wall involvement in temporal changes in freezing tolerance of Jerusalem artichoke (Heli-anthus tuberosus L.) tubers during cold acclimation (1998) Plant Cell Physiol, 39, pp. 97-105
  • Neuner, G., Bannister, P., Larcher, W., Ice formation and foliar frost resistance in attached and excised shoots from seedlings and adult trees of Nothofagus menziesii (1997) N Z J Bot, 35, pp. 221-227
  • Pearce, R.S., Plant freezing and damage (2001) Ann Bot, 87, pp. 417-424
  • Rada, F., Goldstein, G., Azocar, A., Torres, F., Supercooling along an altitudinal gradient in Espeletia schultzii, a caulescent giant rosette species (1987) J Exp Bot, 38, pp. 491-497
  • Rada, F., García-Núñez, C., Boero, C., Gallardo, M., Hilal, M., González, J., Prado, F., Azócar, A., Low-temperature resistance in Polylepis tarapacana, a tree growing at the highest altitudes in the world (2001) Plant Cell Environ, 24, pp. 377-381
  • Rajashekar, C., Gusta, L.V., Burke, M.J., Membrane structural transitions: Probable relation to frost damage in hardy herbaceous species (1979) Low Temperature Stress in Crop Plants: The Role of The Membrane, pp. 255-274. , Lyons JM, Graham D, Raison JK (eds) Academic Press, New York, NY
  • Rajashekar, C.B., Lafta, A., Cell-wall changes and cell tension in response to cold acclimation and exogenous abscisic acid in leaves and cell cultures (1996) Plant Physiol, 111, pp. 605-612
  • Renaut, J., Lutts, S., Hoffmann, L., Hausman, J.-F., Responses of poplar to chilling temperatures: Proteomic and physiological aspects (2004) Plant Biol, 6, pp. 81-90
  • Roden, J.S., Canny, M.J., Huang, C.X., Ball, M.C., Frost tolerance and ice formation in Pinus radiata needles: Ice management by the endoder-mis and transfusion tissues (2009) Funct Plant Biol, 36, pp. 180-189
  • Saito, T., Soga, K., Hoson, T., Terashima, I., The bulk elastic modulus and the reversible properties of cell walls in developing Quercus leaves (2006) Plant Cell Physiol, 47, pp. 715-725
  • Sakai, A., Larcher, W., Frost survival of plants. Responses and adaptation to freezing stress (1987) Ecol Stud, 62, pp. 1-321
  • Sakai, A., Paton, D.M., Wardle, P., Freezing resistance of trees of the south temperate zone, especially subalpine species of Australasia (1981) Ecology, 62, pp. 563-570
  • Scholander, P.F., Hammel, H.T., Bradstreet, E.D., Hemmington, E.A., Sap pressure in vascular plants (1965) Science, 148, pp. 339-346
  • Scholz, F.G., Bucci, S.J., Arias, N., 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
  • Sierra-Almeida, A., Cavieres, L.A., Summer freezing resistance decreased in high-elevation plants exposed to experimental warming in the central Chilean Andes (2010) Oecologia, 163, pp. 267-276
  • Sierra-Almeida, A., Cavieres, L.A., Bravo, L.A., Freezing resistance varies within the growing season and with elevation in high-Andean species of central Chile (2009) New Phytol, 182, pp. 461-469
  • Siminovitch, D., Scarth, G.W., A study of the mechanism of frost injury to plants (1938) Can J Res, 16 c, pp. 467-481
  • Siminovitch, D., Singh, J., Keller, W.A., de la Roche, I.A., Freezing and osmotic dehydration of winter rye cell protoplasts (1976) Cryobiology, 13, p. 670
  • Singh, J., Freezing of protoplasts isolated from cold-hardened and non-hardened winter rye (1979) Plant Sci Lett, 16, pp. 195-201
  • Smallwood, M., Bowles, D.J., Plants in a cold climate (2002) Philos Trans R Soc B, 357, pp. 831-847
  • Soriano, A., Los Distritos Florísticos de la Provincia Patagónica (1956) Rev Invest Agropecuarias, 10, pp. 323-347
  • Squeo, F.A., Rada, F., Azocar, A., Goldstein, G., Freezing tolerance and avoidance in high tropical Andean plants: Is it equally represented in species with different plant height? (1991) Oecologia, 86, pp. 378-382
