Abstract
This introductory overview shows that cold, in particular frost, stresses a plant in manifold ways and that the plant’s response, being injurious or adaptive, must be considered a syndrome rather than a single reaction. In the course of the year perennial plants of the temperate climate zones undergo frost hardening in autumn and dehardening in spring. Using Scots pine (Pinus sylvestris L.) as a model plant the environmental signals inducing frost hardening and dehardening, respectively, were investigated. Over 2 years the changes in frost resistance of Scots pine needles were recorded together with the annual courses of day-length and ambient temperature. Both act as environmental signals for frost hardening and dehardening. Climate chamber experiments showed that short day-length as a signal triggering frost hardening could be replaced by irradiation with far red light, while red light inhibited hardening. The involvement of phytochrome as a signal receptor could be corroborated by respective night-break experiments. More rapid frost hardening than by short day or far red treatment was achieved by applying a short period (6 h) of mild frost which did not exceed the plant’s cold resistance. Both types of signals were independently effective but the rates of frost hardening were not additive. The maximal rate of hardening was − 0.93°C per day and frost tolerance of < − 72°C was achieved. For dehardening, temperature was an even more effective signal than day-length.
Similar content being viewed by others
References
Aronsson A 1975 Influence of photo-and thermoperiod on the initial stages of frost hardening and dehardening of phytotronegrown seedlings of Scots pine (Pinus sylvestris L.) and Norway spruce (Picea abies (L.) Karst.);Studi. For. Suec. 128 1–20
Baek K-H and Skinner D Z 2003 Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines;Plant Sci. 165 1221–1227
Beck E, Hansen J, Heim R, Schäfer C, Vogg G, Leborgne N, Teulieres C and Boudet A M 1995 Cold hardening and dehardening of evergreen trees; inEUROSILVA — Contribution to forest tree physiology (eds) H Sandermann and M Bonnet-Masimbert (Paris: Ed. INRA) vol 76, pp 171–193
Bervaes J C A M, Ketchie D O and Kuiper P J C 1978 Cold hardiness of pine needles and apple bark as affected by alteration of day length and temperature;Physiol. Plant 44 365–368
Bigras F J and D’Aoust A L 1993 Influence of photoperiod on shoot and root frost tolerance and bud phenology of white spruce seedlings (Picea glauca);Can. J. For. Res. 23 219–228
Chen H-H and Li P H 1978 Interactions of low temperature, water stress and short days in the induction of stem frost hardiness in red osier dogwood;Plant Physiol. 62 833–835
Christersson L 1978 The influence of photoperiod and temperature on the development of frost hardiness in seedlings ofPinus silvestris andPinus abies;Physiol. Plant. 44 288–294
Close T J 1997 Dehydrins: A commonality in the response of plants to dehydration and low temperature;Physiol. Plant. 100 291–296
Clough R C and Vierstra R D 1997 Phytochrome degradation;Plant Cell Environ. 20 713–721
Elmlinger M W and Mohr H 1994 Regulation of glutamine synthetase gene expression in Scots pine (Pinus sylvestris L.) seedlings;Nova Acta Leopold. NF70 113–125
Fernbach E and Mohr H 1990 Coaction of blue/ultraviolet — A light and light absorbed by phytochrome in controlling growth of pine (Pinus sylvestris L.) seedlings;Planta 180 212–216
Fowler S and Thomashow M F 2002 Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway;Plant Cell 14 1675–1690
Frankow-Lindberg B E 2001 Adaptation to Winter Stress in Nine White Clover Populations: Changes in Non-structural Carbohydrates During Exposure to Simulated Winter Conditions and ‘Spring’ Regrowth Potential;Ann. Bot. 88 745–751
Gordon-Kamm W J and Steponkus P L 1984 Lamellar-to-hexagonalII phase transitions in the plasma membrane of isolated protoplasts after freeze-induced dehydration;Proc. Natl. Acad. Sci. USA 81 6373–6377
Greer D H and Warrington I J 1982 Effect of photoperiod, night temperature, and frost incidence on development of frost hardiness inPinus radiata;Aust. J. Plant Physiol. 9 333–342
