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Physiological responses to low temperature O. Junttila Department of Plant Physiology and Microbiology, University of Troms!, Tromso, Norway y Introduction ment for geneirative development (flower- and seed production) is higher than ing that for vegetative growth. Our knowledge is one of the main environ- Temperature on exact temperature requirements for mental factors regulating and limiting plant growth of various woody species is limited growth. Basic chemical and biochemical and very little has been done to character- processes in plants are temperature ize the biochemical and physiological dependent and various growth processes bases for growth at low temperature. have their specific requirements for mini- Much more research has been devoted mum, optimum and maximum tempera- to studies of low temperature as a limiting tures. Distribution of woody plants is often factor for survival of the trees. This is part- limited by low temperature and we can a question of the maximum level of ly separate two main effects: 1) limitation of hardiness in the species, partly a question growth and development: temperature of a proper timing of hardening and during the growing season is too low dehardening in relation to the annual tem- and/or the growing season is too short for perature variation and partly a question of completion of growth and development, tolerance of unexpected periods of low 2) limitation of survival: minimum temper- temperature. Several extensive studies atures during some period of the annual (see Sakai and Larcher, 1987, for refer- cycle are regularly lower than can be toler- ences) have clearly shown correlations ated by the plant. Native species and between the level of cold hardiness and provenances are normally adapted to local the local winter temperature conditions for climate but responses to low temperature various species. Survival adaptation to low are of great importance when species or temperature has a genetic basis, but the ecotypes are moved from their original biochemical and physiological changes location to new areas. in occurring plants regulated by are an Low temperature has been summer interaction of genotype and environmental to be limiting factor for distri- suggested a factors. bution of several vascular plants in Scan- dinavia, primarily due to the temperature The aim of this review is to give a short effect on oxidative phosphorylation (Skre, description of some basic aspects of envi- i 979). Generally, the temperature require- ronmental and genetic controls of cold
This is the case with spruce hardiness in temperate woody plants and supercooling. and willow, while even rapidly growing briefly to discuss physiological mecha- shoots of pine tolerate ice formation nisms for cold hardiness, with the main (Christersson, 1978, 1985; Christersson emphasis on supercooling and the role of the cell membranes. et al., 1987; von Fircks, 1985). The degree of supercooling is depen- dent, in addition to the rate of cooling, upon the occurrence of heterogeneous ice nuclei. It has been suggested that plants Response to frost during active growth do not contain intrinsic ice nuclei active above -8 to -11 °C (Lindow et al., 1982), but such ice nuclei may well exist (cf. Frost during the growth season is com- Andrews et al., 1986). In any case, certain in many areas. In Fennoscandia, strains of various epiphytic bacteria are mon frost is quite frequent during the summer important ice nucleators (ice nucleation and temperatures down to -10°C in the active, (INA) bacteria). Pseudomonas middle of the growing period have been syringae, one of the most effective INA reported in southern Sweden (Christers- bacteria, will catalyze ice formation at son, 1985). In these areas, summer frost about -1.5°C. INA bacteria are known to can be more injurious to forest trees than be important for cold injury in herbaceous frost in winter. Generally, the frost toler- species (Lindow, 1983; Gusta, 1985) and ance of growing trees is very limited. this has stimulated studies on new There are, however, significant differences methods to control frost injury to crops between species, but probably not be- (Lindow, 1983; Hirano and Upper, 1985). tween latitudinal provenances (Christers- One approach is to control the population son, 1985). Seedlings of spruce are less density of these bacteria, another is to resistant than those of pine, and birch and inhibit the nucleation activity of the bacte- alder are quite hardy during active growth. ria. Recently, Watanabe et al. (1988) have Normally non-hardy tissue does not toler- reported a number of chemicals which ate ice formation and the level of hard- inhibit the nucleation activity of INA Er- iness is dependent upon the degree of winia. Among the most effective com-