  • Stefanowska, M., Kuras, M., Kubacka-Zebalska, M., Kacperska, A., Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. Oleifera L.) (1999) Ann Bot, 84, pp. 313-319
  • Stuart, S.A., Choat, B., Martin, K.C., Holbrook, N.M., Ball, M.C., The role of freezing in setting the latitudinal limits of mangrove forests (2007) New Phytol, 173, pp. 576-583
  • Tao, D., Li, P.H., Carter, J.V., Role of cell wall in freezing tolerance of cultured potato cells and their protoplasts (1983) Physiol Plant, 58, pp. 527-532
  • Tyree, M.T., Hammel, H.T., The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique (1972) J Exp Bot, 23, pp. 267-282
  • Tyree, M.T., Cheung, Y.N.S., MacGregor, M.E., Talbot, A.J.B., The characteristics of seasonal and ontogenetic changes in the tissue – Water relations of Acer, Populus, Tsuga, and Picea (1978) Can J Bot, 56, pp. 635-647
  • Wilner, J., Relative and absolute electrolytic conductance tests for frost hardiness of apple varieties (1960) Can J Plant Sci, 40, pp. 630-637
  • Wilson, P.W., Heneghan, A.F., Haymet, A.D.J., Ice nucleation in nature: Supercooling point (SCP) measurements and the role of heterogeneous nucleation (2003) Cryobiology, 46, pp. 88-98
  • Wisniewski, M., Fuller, M., Ice nucleation and deep supercooling in plants: New insights using infrared thermography (1999) Cold-Adapted Organisms—Ecology, Physiology, Enzy-Mology and Molecular Biology, pp. 105-118. , Margesin R, Schinner F (eds) Springer, Berlin
  • Wisniewski, M., Davis, G., Arora, R., Effect of macerase, oxalic acid, and EGTA on deep supercooling and pit membrane structure of xylem parenchyma of peach (1991) Plant Physiol, 96, pp. 1354-1359
  • Wisniewski, M., Lindow, S.E., Ashworth, E.N., Observations of ice nucleation and propagation in plants using infrared video thermography (1997) Plant Physiol, 113, pp. 327-334
  • Woodward, F.I., (1987) Climate and Plant Distribution, , Cambridge University Press, Cambridge
  • Yamada, T., Kuroda, K., Jitsuyama, Y., Takezawa, K., Arakawa, K., Fujikawa, S., Roles of the plasma membrane and the cell wall in the responses of plant cells to freezing (2002) Planta, 215, pp. 770-778
  • Zhang, Y.-J., Holbrook, N.M., Cao, K.-F., Seasonal dynamics in photosynthesis of woody plants at the northern limit of Asian tropics: Potential role of fog in maintaining tropical rainforests and agriculture in Southwest China (2014) Tree Physiol, 34, pp. 1069-1078

Citas:

---------- APA ----------
Zhang, Y.-J., Bucci, S.J., Arias, N.S., Scholz, F.G., Hao, G.-Y., Cao, K.-F. & Goldstein, G. (2016) . Freezing resistance in Patagonian woody shrubs: the role of cell wall elasticity and stem vessel size. Tree Physiology, 36(8), 1007-1018.
http://dx.doi.org/10.1093/treephys/tpw036
---------- CHICAGO ----------
Zhang, Y.-J., Bucci, S.J., Arias, N.S., Scholz, F.G., Hao, G.-Y., Cao, K.-F., et al. "Freezing resistance in Patagonian woody shrubs: the role of cell wall elasticity and stem vessel size" . Tree Physiology 36, no. 8 (2016) : 1007-1018.
http://dx.doi.org/10.1093/treephys/tpw036
---------- MLA ----------
Zhang, Y.-J., Bucci, S.J., Arias, N.S., Scholz, F.G., Hao, G.-Y., Cao, K.-F., et al. "Freezing resistance in Patagonian woody shrubs: the role of cell wall elasticity and stem vessel size" . Tree Physiology, vol. 36, no. 8, 2016, pp. 1007-1018.
http://dx.doi.org/10.1093/treephys/tpw036
---------- VANCOUVER ----------
Zhang, Y.-J., Bucci, S.J., Arias, N.S., Scholz, F.G., Hao, G.-Y., Cao, K.-F., et al. Freezing resistance in Patagonian woody shrubs: the role of cell wall elasticity and stem vessel size. Tree Physiol. 2016;36(8):1007-1018.
http://dx.doi.org/10.1093/treephys/tpw036