Skip to main content

Advertisement

Log in

Environmental regulation and physiological basis of freezing tolerance in woody plants

  • Mini Review
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Cold acclimation of plants is a complex process involving a number of biochemical and physiological changes. The ability to cold acclimate is under genetic control. The development of freezing tolerance in woody plants is generally triggered by non-freezing low temperatures but can also be induced by mild drought or exogenous abscisic acid, as well as by short photoperiod. In nature, the extreme freezing tolerance of woody plants is achieved during sequential stages of cold acclimation the first of which is initiated by short photoperiods and non-freezing low temperatures, and the second by freezing temperatures. Although recent breakthroughs have increased our knowledge on the physiological molecular basis of freezing tolerance in herbaceous species, which acclimate primarily in response to non-freezing low temperatures, very little is known about cold acclimation of woody plants. This article attempts to review our current understanding of the physiological aspects that underline cold acclimation in woody plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aitken S.N., Hannerz M. 2001. Genecology and gene resource management strategies for conifer cold hardiness. In: Conifer Cold Hardiness, Bigras F.J., Colombo S.J. (Eds), Kluwer Academic Press, Dordrecht, pp. 23–54.

    Google Scholar 

  • Anisko T., Lindstrom O.M. 1996. Cold hardiness and water relations parameters in Rhododendron cv. Catawbiense Boursault subjected to drought episodes. Physiol. Plant. 98: 147–155.

    Article  CAS  Google Scholar 

  • Antikainen M., Griffith M. 1997. Antifreeze protein accumulation in freezing-tolerant cereals. Physiol. Plant. 99: 423–432.

    Article  CAS  Google Scholar 

  • Arora R., Rowland L.J., Panta G.R. 1997. Chill-responsive dehydrins in blueberry: Are they associated with cold hardiness or dormancy transitions? Physiol. Plant. 101: 8–16.

    Article  CAS  Google Scholar 

  • Arora R., Wisniewski M., Rowland L.J. 1996. Cold acclimation and alterations in dehydrin-like and bark storage proteins in the leaves of sibling deciduous and evergreen peach. J. Amer. Soc. Hortic. Sci. 121: 915–919.

    CAS  Google Scholar 

  • Arora R., Wisniewski M.E., Scorza R. 1992. Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica L. Batsch). I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues. Plant Physiol. 99: 1562–1568.

    PubMed  CAS  Google Scholar 

  • Artlip T.S., Callahan A.M., Basset, C.L., Wisniewski M.E. 1997. Seasonal expression of a dehydrin gene in sibling deciduous and evergreen genotypes of peach (Prunus persica [L.] Batsch). Plant Mol. Biol. 33: 61–70.

    Article  PubMed  CAS  Google Scholar 

  • Ashworth E.N., Wisniewski M.E. 1991. Response of fruit tree tissues to freezing temperatures. HortScience 26: 501–504.

    Google Scholar 

  • Baldwin B.D., Bandara M.S., Tanino K.K. 1998. Is tissue culture a viable system with which to examine environmental and hormonal regulation of cold acclimation in woody plants? Physiol. Plant. 102: 201–209.

    Article  CAS  Google Scholar 

  • Browse J., Xin Z.G. 2001. Temperature sensing and cold acclimation. Curr. Opin. Plant Biol. 4: 241–246.

    Article  PubMed  CAS  Google Scholar 

  • Campbell S.A., Close T.J. 1997. Dehydrins: genes, proteins and associations with phenotypic traits. New Phytol. 137: 61–74.

    Article  CAS  Google Scholar 

  • Chen H.H., Li P.H. 1978. Interaction of low temperature, water stress, and short days in the induction of stem frost hardiness in red osier dogwood. Plant Physiol. 62: 833–835.

    PubMed  Google Scholar 

  • Chen H.H., Li P.H., Brenner M.L. 1983. Involvement of abscicis acid in potato cold acclimation. Plant Physiol. 71: 362–365.

