In nature, temperature acts as a selective pressure for plant growth and has limited the geographical distribution of many species (Becwar et al., 1981; George et al., 1974; Gray et al., 1997; Gusta et al., 1983; Linden et al., 1999; Sakai and Weiser, 1973; Smithberg and Weiser, 1968; Thomashow, 1999). In response to varying seasonal temperatures within temperate climates, plants have evolved the ability to survive when exposed to subzero temperatures through a process known as cold acclimation. In temperate woody plants, a first stage of cold acclimation is typically triggered in response to the seasonal decrease in day length (Fuchigami et al., 1971; Howell and Weiser, 1970; Hurst et al., 1967; Irving and Lanphear, 1967; Malone and Ashworth, 1991b; McKenzie et al., 1974; VanHuystee et al., 1967; Weiser, 1970). A second stage of cold acclimation triggered by exposure to low temperature was initially documented in Cornus sericea (VanHuystee et al., 1967; Weiser, 1970) and is recognized to occur in many freeze-tolerant temperate woody plants (Li et al., 2003; Welling et al., 2002, 2004; Wisniewski et al., 2003).
Woody plants evolved two freezing responses for surviving prolonged exposure to subzero temperatures: freeze tolerance (nonsupercooling) and freezing avoidance (deep supercooling) (Burke et al., 1976; George et al., 1982). In nonsupercooling cells, ice formation is initiated in extracellular spaces and intracellular water is withdrawn to the extracellular ice crystals resulting from the presence of a vapor pressure gradient (Burke et al., 1976; Guy, 1990; Levitt, 1980; Ristic and Ashworth, 1994). Thus, nonsupercooling cells are exposed to freeze-induced dehydration and tolerant species are capable of surviving this stress in a cold-acclimated state (Ashworth et al., 1993; Fujikawa et al., 1997; Wisniewski and Arora, 2000; Wisniewski et al., 2003).
Deep supercooling is the second freezing response that is characterized by the ability of woody plants to resist the formation of intracellular ice below subzero temperatures. However, in contrast to nonsupercooling cells, hardiness or survival is typically limited to the homogenous ice nucleation temperature (–40 °C) of water (Rasmussen and MacKenzie, 1972). As a result of this inherent limitation of deep supercooling, the geographical distribution of woody plants has been extensively studied in relation to freezing response (Becwar et al., 1981; George et al., 1974; Sakai and Weiser, 1973; Smithberg and Weiser, 1968).
In general, deep supercooling plants are restricted in geographical range to areas that do not fall below –40 °C (George et al., 1974). Because this temperature coincides with the homogenous nucleation temperature of water, plant species exhibiting deep supercooling are limited in their ability to survive temperatures below –40 °C, although exceptions to this restraint have been documented (Gusta et al., 1983). At this temperature, the spontaneous nucleation of intracellular supercooled water can occur, resulting in cellular death (Burke et al., 1976). In contrast, no discrete lower temperature limit exists for the survival of freeze-tolerant, nonsupercooling woody plants. Instead, the ability of nonsupercooling woody plants to survive winter is primarily limited by their capacity to withstand the intracellular dehydration that is induced by formation of extracellular ice crystals at low temperatures (Ashworth et al., 1993; Burke et al., 1976; Fujikawa et al., 1997). Thus, the geographical ranges of nonsupercooling species may extend to northernmost regions with annual temperatures that are substantially colder than the –40 °C isotherm (George et al., 1974). In the Cornus genus, C. florida and C. sericea differ in their xylem freezing response and highlight differences in geographical range that are based on their mechanisms of cold-hardiness (Karlson et al., 2004). Although the northern distribution of C. florida is limited to regions warmer than –40 °C, C. sericea is unrestricted in its northernly distribution. Under controlled conditions, C. sericea has been shown to exhibit extreme freeze tolerance and can survive exposure in liquid helium (Guy et al., 1986). Geographical distribution of other species linked to freezing response has also been documented (George et al., 1974).
A previous interspecific study within Cornus (dogwoods) investigated xylem freezing response and determined that the majority of Cornus species exhibit deep supercooling (Karlson et al., 2004). In that study, a phylogenetic analysis of Cornus indicated that nonsupercooling (freezing tolerance) arose in the most recently divergent group of dogwoods as a late evolutionary event and this may have facilitated the expansion of no-supercooling species into northern ranges (Karlson et al., 2004). Because similar interspecific studies are lacking in other woody species, the purpose of this study was to characterize the freezing response in a range of species within two temperate woody genera. By determining the freezing response of Betula and Acer species, we have demonstrated that the majority of Betula species are nonsupercooling, whereas Acer species are predominantly supercooling. From this current study, these data from two additional woody plant genera add support to the previously established hypothesis that xylem supercooling freezing response is an ancestral trait (Karlson et al., 2004) in multiple temperate woody genera.