Greer D H and Stanley C J 1985 Regulation of the loss of frost hardiness inPinus radiata by photoperiod and temperature;Plant Cell Environ. 8 111–116
Greer D H, Stanley C J and Warrington I J 1989 Photoperiod control of the initial phase of frost hardiness development inPinus radiata;Plant Cell Environ. 12 661–668
Hansen J and Beck E 1994 Seasonal changes in the utilization and turnover of assimilation products in a 8-year-old Scots pine (Pinus sylvestris L.) trees;Trees 8 172–182
Hansen J, Türk R, Vogg G, Heim R and Beck E 1997 Conifer carbohydrate physiology: Updating classical views; inTrees - Contributions to modern tree physiology (eds) H Rennenberg, W Eschrich and H Ziegler (Leiden: Backhuys Publ.) pp 97–108
Hernández-Nistal J, Dopico B and Labrador E 2002 Cold and salt stress regulates the expression and activity of a chickpea cytosolic Cu/Zn superoxide dismutase;Plant Sci. 163 507–514
Hoddinott J and Scott R 1996 The influence of light quality and carbon dioxide enrichment on the cold hardiness of three conifer species seedlings;Biotronics 25 33–44
Howell G S and Weiser C J 1970 The environmental control of cold acclimation in apple;Plant Physiol. 45 390–394
Hughes M A and Dunn M A 1996 The molecular biology of plant acclimation to low temperature;J. Exp. Bot. 47 291–305
Ishitani M, Xiong L, Stevenson B and Zhu J K 1997 Genetic analysis of osmotic and cold stress signal transduction inArabidopsis: interactions and convergence of abscisic acid-dependent and abscisic acid-independent pathways;Plant Cell 9 1935–1949
Jaglo-Ottosen K R, Glimour S J, Zarka D G, Schabenberger O and Thomashow M F 1998Arabidopsis CBF1 overexpression induces cor genes and enhances freezing tolerance;Science 280 104–106
Janácek J and Prásil I 1991 Qantification of plant frost injury by nonlinear fitting of an S-shaped function;Cryo-Letters 12 47–52
Jonsson A, Eriksson G, Dormling I and Ifver J 1981 Studies on frost hardiness ofPinus contorta Dougl. Seedlings grown in climate chambers;Studi. For. Suec. 157 3–47
Juntilla O and Kaurin A 1990 Environmental control of cold acclimation inSalix pentandra;Scand. J. For. Res. 5 195–204
Kandler O, Dover C and Ziegler P 1979 Kälteresistenz der Fichte. I. Steuerung von Kälteresistenz, Kohlenhydrat-und Proteinstoffwechsel durch Photoperiode und Temperatur;Ber. Deutsch. Bot. Ges. 92 225–241
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K and Shinozaki K 1999 Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor;Nat. Biotech. 17 287–291
Larcher W 2001 Ökophysiologieder Pflanzen (Stuttgart: Eugen Ulmer) p. 302
Liu J-J J, Krenz D C, Galvez A F and de Lumen B O 1998 Galactinol synthase (GS): increased enzyme activity and levels of mRNA due to cold and desiccation;Plant Sci. 134 11–20
McKenzie J S, Weiser C J and Burke M J 1974 Effects of red and far red light on the initiation of cold acclimation inCornus stolonifera Michx.:Plant Physiol. 53 783–789
Mohr H 1994 Coaction between pigment systems; inPhotomorphogenesis in plants (eds) R E Kendrick and G H M Kronenberg (Dordrecht: Kluwer Academic Publ.) pp 353–373
Monroy A F and Dhindsa R S 1995 Low-Temperature Signal Transduction: Induction of Cold Acclimation-Specific Genes of Alfalfa by Calcium at 25°C;Plant Cell 7 321–331
Monroy A F, Labbé E and Dhindsa R S 1997 Low temperature perception in plants: effects of cold on protein phosphorylation in cell-free extracts;FEBS Lett. 410 206–209
Monroy A F, Sarhan F R S and Dhindsa R S 1993 Cold-Induced Changes in Freezing Tolerance, Protein Phosphorylation, and Gene Expression (Evidence for a Role of Calcium);Plant Physiol. 102 1227–1235
Nanjo T, Kobayashi M, Yoshida Y, Kakubari Y, Yamaguchi-Shinozaki K and Shinozaki K 1999 Antisense suppression of proline degradation improves tolerance to freezing and Salinity inArabidopsis thaliana;FEBS Lett. 461 205–210
Qamaruddin M, Dormling I, Ekberg I, Eriksson G and Tillberg E 1993 Abscisic acid content at defined levels of bud dormancy and frost tolerance in two contrasting populations ofPicea abies grown in a phytotrone;Physiol. Plant. 87 203–210
Quinn P J 1985 A lipid phase separation model of low temperature damage to biological membranes;Cryobiology 22 28–46
Repo T 1992 Seasonal changes of frost hardiness inPicea abies andPinus sylvestris in Finland;Can. J. For. Res. 22 1949–1957