    PubMed  CAS  Google Scholar 

  • Chen P.M., Li P.H. 1977. Induction of frost hardiness in stem cortical tissues of Cornus stolonifera Michx. by water stress. II. Biochemical changes. Plant Physiol. 59: 240–243.

    PubMed  CAS  Google Scholar 

  • Chen T.H.H., Gusta L.V. 1983. Abscisic acid-induced freezing tolerance resistance in cultured plant cells. Plant Physiol. 73: 71–75.

    PubMed  CAS  Google Scholar 

  • Close T.J. 1996. Dehydrins: Emergence of a biochemical role of a family of plant dehydration proteins. Physiol. Plant. 97: 795–803.

    Article  CAS  Google Scholar 

  • Close T.J. 1997. Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Physiol. Plant. 100: 291–296.

    Article  CAS  Google Scholar 

  • Daie J., Campbell W.F. 1981. Response of tomato plants to stressful temperatures. Plant Physiol. 67: 26–29.

    PubMed  CAS  Google Scholar 

  • Gilmour S.J., Thomashow M.F. 1991. Cold acclimation and cold regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol. Biol. 17: 1233–1240.

    Article  PubMed  CAS  Google Scholar 

  • Greer D.H., Robinson L.A., Hall A.J., Klages K., Donnison H. 2000. Frost hardening of Pinus radiata seedings: effects of temperature on relative growth rate, carbon balance and carbohydrate concentration. Tree Physiol. 20: 107–114.

    PubMed  CAS  Google Scholar 

  • Guy C.L. 1990. Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41: 187–223.

    CAS  Google Scholar 

  • Guy C.L., Haskell D. 1988. Detection of polypeptides associated with the cold acclimation process in spinach. Electrophoresis 9: 787–796.

    Article  PubMed  CAS  Google Scholar 

  • Heino P., Sandman G., L ng V., Nordin K., Palva E.T. 1990. Abscisic acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Theor. Appl. Genet. 79: 801–806.

    Article  CAS  Google Scholar 

  • Hiilovaara-Teijo M., Palva E.T. 1999. Molecular responses in cold-adapted plants. In: Cold-Adapted Organisms: Ecology, Physiology, Enzymology and Molecular Biology, Margesin R., Schinner F. (Eds), Spring-Verlag, Berlin Heidelberg, pp.349–384.

    Google Scholar 

  • Hinesley L.E., Pharr D.M., Snelling L.K., Funderburk S.R. 1992. Foliar raffinose and sucrose in four conifer species: relationship to seasonal temperature. J. Amer. Soc. Hortic. Sci. 117: 852–855.

    CAS  Google Scholar 

  • Howe G.T., Hackett W.P., Furnier G.R., Klevorn R.E. 1995. Photoperiodic responses of a northern and southern ecotype of black cottonwood. Physiol. Plant. 93: 695–708.

    Article  CAS  Google Scholar 

  • Hughes M.A., Dunn, M.A. 1996. The molecular biology of plant acclimation to low temperature. J. Exp. Bot. 47: 291–305.

    Article  CAS  Google Scholar 

  • Hurme P., Repo T., Savolainen O., Pääkkönen T. 1997. Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris L.). Can. J. For. Res. 27: 716–723.

    Article  Google Scholar 

  • Irving R.M. 1968. Regulation of cold hardiness in Acer negundo. Plant Physiol. 43: 9–13.

    PubMed  CAS  Google Scholar 

  • Irving R.M. 1969. Characterization and role of an endogenous inhibitor in the induction of cold hardiness in Acer negundo. Plant Physiol. 44: 801–805.

    PubMed  CAS  Google Scholar 

  • Irving R.M., Lanphear F.O. 1967. Environmental control of cold hardiness in woody plants. Plant Physiol. 42: 1191–1196.

    Article  PubMed  Google Scholar 

  • Ismail A.M., Hall A.E., Close T.J. 1999. Purification and partial characterization of a dehydrin involved in chilling tolerance during seedling emergence of cowpea. Plant Physiol. 120: 237–244.