growth cessation under pounds was n-octylbenzyldimethyl-ammo- long photo- even nium salt, which they used to protect tea periods. plants from freeze-injury. The physiolo
various other conditions (availability of hardening (Aronsson, 1975; Christersson, mineral nutrition, atmospheric 1978; Jonsson et al., 1981). Cannel ef al. water, conditions, etc.), which affect plant growth (1985) have proposed a model based on and development. Effects of various types day length and temperature for calculation of pollutants on the frost sensitivity of of acclimation in P. sitchensis. Their model plants now need particular attention. Stu- accurately predicted known instances of dies with Picea abies (Barnes and David- autumn frost damage at selected loca- son, 1988) and with P. sitchensis (Lucas tions. However, at least some plants may et aL, 1988) indicate that exposure of the develop a high level of hardiness without plants to ozone increases their frost sensi- an exposure to low temperature, if they tivity (see also presentations at this sym- are kept for a long period under short days. This is illustrated for Salix pentan- posium). dra in Table II. Although species such as Salix may harden slowly under short days at relative- aspects of cold hardiness Genetic ly high temperature, a rapid increase in hardiness is induced by short exposures to subzero temperatures. Even one day at Numerous studies with broadleaf and - 3°C can significantly enhance the hardi- conifer species have shown differences in ness (Junttila and Kaurin, unpublished) cold hardiness between various prove- and this response is thought to be com- nances and ecotypes. Normally, the maxi- mon for many woody species. mum level of hardiness or the potential for hardening is not significantly different in Deacclimation is primarily a tempera- various ecotypes of a tree species. For ture-controlled process, but both the rate example, both a southern (60° N Lat.) and and the magnitude of response to tem- a northern (70° N Lat.) ecotypes of S. perature treatment can greatly vary be- pentandra has the capacity to tolerate tween species and cultivars. In addition, liquid N (Junttila and Kaurin, unpub- 2 deacclimation is affected by an endogen- lished). However, these ecotypes differ ous rhythm of the plant (Kaurin et al., greatly from each other in respect to the 1981).). In terms of the degree growth of acclimation (Table III). model developed by Fuchigami and his regulation Delayed acclimation in the southern ecoty- coworkers (Fuchigami et aL, 1982), the pe is closely connected to delayed growth rate of dehardening increases gradually cessation. In some cases, too rapid deac- when the plant changes from the stage of climation and/or spring bud break in rela- maximum dormancy (270°GS) towards tion to the local temperature conditions the stage of spring bud break (360°GS). can be the main reason for cold injury (see This has been shown for Pinus sylvestris Cannell et al., 1985). Thus, both the timing in a recent study by Repo and Pelkonen and the rate of acclimation/deacclimation (1986). We must, however, be aware that are often more critical than the maximum there is not necessarily any direct de- level of hardiness for avoidance of frost pendence between the physiological injury in woody plants. dormancy and the state of cold hardiness. It should also be mentioned that, in Euca- Results in Table III also show that both lyptus, roots are involved in the deharden- and development of growth cessation ing process in shoots (Paton et al., 1979). hardiness in Salix show an approximately intermediate inheritance in the F Annual changes in cold hardiness of -genera- l tion. Photoperiodic regulation of bud set in are, of course, also influenced by plants
