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 In nonsupercooling cells, ice formation is initiated in extracellular spaces and intracellular water is withdrawn to the extracellular ice crystals resulting from the presence of a vapor pressure gradient (Burke et al., 1976; Guy, 1990; Levitt, 1980; Ristic and Ashworth,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.
BecwarM.R.RajashekarC.BristowK.J.H.BurkeM.J.1981Deep undercooling of tissue water and winter hardiness limitations in timberline flora [Picea engelmannii, Abies lasiocarpa]Plant Physiol.68111114
BurkeM.J.StushnoffC.1979Frost hardiness: A discussion of possible molecular causes of injury with particular reference to deep supercooling of water199225MussellH.StaplesR.C.Stress physiology of crop plantsWileyNew York, NY
FujikawaS.KurodaK.OhtaniJ.1997Seasonal changes in dehydration tolerance of xylem ray parenchyma cells of Stylax obassia twigs that survive freezing temperatures by deep supercooling [Erratum: 1997;198:231]Protoplasma1973444
GrayG.R.ChauvinL.P.SarhanF.HunerN.1997Cold acclimation and freezing tolerance (a complex interaction of light and temperature)Plant Physiol.114467474
GuyC.L.NiemiK.J.FennellA.CarterJ.V.1986Survival of Cornus sericea L. stem cortical cells following immersion in liquid heliumPlant Cell Environ.9447450
KarlsonD.T.XiangQ.Y.StirmV.E.ShiraziA.M.AshworthE.N.2004Phylogenetic analyses in Cornus substantiate ancestry of xylem supercooling freezing behavior and reveal lineage of desiccation related proteinsPlant Physiol.13516541665
LiC.Y.JunttilaO.ErnstsenA.HeinoP.PalvaE.T.2003Photoperiodic control of growth, cold acclimation and dormancy development in silver birch (Betula pendula) ecotypesPhysiol. Plant.117206212
LiJ.H.ShoupS.ChenZ.D.2007Phylogenetic relationships of diploid species of Betula (Betulaceae) inferred from DNA sequences of nuclear nitrate reductaseSyst. Bot.32357365
LindenL.PalonenP.SeppanenM.1999Cold hardiness research on agricultural and horticultural crops in FinlandAgricultural and Food Science in Finland8459477
MaloneS.R.AshworthE.N.1991aFreezing stress response in woody tissues observed using low-temperature scanning electron microscopy and freeze substitution techniquesPlant Physiol.95871881
MaloneS.R.AshworthE.N.1991bFreezing stress response in woody tissues observed using low-temperature scanning electron microscopy and freeze substitution techniquesPlant Physiol.95871881
McKenzieJ.S.WeiserC.J.BurkeM.J.1974Effects of red and far red light on the initiation of cold acclimation in Cornus stolonifera MichxPlant Physiol.53783789
RasmussenD.H.MacKenzieA.P.1972Effect of solute on ice solution interfacial free energy; calculation from measured homogenous nucleation temperatures126145JellinekH.H.G.Water structure at the water–polymer interfacePlenum Publishing CoNew York, NY
RisticZ.AshworthE.N.1994Response of xylem ray parenchyma cells of red osier dogwood (Cornus sericea L.) to freezing stress. Microscopic evidence of protoplasm contractionPlant Physiol.104737746
VanHuysteeR.B.WeiserC.J.LiP.H.1967Cold acclimation in Cornus stolonifera under natural and controlled photoperiod and temperatureBot. Gaz.128200205
WellingA.MoritzT.PalvaE.T.JunttilaO.2002Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspenPlant Physiol.12916331641
WellingA.RinneP.Vihera-AarnioA.Kontunen-SoppelaS.HeinoP.PalvaE.T.2004Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.)J. Expt. Bot.55507516
WisniewskiM.1995Deep supercooling in woody plants and the role of cell wall structure163182LeeR.E.WarrenG.J.GustaL.V.Biological ice nucleation and its applicationsAPS PressSt. Paul, MN
WisniewskiM.AroraR.2000Structural and biochemical aspects of cold acclimation in woody plants419437JainS.M.MinochaS.C.Molecular biology of woody plantsKluwer AcademicDordrecht, The Netherlands
WisniewskiM.BassettC.GustaL.V.2003An overview of cold hardiness in Woody plants: Seeing the forest through the treesHortScience38952959
WisniewskiM.DavisG.1989Evidence for the involvement of a specific cell-wall layer in regulation of deep supercooling of xylem parenchymaPlant Physiol.91151156
WisniewskiM.DavisG.AroraR.1991aEffect of macerase, oxalic-acid, and EGTA on deep supercooling and pit membrane-structure of xylem parenchyma of peachPlant Physiol.9613541359
WisniewskiM.DavisG.SchafferK.1991bMediation of deep supercooling of peach and dogwood by enzymatic modifications in cell-wall structurePlanta184254260