    Article  PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen K.R., Gilmour S.J., Zarka D.G., Schabenberger O., Thomashow M.F. 1998. Arabidopsis CBF1 overexpression induces cor genes and enhances freezing tolerance. Science 280: 104–106.

    Article  PubMed  CAS  Google Scholar 

  • Junttila O. 1982. The cessation of apical growth in latitudinal ecotypes and ecotype crosses of Salix pentandra L. J. Exp. Bot. 33: 1021–1029.

    Article  Google Scholar 

  • Junttila O., Kaurin . 1990. Environmental control of cold acclimation in Salix pentandra. Scand. J. For. Res. 5: 195–204.

    Google Scholar 

  • Junttila O., Welling A., Li C., Tsegay B.A., Palva E.T. 2002. Physiological aspects of cold hardiness in northern deciduous tree species. In: Plant Cold Hardiness, Li P., Palva E.T. (Eds), Kluwer Academic/Plenum Publishers, pp.65-76.

  • Kacperska A. 1989. Metabolic consequences of low temperature stress in chilling-insensitive plants. In: Low Temperature Stress Physiology in Crops, Li P.H. (Ed), CRC Press, Boca Raton, Florida, pp. 27–40.

    Google Scholar 

  • Kacperska A. 1993. Water potential alterations — a prerequisite or a triggering stimulus for the development of freezing tolerance in overwintering herbaceous plants. In: Advances in plant cold hardiness, Li P.H., Christersson L. (Eds), CRC Press, Boca Raton, Florida, USA, pp.73–91.

    Google Scholar 

  • Karlson D.T., Zeng Y., Stirm V.E., Joly R.J., Ashworth E.N. 2003. Photoperiod regulation of a 24-KD dehydrin-like protein in red-osier dogwood (Cornus sericea L.) in relation to freeze-tolerance. Plant Cell Physiol. 44: 25–34.

    Article  PubMed  CAS  Google Scholar 

  • Kaurin, Junttila O., Hansen J. 1981. Seasonal changes in frost hardiness in cloud berry (Rubus chamaemorus) in relation to carbohydrate content with special reference to sucrose. Physiol. Plant. 52: 310–314.

    Article  CAS  Google Scholar 

  • Kontunen-Soppela S., Laine K. 2001. Seasonal fluctuations of dehydrins is related to osmotic status in Scots ping seedlings. Trees 15: 425–430.

    CAS  Google Scholar 

  • Koornneef M., Reuling G., Karssen C.M. 1984. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol. Plant. 61: 377–383.

    Article  CAS  Google Scholar 

  • Kuroda H., Sagisaka S. 1993. Ultrastructural changes in cortical cell of apple (Malus pumila Mill.) associated with cold hardiness. Plant Cell Physiol. 34: 357–365.

    Google Scholar 

  • Lalk I., Dörffling K. 1985. Hardening, abscisic acid, proline and freezing resistance in two winter wheat varieties. Physiol. Plant. 63: 287–292.

    Article  CAS  Google Scholar 

  • Lng V., Heino P., Palva E.T. 1989. Low temperature acclimation and treatment with exogenous abscisic acid induce common polypeptides in Arabidopsis thaliana (L) Heynh. Theor. Appl. Genet. 77: 729–734.

    Google Scholar 

  • Lng V., Mantyla E., Welin B., Sundberg B., Palva E.T. 1994. Alterations in water status, endogenous abscisic acid content, and expression of rab18 gene during the development of freezing tolerance in Arabidopsis thaliana. Plant Physiol. 104: 1341–1349.

    Google Scholar 

  • Lee H., Xiong L.M., Ishitani M., Stevenson B., Zhu J.K. 1999. Cold-regulated gene expression and freezing tolerance in an Arabidopsis thaliana mutant. Plant J. 17: 301–308.

    Article  PubMed  CAS  Google Scholar 

  • Li C., Puhakainen T., Welling A., Viherä-Aarnio A., Ernstsen A., Junttila O., Heino P., Palva E.T. 2002. Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes. Physiol. Plant. 116: 478–488.