Quamme, 1985). Deep supercooling is Picea has been shown to be regulated by dependent upon the existence of barriers genes with additive effects (Eriksson et al., 1978). Recently, Norell et al. (1986) for ice seeding in plant tissue. Due to such have published results supporting a poly- barriers, small pockets of liquid water are retained in tissue, until it is finally frozen genic inheritance of frost hardiness in P. sylvestris. Quantitative inheritance of cold due to a homogeneous nucleation. In tis- hardiness is also supported by several sues with deep supercooling, the killing studies with fruit crops (Stushnoff et al., point is normal’ly identical or close to the freezing point of supercooled water. This 1985). freezing point can be exactly detected as Adaptation to climatic conditions is a low temperature exotherm by differential based on genetic mechanisms and usually thermal analysis (DTA) and the hardiness takes several generations. There is, how- level of tissues; showing deep supercool- ever, a possibility that significant changes ing can be rapidly measured using DTA. can occur quite rapidly, and that we Due to the temperature for homoge- perhaps also have to be aware of long- nucleation, the hardiness limit of lasting physiological after-effects (Bjorn- neous woody plants showing deep supercooling stad, 1981; Johnsen, 1988). in xylem ray parenchyma should be around -40°C. This has been reported to be the case with several species of deci- duous hardwoods (George et al., 1974; Deep supercooling literature cited by Quamme, 1985). How- ever, certain species with deep supercool- found in areas where the minimum In the absence of ice ing heterogeneous are temperature often is below -45°C (Gusta nucleators, water can be undercooled until it freezes due to a homogeneous nuclea- et al., 1983). This study revealed that low temperature exotherms could be found as tion at about -38°C. Deep supercooling is low as -53°C in Quercus coccinea, Vitis a mechanism for avoiding freezing in the xylem of several deciduous hardwoods, in riparia and Ulmus americana. In Fraxinus pennsylvanica and Prunus padus the low bark, in vegetative and flower buds of both hardwoods and conifers, and in seeds of temperature exotherms disappeared en- tirely in non-thawed, fully hardy twigs various species (Burke et al., 1976; Juntti- (Gusta et al., 1983). Some recent studies la and Stushnoff, 1977; Sakai, 1978;
also indicate that low temperature exo- 1985). The availability of tissue water for however, be therms in the xylem tissue are not neces- important freezing an can, aspect in cold tolerance. According to Ver- sarily connected with the killing point of tucci et al. (1988), water in vegetative the tissue (L.V. Gusta, personal communi- cation). Thus, the relationship between buds of a frost-sensitive apple cultivar low temperature exotherms and tissue (Golden Delicious) was more available to injury should be carefully studied before freeze than water in buds of resistant a DTA is applied as a method for estimation cultivar (Dolgo). of cold hardiness. Frost dehydration and rehydration xylem, buds and seeds, the ability In the during thawing induces a multitude of for supercooling is primarily dependent stresses (mechanical, chemical, thermal upon certain intact anatomical/morphologi- and possibly also electrical) (Steponkus, cal structures and, in most cases, low tem- 1984). Often the mechanical and the perature exotherms are found both in chemical stresses are the most important. living and dead intact tissues. In xylem, Hincha et a/. (1987) have suggested that the cell walls seem to be an important bar- in vivo dehydration both by freezing and rier to ice growth, but the plasma mem- desiccation of spinach leaves results in brane is essential for supercooling to mechanical damage, rupture of the thyla- at temperatures below -40°C membrane. Cold acclimation in- koid occur (Gusta et aL, 1983). According to Quam- the cell’s ability to tolerate these creases me (1985), starch in the tissue may retain stresses. Changes occurring during accli- water within the cell during freezing until mation may decrease the extent of cell the point of homogeneous nucleation is dehydration, minimize the concentration of reached. In floral primordia of azalea toxic solutes and increase the stability of (George et al., 1974), in peach flower the cell membranes (Steponkus, 1984). buds (Ashworth, 