Sakai A and Larcher W 1987Frost survival of plants: response and adaptation to freezing stress Ecol. Studies 62 (eds) W D Billings, F Golley, O L Lange, J S Olson and H Remmert (Berlin, New York: Springer)
Sakai A, Otsuka K and Yoshida S 1968 Mechanisms of survival of plant cells at super-low temperatures by rapid cooling and rewarming;Cryobiology 4 165–173
Senser M and Beck E 1982 Frost resistance in Spruce (Picea abies (L.) Karst): V. Influence of photoperiod and temperature on the membrane lipids of the needles; Z.Pflanzenphysiol. 108 71–85
Senser M and Beck E 1977 On the mechanisms of frost injury and frost hardening of spruce chloroplasts;Planta 137 195–201
Shinozaki K and Yamaguchi-Shinozaki K 2000 Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways;Curr. Opinion Plant Biol. 3 217–223
Silim S N and Lavender D P 1994 Seasonal patterns and environmental regulation of frost hardiness in shoots of seedlings ofThuja plicata, Chamaecyparis nootkatensis, andPicea glauca;Can. J. Bot. 72 309–316
Smits-Spinks B, Swanson B T and Markhart A H 1985 The effect of photoperiod and thermoperiod on cold acclimation and growth ofPinus sylvestris;Can. J. For. Res. 15 453–460
Steponkus P L and Lanphear F O 1967 Refinement of the triphenyl tetrazolium chlorid method of determining cold injury;Plant Physiol. 42 1423–1426
Steponkus P L, Uemura M, Joseph R A, Gilmour S J and Thomashow M F 1998 Mode of action of the COR15a gene on the freezing tolerance ofArabidopsis thaliana;Proc. Natl. Acad. Sci. USA 95 14570–14575
Takagi T, Nakamura M, Hayashi H, Inatsugi R, Yano R and Nishida I 2003 The Leaf-Order-Dependent Enhancement of Freezing Tolerance in Cold-AcclimatedArabidopsis Rosettes in not Correlated with the Transcript Levels of the ColdInducible Transcription Factors of CBF/DREB1;Plant Cell Physiol. 44 922–931
Tao D-L, Öquist G and Gunnar Wingsle G 1998 Active Oxygen Scavengers during Cold Acclimation of Scots pine Seedlings in Relation to Freezing Tolerance;Cryobiology 37 38–45
Thomashow M F 1999 Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms;Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 571–599
Thomashow M F 2001 So what’s new in the field of plant cold acclimation? Lots!;Plant Physiol. 125 89–93
Tremblay M F and Lalonde M 1987 Effect of photoperiod and temperature on the development of frost hardiness in threeAlnus species;Physiol. Plant. 70 327–331
Tumanov I and Krasavtsev O A 1959 Hardening of northern woody plants by temperature below zero;Sov. Plant Physiol. 6 663–673
Van den Driesche R 1969 Influence of light intensity and photoperiod on frost-hardiness development in Douglas-fir seedlings;Can. J. Bot. 48 2129–2134
Vogg G, Heim R, Gotschy B, Beck E and Hansen J 1998b Frost hardening and photosynthetic performance of Scots pine (Pinus sylvestris L.). II. Seasonal changes in the fluidity of thylakoid membranes;Planta 204 201–206
Vogg G, Heim R, Hansen J, Schaefer C and Beck E 1998a Frost hardening and photosynthetic performance of Scots pine (Pinus sylvestris L.) needles. I. Seasonal changes in the photosynthetic apparatus and its function;Planta 204 193–200
Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou H-E, Rajashekar C B, Williams T D and Wang X 2002 Profiling membrane lipids in plant stress responses. Role of phospholipase Da in freezing induced lipid changes inArabidopsis;J. Biol. Chem. 277 31994–32002
Williams W P 1990 Cold-induced lipid phase transitions;Philos. Trans. R. Soc. London B326 555–570
Ying J, Lee E A and Tollenaar M 2000 Response of maize leaf photosynthesis to low temperature during the grain-filling period;Field Crops Res. 68 87–96
Zehnder L R and Lanphear F O 1966 The influence of temperature and light on the cold hardiness ofTaxus cuspidata;Proc. Am. Soc. Hortic. Sci. 89 706–113
Zhu J J and Beck E 1991 Water relations ofPachysandra leaves during freezing and thawing;Plant Physiol. 97 1146–1153
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Beck, E.H., Heim, R. & Hansen, J. Plant resistance to cold stress: Mechanisms and environmental signals triggering frost hardening and dehardening. J. Biosci. 29, 449–459 (2004). https://doi.org/10.1007/BF02712118
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF02712118