    Article  CAS  Google Scholar 

  • Li C., Junttila O., Ernstsen A., Heino P., Palva E.T. 2003a. Photoperiodic control of growth, cold acclimation and dormancy development in silver birch (Betula pendula) ecotypes. Physiol. Plant. 117: 206–212.

    Article  CAS  Google Scholar 

  • Li C., Viherä-Aarnio A., Puhakainen T., Junttila O., Heino P., Palva E.T. 2003b. Ecotype-dependent control of growth, dormancy and freezing tolerance under seasonal changes in Betula pendula Roth. Trees 17: 127–132.

    CAS  Google Scholar 

  • Li C., Junttila O., Heino P., Palva E.T. 2003c. Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application. Tree Physiol. 23: 481–487.

    PubMed  CAS  Google Scholar 

  • Lim C.C., Krebs S.L., Arora R. 1999. A 25-kDa dehydrin associated with genotype- and age-dependent leaf freezing tolerance in Rhododendron: a genetic marker for cold hardiness? Theor. Appl. Genet. 99: 912–920.

    Article  CAS  Google Scholar 

  • Mäntylä E., Lng V., Palva E.P. 1995. Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LTI78 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol. 107: 141–148.

    PubMed  Google Scholar 

  • McCamant T., Black R.A. 2000. Cold hardiness in coastal, montane, and inland populations of Populus trichocarpa. Can. J. For. Res. 30: 91–99.

    Article  Google Scholar 

  • McKenzie J.S., Weiser C.J., Li P.H. 1974. Changes in water relations of Cornus stolonifera during cold acclimation. J. Amer. Soc. Hortic. Sci. 99: 223–228.

    Google Scholar 

  • Mitcham-Butler E.J., Hinesley, L.E. and Pharr D.M. 1987. Soluble carbohydrate concentration of Fraser fir foliage and its relationship to postharvest needle retention. J. Amer. Soc. Hortic. Sci. 112: 672–676.

    CAS  Google Scholar 

  • Murata N. 1983. Molecular species composition of phosphatidylglycerols from chilling-sensitive and chilling-resistant plants. Plant Cell Physiol. 24: 81–86.

    CAS  Google Scholar 

  • Murata N., Los, D.A. 1997. Membrane fluidity and temperature perception. Plant Physiol. 115: 875–879.

    PubMed  CAS  Google Scholar 

  • Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., Fujiyoshi Y. 2000. Structural determinants of water permeation through aquaporin-1. Nature 407: 599–605.

    Article  PubMed  CAS  Google Scholar 

  • Nishida I., Murata N. 1996. Chilling sensitivity in plants and cyanobacteria: The crucial contribution of membrane lipids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 541–568.

    Article  PubMed  CAS  Google Scholar 

  • Nuotio S., Heino P., Palva E.P. 2001. Signal transduction under low-temperature stress. In: Crop Responses and Adaptations to Temperature Stress, Basra A.S. (Ed), Food Products Press, New York, pp.151–175.

    Google Scholar 

  • Ögren E., Nilsson T. and 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 spruce and pine. Plant Cell Environ. 20: 247–253.

    Article  Google Scholar 

  • Öquist G., Gardeström P., Huner N.P.A. 2001. Metabolic changes during cold acclimation and subsequent freezing and thawing. In: Conifer Cold Hardiness, Bigras F.J., Colombo S.J. (Eds). Kluwer Academic Publishers, Dordrecht, pp.137–163.

    Google Scholar 

  • Palonen P. 1999. Relationship of seasonal changes in carbohydrates and cold hardiness in canes and buds of three red raspberry cultivars. J. Amer. Soc. Hortic. Sci. 124: 507–513.

    CAS  Google Scholar 

  • Palonen P., Buszard D., Donnelly D. 2000. Changes in carbohydrates and freezing tolerance during cold acclimation of red raspberry cultivars grown in vitro and in vivo. Physiol. Plant. 110: 393–401.

    Article  CAS  Google Scholar 

  • Palta J., Weiss L.S. 1993. Ice formation and freezing injury: an overview on the survival mechanisms and molecular aspects of injury and cold acclimation in herbaceous plants. In: Advances in plant cold hardiness, Li P.H., Christersson L. (Eds), CRC Press, Boca Raton, Florida, USA, pp. 143–176.