1982), and in winter buds Membrane stabilization may include of some conifers (Sakai, 1978), certain both changes in membrane fatty acids morphological features of the buds seem and accumulation of cryoprotective sub- to be essential for supercooling. stances. Kacperska (1985) has presented a model for frost hardening in herbaceous plants consisting of two types of mecha- nisms: 1) mechanisms that allow plants to Membranes and frost resistance function at low non-freezing temperature, (i.e., maintenance of high membrane fluid- ity, mainly due to a rapid increase in the It is generally assumed that the cell mem- content of polyunsaturated fatty acids in branes are the primary target of frost injury membrane lipids); 2) mechanisms that (Steponkus, 1984). Under natural condi- protect a cell against deleterious effects of tions, ice in hardy tissues is normally frost (i.e., accumulation of compounds that formed extracellularly, first in areas with increase the stability of the membranes). relatively large amounts of free water. Ice The plasma membrane (plasmalemma) formation causes a water vapor pressure and the tonoplast are in many cases the gradient and water then migrates to the primary sites of frost injury, but especially ice crystals. This results in dehydration of in conifers the frost resistance of the thyla- the cells and an increase in solute concen- koid membranes can be of great import- tration. For most cells, over 60% of the ance. Frost on cold-acclimated Scots pine water is frozen at -4°C and nearly all can cause both reversible and irreversible freezable water is frozen at -15°C (Gusta,
inhibitions of photosynthesis (Strand, nization, then selection for these charac- 1987). The reversible effect can be due to ters at the cell culture level would be diffi- inactivation of enzymes in photosynthetic cult, if not impossible. Deep supercooling carbon reduction cycle and/or a restriction is dependent upon certain anatomical and of photophosphorylation. The irreversible morphological structures which are not effect is thought to be due to an injury to present in cell cultures. The importance of the thylakoid membranes involving dam- the developmental stage for expression of age to the Q (Strand, 1987; -protein B cold hardiness is also shown by the fact bquist, 1987). Studies of Oquist and that, although differences in frost hardi- coworkers have also shown that a com- between a hardy (Dolgo) and an ness bined exposure to light and low tempera- unhardy (Golden Delicious) cultivar of ture causes photoinhibition of photosyn- apple could be detected in young seed- thesis in Scots pine. Photosystem II is lings (Stushnoff et al., 1985), there was no inhibited and this effect can be observed difference in frost hardiness of ungermi- by measuring the variable fluorescence of nated seeds of these cultivars (Junttila the P Due to the effects of temperature II’ and Stushnoff, unpublished). On the other on the fluorescence from the P it has hand, somaclonal variation in plants ob- , II been suggested that measurement of tained from c cultures can be a i Ed source chlorophyll fluorescence can be used as a for new, cold-hardy genotypes (Lazar screening method for frost tolerance et al., 1988). (Sundbom ef al., 1982). A completeily new line of research is emerging in connection with the develop- ment of methods for genetic transforma- tion of plants. The process is, however, Future aspects delayed by the lack of knowledge on the regulation of cold hardiness at the molecu- Development of tissue and cell suspen- lar level. Several research groups are now sion cultures has provided new possibili- investigating the molecular basis of cold ties for selection and manipulation of cold hardiness in higher plants. Specific pro- hardiness. These techniques make it pos- teins associated with the development of sible to work with an almost unlimited cold hardiness, either induced by low tem- number of genotypes which should in- perature or by ABA, have been described crease the probability of finding more for several herbaceous species (Robert- hardy genotypes. In spite of the promising son et al., 1988; Guy and Haskell, 1987; aspects (Chen and Gusta, 1986), so far no Gilmour et al., 1988). Such studies can real success has been reported from stu- lead to identification, isolation and