Becwar, M.R., Rajashekar, C., Bristow, K.J.H. & Burke, M.J. 1981 Deep undercooling of tissue water and winter hardiness limitations in timberline flora [Picea engelmannii, Abies lasiocarpa] Plant Physiol. 68 111 114
Burke, M.J. & Stushnoff, C. 1979 Frost hardiness: A discussion of possible molecular causes of injury with particular reference to deep supercooling of water 199 225 Mussell H. & Staples R.C. Stress physiology of crop plants Wiley New York, NY
Fujikawa, S., Kuroda, K. & Ohtani, J. 1997 Seasonal changes in dehydration tolerance of xylem ray parenchyma cells of Stylax obassia twigs that survive freezing temperatures by deep supercooling [Erratum: 1997;198:231] Protoplasma 197 34 44
George, M.F., Becwar, M.R. & Burke, M.J. 1982 Freezing avoidance by deep undercooling of tissue water in winter-hardy plants Cryobiology 19 628 639
George, M.F., Burke, M.J., Pellet, H.M. & Johnson, A.G. 1974 Low temperature exotherms and woody plant distribution HortScience 9 519 522
Gray, G.R., Chauvin, L.P., Sarhan, F. & Huner, N. 1997 Cold acclimation and freezing tolerance (a complex interaction of light and temperature) Plant Physiol. 114 467 474
Gusta, L.V., Tyler, N.J. & Chen, T. 1983 Deep undercooling in woody taxa growing north of the –40 °C isotherm Plant Physiol. 72 122 128
Guy, C.L. 1990 Cold acclimation and freezing stress tolerance: Role of protein metabolism Annu. Rev. Plant Physiol. Plant Mol. Biol. 41 187 223
Guy, C.L., Niemi, K.J., Fennell, A. & Carter, J.V. 1986 Survival of Cornus sericea L. stem cortical cells following immersion in liquid helium Plant Cell Environ. 9 447 450
Hurst, C., Hall, T.C. & Weiser, C.J. 1967 Reception of the light stimulus for cold acclimation in Cornus stolonifera Michx HortScience 2 164 166
Karlson, D.T., Xiang, Q.Y., Stirm, V.E., Shirazi, A.M. & Ashworth, E.N. 2004 Phylogenetic analyses in Cornus substantiate ancestry of xylem supercooling freezing behavior and reveal lineage of desiccation related proteins Plant Physiol. 135 1654 1665
Levitt, J. 1980 Responses of plants to environmental stresses Chilling, freezing, and high temperature stresses Vol. 1 Academic Press New York, NY
Li, C.Y., Junttila, O., Ernstsen, A., Heino, P. & Palva, E.T. 2003 Photoperiodic control of growth, cold acclimation and dormancy development in silver birch (Betula pendula) ecotypes Physiol. Plant. 117 206 212
Li, J.H., Shoup, S. & Chen, Z.D. 2007 Phylogenetic relationships of diploid species of Betula (Betulaceae) inferred from DNA sequences of nuclear nitrate reductase Syst. Bot. 32 357 365
Linden, L., Palonen, P. & Seppanen, M. 1999 Cold hardiness research on agricultural and horticultural crops in Finland Agricultural and Food Science in Finland 8 459 477
Malone, S.R. & Ashworth, E.N. 1991a Freezing stress response in woody tissues observed using low-temperature scanning electron microscopy and freeze substitution techniques Plant Physiol. 95 871 881
Malone, S.R. & Ashworth, E.N. 1991b Freezing stress response in woody tissues observed using low-temperature scanning electron microscopy and freeze substitution techniques Plant Physiol. 95 871 881
McKenzie, J.S., Weiser, C.J. & Burke, M.J. 1974 Effects of red and far red light on the initiation of cold acclimation in Cornus stolonifera Michx Plant Physiol. 53 783 789
Rasmussen, D.H. & MacKenzie, A.P. 1972 Effect of solute on ice solution interfacial free energy; calculation from measured homogenous nucleation temperatures 126 145 Jellinek H.H.G. Water structure at the water–polymer interface Plenum Publishing Co New York, NY
Ristic, Z. & Ashworth, E.N. 1994 Response of xylem ray parenchyma cells of red osier dogwood (Cornus sericea L.) to freezing stress. Microscopic evidence of protoplasm contraction Plant Physiol. 104 737 746
Thomashow, M.F. 1999 Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 571 599
VanHuystee, R.B., Weiser, C.J. & Li, P.H. 1967 Cold acclimation in Cornus stolonifera under natural and controlled photoperiod and temperature Bot. Gaz. 128 200 205
Welling, A., Moritz, T., Palva, E.T. & Junttila, O. 2002 Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen Plant Physiol. 129 1633 1641
Welling, A., Rinne, P., Vihera-Aarnio, A., Kontunen-Soppela, S., Heino, P. & Palva, E.T. 2004 Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.) J. Expt. Bot. 55 507 516
Wisniewski, M. 1995 Deep supercooling in woody plants and the role of cell wall structure 163 182 Lee R.E., Warren G.J. & Gusta L.V. Biological ice nucleation and its applications APS Press St. Paul, MN
Wisniewski, M. & Arora, R. 2000 Structural and biochemical aspects of cold acclimation in woody plants 419 437 Jain S.M. & Minocha S.C. Molecular biology of woody plants Kluwer Academic Dordrecht, The Netherlands
Wisniewski, M., Bassett, C. & Gusta, L.V. 2003 An overview of cold hardiness in Woody plants: Seeing the forest through the trees HortScience 38 952 959
Wisniewski, M. & Davis, G. 1989 Evidence for the involvement of a specific cell-wall layer in regulation of deep supercooling of xylem parenchyma Plant Physiol. 91 151 156
Wisniewski, M., Davis, G. & Arora, R. 1991a Effect of macerase, oxalic-acid, and EGTA on deep supercooling and pit membrane-structure of xylem parenchyma of peach Plant Physiol. 96 1354 1359
Wisniewski, M., Davis, G. & Schaffer, K. 1991b Mediation of deep supercooling of peach and dogwood by enzymatic modifications in cell-wall structure Planta 184 254 260