    Google Scholar 

  • Palva E.T. 1994. Gene expression under low temperature stress. In: Stress Induced Gene Expression in Plants, Basra A.S. (Ed). Harwood Academic Publishers, Chur Switzerland, pp. 103–130.

    Google Scholar 

  • Palva E.T., Heino P. 1998. Molecular mechanism of plant cold acclimation and freezing tolerance. In: Plant Cold Hardiness, Li P.H., Chen T.H.H.(Eds), Plenum Press, New York, pp. 3–14.

    Google Scholar 

  • Pan R.C. 1990. The role of abscisic acid in chilling resistance. In: Plant Growth Substances, Pharis R.T., Rood S.B. (Eds), Springer-Slaag, Berlin, pp. 391–399.

    Google Scholar 

  • Parsons L.R. 1978. Water relations, stomatal behavior, and root conductivity of red osier dogwood during acclimation to freezing temperatures. Plant Physiol. 62: 64–70.

    PubMed  Google Scholar 

  • Pomeroy M.K., Siminovitch D., Wightman F. 1970. Seasonal biochemical changes in the living bark and needles of red pine (Pinus resinosa) in relation to adaptation to freezing. Can. J. Bot. 48: 953–967.

    CAS  Google Scholar 

  • Qamaruddin M., Dormling I., Ekberg I., Eriksson G., Tillerg E. 1993. Abscisic acid content at defined levels of bud dormancy and frost tolerance in two contrasting populations of Picea abies grown in a phytotron. Physiol. Plant. 87: 203–210.

    Article  CAS  Google Scholar 

  • Repo T., Zhang G., Ryyppö A., Rikala R., Vuorinen M. 2000. The relationship between growth cessation and frost hardening in Scots pines of different origins. Trees 14: 456–464.

    Article  Google Scholar 

  • Rinne P., Welling A., Kaikuranta P. 1998. Onset of freezing tolerance in birch (Betula pubescens Ehrh.) involves LEA proteins and osmoregulation and is impaired in an ABA-deficient genotype. Plant Cell Envir. 21: 601–611.

    Article  CAS  Google Scholar 

  • Rinne P.L.H., Kaikuranta P.L.M, van der Plas L.H.W., van der Schoot C. 1999. Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209: 377–388.

    Article  CAS  PubMed  Google Scholar 

  • Sakai A., Larcher W. 1987. Frost survival of plants: responses and adaptation to freezing stress. Springer-Verlag, New York. 321p.

    Google Scholar 

  • Santarius K.A. 1973. The protective effect of sugars on chloroplast membranes during temperature and water stress and its relationship to frost, desiccation and heat resistance. Planta 113: 105–114.

    Article  CAS  Google Scholar 

  • Sarnighausen E., Karlson D., Ashworth E. 2002. Seasonal regulation of a 24-kDa protein from red-osier dogwood (Cornus sericea) xylem. Tree Physiol. 22: 423–430.

    PubMed  CAS  Google Scholar 

  • Sauter J.J., Westphal S., Wisniewski M. 1999. Immunological identification of dehydrin-related proteins in the wood of five species of Populus and in Salix caprea L. J. Plant Physiol. 154: 781–788.

    CAS  Google Scholar 

  • Shinozaki K., Yamaguchi-Shinozaki K. 1996. Molecular responses to drought and cold stress. Curr. Opin. Biot. 7: 161–167.

    Article  CAS  Google Scholar 

  • Siminovitch D., Cloutier Y. 1982. Twenty-four-hour induction of freezing and drought tolerance in plumules of winter rye seedlings by desiccation stress at room temperature in the dark. Plant Physiol. 69: 250–255.

    PubMed  Google Scholar 

  • Siminovitch D., Rheaume B., Pomeroy K., Lepage M. 1968. Phospholipid, protein, and nucleic acid increases in protoplasm and membrane structures associated with development of extreme freezing resistance in black locust tree cells. Cryobiology 5: 202–225.