cloning dies of this type and probably the possibili- of genes which code for possible cold ties for successful selections from cell cul- hardiness proteins. Small molecular tures of woody plants are rather limited. In organic osmolytes, such as trehalose, most cases, the hardiness problem in betaine and proline, are known to have woody plants is connected with the regula- cryoprotective effects in plant cells and tion of acclimation and deacclimation, genetic regulation of the biosynthesis of rather than with the absolute capacity for such compounds could provide another cold hardiness. If the regulation of these approach to control cold hardiness in plant processes, for example photoperiodic cells. Genes regulating the biosynthesis of regulation, is dependent upon a certain glycine, betaine and trehalose in Escheri- stage of development and/or tissue orga- chia coli have already been identified
(Strom et al., 1986; Giaever et al., 1988), extracellular ice formation. The cell mem- preparing the way for experiments with the branes, especially the plasmalemma and introduction of such genes into plant cells. the thylakoid membranes, are supposed to be the primary target of frost injury. This Development within the field of molecular injury is a result of several types of biology is very rapid but, knowing the complexity of factors regulating the hard- stresses induced during a freeze-thaw iness at the whole tree level, there is still a cycle. Cold acclimation makes plant cells long way to go before we can expect capable of tolerating these stresses by inducing a multitude of changes in the major breakthroughs. membranes and in their environments. Development of methods for in vitro cul- plant cells and for genetic transfor- ture of Summary mation of plants has opened up new pos- sibilities in the study of cold hardiness. However, our knowledge of the molecular Low temperature resistance in temperate basis of cold hardiness is presently too woody plants is characterized by a zone weak to substantiate an effective use of market annual variation generally showing these methods for improvement of cold inverse relationship between the an hardiness in woody plants. growth activity and the level of hardiness. These annual changes in hardiness are controlled by an interaction between the genotype and environmental factors, Acknowledgments especially day length and temperature. Cessation of elongation growth is a prere- I would like to thank L.V. Gusta and Karen Tani- quisite for acclimation in most species with for their comments on the manuscript. no a free growth pattern and this process is Thanks are due to the Norwegian Research primarily controlled by photoperiod. Short- Council for Sciences and Humanities for finan- cial support. day-induced blockage of the biosynthesis of active gibberellin could be an early step leading to the cessation of growth. Cold acclimation is induced most effectively by References a combination of short photoperiod and low temperature. Deacdimation is mainly Andrews P.K., Proebsting E.L. Jr. & Gross D.C. a response to an increasing temperature. (1986) Ice nucleation and supercooling in Cold hardiness is a quantitative character freeze-sensitive peach and sweet cherry and its genetic background in woody tissues. J. Am. Soc. Hortic. Sci. 111, 232-236 plants is not known in any detail. Aronsson A. (1975) Influence of photo- and thermoperiod on initial stages of frost hardening Cold hardiness during active growth is and dehardening of phytotron-grown seedlings normally based on an avoidance of freez- of Scots pine (Pinus silvestris L.) and Norway ing and the level of hardiness is depen- spruce (Picea abies (L.) Karst.). Stud. For. Suec. 128, 1-20 dent upon the supercooling of the tissue. Ashworth E.N. (1982) Properties of peach flow- However, some species seem to tolerate er buds which facilitate supercooling. Plant ice formation even in a non-acclimated PhysioL 70, 1475-1479 stage. Deep supercooling is a mechanism Barnes J.D. & Davison A.W. (1988) The influ- for cold tolerance in xylem and bud tis- ence of ozone on the winter hardiness of Norway sues of certain species, but normally the spruce (Picea abies (L.) Karst.). New Phytol. hardiness is based on the tolerance of 108, 159-166