    Article  PubMed  CAS  Google Scholar 

  • Stushnhoff C., Junttila O. 1986. Seasonal development of cold stress resistance in several plant species at a coastal and a continental location in North Norway. Polar Biol. 5: 129–133.

    Article  Google Scholar 

  • Tamassy I., Zayan M. 1982. Seasonal changes in total sugars, reducing and non-reducing sugars and starch contents in relation to cold hardiness of some apricot varieties from different groups. Acta Hort. 121: 125–139.

    Google Scholar 

  • Tamminen I., Mäkelä P., Heino P., Palva E.T. 2001. Ectopic expression of ABI3 gene enhances freezing tolerance in response to abscisic acid and low temperature in Arabidopsis thaliana. Plant J. 25: 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Tang X. 2002. Breeding in sea buckthorn (Hippophae rhamnoides): Genetics of berry yield, quality and plant cold hardiness. University of Helsinki, Department of Applied Biology, Publication no. 11. 48p.

  • Tasaka Y., Nishida I., Higashi S., Beppu T., Murata N. 1990. Fatty acid composition of phosphatidylglycerols in relation to chilling sensitivity of woody plants. Plant Cell Physiol. 31:545–550.

    CAS  Google Scholar 

  • Thomashow M.F. 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 571–599.

    Article  PubMed  CAS  Google Scholar 

  • Weiser C.J. 1970. Cold resistance and injury in woody plants. Science 169: 1269–1278.

    Article  PubMed  Google Scholar 

  • Welling A. 2003. Overwintering in woody plants: Involvement of ABA and dehydrins. University of Helsinki, Viikki Biocenter, Publication No. 19/2003. 59p.

  • Welling A., Kaikuranta P., Rinne P. 1997. Photoperiodic induction of dormancy and freezing tolerance in Betula pubescens. Involvement of ABA and dehydrins. Physiol. Plant. 100: 119–125.

    Article  CAS  Google Scholar 

  • Williams B.J.J., Pellett N.E., Klein R.M. 1972. Phytochrome control of growth cessation and initiation of cold acclimation in selected woody plants. Plant Physiol. 50: 262–265.

    PubMed  Google Scholar 

  • Wisniewski M., Close T., Artlip T., Arora R. 1996. Seasonal patterns of dehydrins and 70-kDa heat-shock proteins in bark tissues of eight species of woody plants. Physiol. Plant. 96: 496–505.

    Article  CAS  Google Scholar 

  • Wisniewski M., Webb R., Balsamo R., Close T.J., Yu X.M., Griffith M. 1999. Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol. Plant. 105: 600–608.

    Article  CAS  Google Scholar 

  • Xin Z., Browse J. 2000. Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ. 23: 893–902.

    Article  Google Scholar 

  • Yelenosky G. 1979. Water-stress induced cold hardening of young citrus trees. J. Amer. Soc. Hortic. Sci. 104: 270–273.

    Google Scholar 

  • Yoshida S. 1984. Chemical and biophysical changes in the plasma membrane during cold acclimation of mulberry bark cells (Morus bombycis Koidz. cv. Goroji). Plant Physiol. 76: 257–265.

    PubMed  CAS  Google Scholar 

  • Yoshida S., Sakai A. 1973. Phospholipid changes associated with the cold hardiness of cortical cells from poplar stem. Plant Cell Physiol. 14: 353–359.

    CAS  Google Scholar 

  • Zwiazek J.J., Renault S., Croser C., Hansen J., Beck E. 2001. Biochemical and biophysical changes in relation to cold hardiness. In: Conifer Cold Hardiness, Bigras F.J., Colombo S.J. (Eds). Kluwer Academic Publishers, Dordrecht, pp. 165–186.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chunyang Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, C., Junttila, O. & Palva, E.T. Environmental regulation and physiological basis of freezing tolerance in woody plants. Acta Physiol Plant 26, 213–222 (2004). https://doi.org/10.1007/s11738-004-0010-2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-004-0010-2

Key words

Navigation