Bjornstad A. (1981) Photoperiodical after-effect Gilmour S.J., Zeevaart J.A.D., Schwenen L. & of parent plant environment in Norway spruce Graebe J.E. (1986) Gibberellin metabolism in (Picea abies (L.) Karst.) seedlings. Rep. Norw. cell-free extracts from spinach leaves in relation For. Res. Inst 36, 1-30 photoperiod. Plant Physiol. 82, 190-195 to Burke M.J., Gusta L.V., Quamme H.A., Weiser G1a3ver H.M., Sfyrvold O.B., Kaasen I. & Strom C.J. & Li P.H. (1976) Freezing injury in plants. A.R. (1988) Biochemical and genetic characteri- Annu. Rev. Plant Physiol. 27, 507-528 zation of osmoregulatory trehalose synthesis in Escherichia coli. J. Bacteriot 170, 2841-2849 Cannell M.G.R., Murray M.B. & Sheppard L.J. (1985) Frost avoidance by selection for late bud Graebe J.E. (1987) Gibberellin biosynthesis and break in Picea sitchensis. J. AppL Ecol. 22, control. Annu. Rev. Ptant Physiol 38, 419-465 931-941 Gusta L.V. (1985) Freezing resistance in plants. Cannel M.G.R., Sheppard L.J., Smith R.I. & In: Plant Production in the North. (Kaurin A., Murray M.B. (1985) Autumn frost damage on Junttila O. & Nilsen J., eds.), Norwegian Univ. young Picea sitchensis. 2. Shoot frost harden- Press, Oslo, pp. 219-235 ing, and the probability of frost damage in Scot- Gusta L.V.,Tyler N.J. & Chen T.H.H. (1983) land. Forestry 58, 145-166 Deep undercoollng in woody taxa growing north Chen T.H.H. & Gusta L.V. (1983) Abscisic acid- of the !0°C isotherm. Plant Physiol. 72, 122- induced freezing resistance in cultured plant 128 cells. Ptant Physiol. 73, 71-75 Guy C.L. & Haskell D. (1987) Induction of freez- Chen TH.H. & Gusta L.V. (1986) Isolation and ing tolerance in spinach in association with the characterization of mutant cell lines and plants: synthesis of cold acclimation induced proteins. cold tolerance. In: Cell Culture and Somatic Plant Physiof. 84, 872-878 Cell Genetics of Plants. Vol. 3. Academic Press, New York, pp. 527-535 Håbjørg A. (1978) Photoperiodic ecotypes in Scandinavian trees and shrubs. Meld. Norw. Christersson L. (1978) The influence of photo- Landbrhogsk. 5;7, 1-20 period and temperature on the development of frost hardiness in seedlings of Pinus silvestris Heide O.M. (1f174) Growth and dormancy in and Picea abies. Physiol. Plant. 44, 288-294 Norway spruce ecotypes (Picea abies). 1. Inter- action of photoperiod and temperature. Physiol. Christersson L. (1985) Frost damage during the Plant. 30,1-12 2 growing season. In: Plant Production in the North. (Kaurin A, Junttila, O. & Nilsen J., eds.), Hincha D.K., Hrafner R., Schwab K.B., Heber U. Norwegian Univ. Press, Oslo, pp. 191-198 & Schmitt J.M. (1987) Membrane rupture is a Christersson L., von Fircks H. & Sihe Y (1987) of damage to chloroplast mem- common cause to conifer branes in leaves injured by freezing or exces- frost Damage seedlings by summer and winter drought. In: Plant Cold Hardiness. sive wilting. Plant Physiol. 83, 251-253 (Li P.H., ed.), Alan R. Liss, Inc., New York, Hirano S.S. & Upper C.D. (1985) Ecology and pp. 203-2100 physiology of P syringae. Biotech- eudo/nonas s Eriksson G., Ekberg I., Dormling I. & Matern B. nology 3, 1073- 078 1 (1978} Inheritance of bud-set and bud-flushing Johnsen 0. (1988) Altered progeny perfor- in Picea abies (L.) Karst. Theor. AppL Genet. mance from a southern seed orchard containing 52, 3-19 9 northern clones of Picea abies. I. Frost hardi- Fuchigami L.H., Weiser C.J., Kobayashi K., ness in a phytotron experiment. Scan J. For. Timmis R. & Gusta L.V. (1982) A degree growth Res. (in press) stage ( model and cold acclimation in tem- GS) o Jonsson A., Eriksson G., Dormling I. & Ifver J. perate woody plants. In: Plant Cold Hardi- (1981) Studies on frost hardiness of Pinus ness and Freezing Stress, Mechanisms and contorta seedlings grown in climate chambers. Crop Implications. (Li P.H. & Sakai A., eds.), Stud. For. Suec. 157, 1-47 Academic Press, New York, pp. 93-116 6 Junttila O. & Jensen E. (1988) Gibberellins and George M.F., Burke M.J. & Weiser C.J. (1974) photoperiodic control of shoot elongation in Supercooling in overwintering azalea flower Salix. Physiol. Plant. 74, 371-376 buds. Ptant Physiol. 54, 29-35 Junttila O. & Stushnoff C. (1977) Freezing Gilmour S.J., Hajela R.K. & Thomashow M.F. avoidance by deep supercooling in hydrated let- (1988) Cold acclimation in Arabidopsis thalia- tuce seeds. Nature 269, 325-327 na. Plant Physiol. 87, 745-750
Kacperska A. (1985) Biochemical and physio- Robertson A.J., Gusta L.V., Reaney M.J. & lshi- kawa M. (1988) Identification of proteins corre- logical aspects of frost hardening in herbaceous lated with increased freezing tolerance in bro- plants. In: Plant Production in the North. (Kaurin A., Junttila O. & Nilsen J., eds.), Norwegian megrass (Bromus inermis Leyss. cv. Manchaf) Univ. Press, Oslo, pp. 99-115 cell cultures. Plant Physiol. 86, 344-347 5 Sakai A. (1978) Low temperature exotherms of Kaurin A, Junttila O. & Hansen J. (1981) Sea- winter buds of hardy conifers. Plant Cell Phy- sonal changes in frost hardiness in cloudberry siol. 19, 1439-1446 (Rubus chamaemorus) in relation to carbohy- drate content with special reference to sucrose. Sakai A. & Larcher W. (1987) Frost survival of Physiol. Plant 52, 310-3144 plants. In: Ecological Studies, Vol. 62, Springer Verlag, Berlin, pp. 340 Koski V. (1985) Adaptation of trees to the varia- Skre O. (1979) The regional distribution of vas- tion in the length of the growing season. In: Plant Production in the North. (Kaurin A, Junttila cular plants in Scandinavia with requirements for high summer temperatures. Norw. J. Bot O. & Nilsen J., eds.), Norwegian Univ. Press, 26, 295-318 8 Oslo, pp. 267-276 Steponkus P.L. (1984) Role of plasma mem- Lazar M.D., Chen T.H.H., Gusta L.V. & Kharta brane in freezing injury and cold acclimation. K.K. (1988) Somacional variation for freezing Annu. Rev. Plant PhysioL 35, 543-584 tolerance in a population derived from Norstar winter wheat. Theor. Appl. Genet. 75, 480-484 Strand M. (1987) Photosynthetic responses of seedlings of Scots pine (Pinus sylvestris L.) to Levitt J. (1980) In: Responses of Plants to low temperature and excessive light. Ph.D. Environmental Stresses. 2nd edn. Vol. I. Acade- Thesis. Univ. of Umeå, Umea. ISBN 91-7174- mic Press, New York 308-1 Lindow S.E. (1983) The role of bacterial ice Strom A.R., Falkenberg P. & Landfald B. (1986) nucleation in frost injury to plants. Annu. Rev. Genetics of osmoregulation in Escherichia coli: Phytopathol. 21, 363-384 uptake and biosynthesis of organic osmolytes. FEMS Microbiol. Rev. 39, 79-86 Lindow S.E., Arny D.C. & Upper C.D. (1978) Distribution of ice nucleation active bacteria on Stushnoff C., Junttila O. & Kaurin A (1985) plants in nature. Appl. Environ. Microbiol. 36, Genetics and breeding for cold hardiness 831-838 in woody plants. In: Plant Production in the North. (Kaurin A., Junttila O. & Nilsen J., eds.), Lucas P.W., Cottam D.A., Sheppard L.J. & Norwegian Univ. Press, Oslo, pp. 141-156 Francis B.J. (1988) Growth responses and delayed winter hardening in Sitka spruce follow- Sundbom E., Strand M. & Hdllgren J.E. (1982) Temperature-induced fluorescence changes. A ing summer exposure to ozone. New Phytol. screening method for frost tolerance of potato 108, 495-504 (Solanum sp.). Plant Physiol. 70, 1299-1302 Norell L., Eriksson G., Ekberg 1. & Dormling I. Vertucci C.W., Stushnoff C. & Towill L.E. (1988) (1986) Inheritance of autumn frost hardiness in The loss of &dquo;vital&dquo; water contributes to differ- Pinus sylvestris L. seedlings. Theor. Appl ences in apple bud hardiness. Plant Physiol. Genet. 72, 440-448 Suppl. 86, 38 Oquist G. low (1987) Light at stress von Fircks H.A. (1985) Frost hardiness of fast- temperature. In: Photoinhibition. (Kyle D.J., growing Salix species. In: Plant Production in Osmond C.B. & Arntzen C.J., eds.), ’Elsevier the North. (Kaurin A, Junttila O. & Nilsen J., Science Publishers B.V., Amsterdam, pp. 67-87 eds.), Norwegian Univ. Press, Oslo, pp. 199- Paton D.M., Slattery H.D. & Willing R.R. (1979) 204 Low root temperature delays dehardening of Weiser C.J. (1970) Cold resistance and injury in frost resistant Eucalyptus shoots. Ann. Bot. 43, woody plants. Science 169, 1269-1278 123-124 Wareing P.F (1956) Photoperiodism in woody Quamme H.A. (1985) Avoidance of freezing plants. Annu. Rev. P/anf Pnys/o/. 7,191-214 4 in woody plants by deep supercooling. injury Watanabe M., Makino T., Okada K., Hara M., Acta Hortic. 168, 11-27 Watabe S. & Arai S. (1988) Alkylbenzyldi- Repo T. & Pelkonen P. (1986) Temperature step methyl-ammonium salts as inhibitors for the ice response of dehardening in Scots pine seed- nucleating activity of Envinia ananas. Agric. lings. Scan. J. For. Res. 1, 271-284 Biol. Chem. 52, 201-206