Current state of cold hardiness research on fruit crops · Current state of cold hardiness research...

Current state of cold hardiness research on fruit crops

Pauliina Palonen1 and Deborah Buszard2

1University of Helsinki, Department of Plant Production, P.O.Box 27, FIN-00014 University of Helsinki, Finland;2McGill University, Department of Plant Science, Macdonald Campus, 21,111 Lakeshore Road, Ste-Anne-de-

Bellevue, Quebec, Canada H9X 3V9. Received 12 February 1996, accepted 13 December 1996.

CONTENTS

Abstract 399Resumé 399Introduction 400General 400Research Techniques 400Apple (Malus × domestica) 401Pear (Pyrus spp.) 403Peach, nectarine, apricot and cherry (Prunus spp.) 404

Palonen, P. and Buszard, D. 1997. Current state of cold hardiness research on fruit crops. Can. J. Plant Sci. 77: 399–420. Thisarticle gives an overview of the current state of cold hardiness research in fruit crops by reviewing the recently published studieson cold hardiness of both tree fruit and berry crops. Topics discussed include cold hardiness of fruit species, cultivars and differ-ent plant organs, biophysical and biochemical aspects of hardiness, evaluation of hardiness, as well as endogenous, cultural andenvironmental factors affecting cold hardiness in these species. Lack of cold hardiness is a major limiting factor for production offruit crops in many regions of the world and improved cold hardiness one of the major objectives in numerous breeding programsand research projects. Screening cultivars or selections for cold hardiness is commonly done, and different methods applied to theevaluation of hardiness are discussed. The physical limit of deep supercooling may be a restricting factor for expanding the pro-duction of some fruit crops, such as Prunus species and pear. As for biochemical aspects, a relationship between carbohydratesand cold hardiness is most commonly found. Studies have also been made on different hardiness modifying cultural factors includ-ing rootstock, crop load, raised beds and application of growth regulators. The latter seems promising for some species. Cold har-diness is an extremely complex phenomenon and understanding different mechanisms involved is critical. Since hardiness is,however, primarily affected by genotype, developing cold-hardy fruit cultivars and effective screening methods for hardiness areessential. Finally, cultural practices may be improved to further enhance hardiness.

Key words: Berries, cold hardiness, fruits, small fruits, stress, winter hardiness

Palonen, P. et Buszard, D. 1997. Où en est la recherche sur la résistance au froid chez les cultures fruitières?. Can. J. PlantSci. 77: 399–420. A partir de publications récentes concernant les arbres de verger et les petits fruits les auteurs font le point surl’état actuel de la recherche sur la rusticité hivernale des cultures fruitières. Les aspects examinés comprennent 1) les différencesde rusticité selon l’espèce, le cultivar et les différents organes des plantes, 2) les aspects biophysiques et biochimiques en cause,3) les méthodes d’évaluation de la rusticité hivernale et enfin 4) les effets éventuels des facteurs culturaux et environnementauxchez les diverses espèces. Le manque de résistance au froid est un des principaux facteurs limitants de la production fruitière dansde nombreuses régions du globe, il est donc normal que l’amélioration de ce caractère soit un des premiers objectifs de beaucoupde programmes de sélection et de recherche. L’article passe en revue les méthodes courantes de sélection des obtentions et les dif-férentes méthodes d’évaluation de la rusticité. Un des obstacles à l’expansion de la production de certaines espèces fruitières,notamment les Prunus et la poire, serait lié á un phénomène de surfusion interne. Parmi les aspects biochimiques, le rapport entreles concentrations de sucre de la sève et la rusticité est celui le plus souvent constaté. On relève également des travaux sur les dif-férents facteurs culturaux susceptibles d’influer sur la résistance au froid : le choix du porte-greffe, la charge fruitière, la cultureen billon et l’application de régulateurs de croissance. Ces derniers semblent avoir de l’avenir pour certaines espèces. La résistanceau froid est un phénomène d’une extrême complexité, d’où l’importance cruciale d’en élucider les divers mécanismes. Comme lecaractère dépend en premier lieu du génotype, l’amélioration génétique demeure un outil essentiel, assorti de méthodes efficacesde tri et d’évaluation. Enfin, il y a encore place pour l’amélioration des pratiques culturales.

Mots clés: Petits fruits, résistance au froid, fruits de verger, stress, rusticité hivernale

temperature exotherm; NMR, nuclear magnetic resonance;PNA, Pacific/North America; r-PNA, reverse Pacific/NorthAmerica; RFO, raffinose family oligosaccharides; TTC,tetrazolium chloride test

399

Abbreviations: ABA, ; DN, day neutral; DTA, differen-tial thermal analysis; EC, electrical conductivity of diffusedelectrolytes; FDA, fluorescein diacetate; ENSO, El Niño/Southern Oscillation; INA, ice nucleation active; LTE, low

Brambles (Rubus spp.) 407Strawberry (Fragaria × ananassa) 409Blueberry (Vaccinium spp.) 411Cranberry (Vaccinium macrocarpon) 412Currants (Ribes spp.) 412Grapes (Vitis spp.) 414Summary 415References 416

HORTICULTURE SECTION

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400 CANADIAN JOURNAL OF PLANT SCIENCE

Lack of cold hardiness is a major limiting factor for produc-tion of fruit crops in many regions of the world. Low-tem-perature injuries cause serious economic losses. In Canada,major losses of tender fruit trees are estimated to occur onceor twice every 5–10 yr depending on type of fruit and loca-tion (Brown and Blackburn 1987). Injuries to fruit trees areassociated with either low fall or winter temperatures whichkill trees or fruit buds, or with late spring frosts duringbloom.

Cold hardiness of plants is a complex phenomenon, and isaffected by temperature, daylength and conditions of aplant, such as maturity, water content, nutritional stage,physiological age and dormancy status (Stushnoff 1972).The maximum intensity of cold hardiness alone is not oftencrucial for survival. Time and rate of development of hardi-ness, retention of hardiness, time and rate of dehardeningand ability to reharden, all contribute to winter hardinessand survival of a plant. This also makes evaluation of coldhardiness difficult. Research papers often deal with only oneaspect of cold hardiness, such as mid-winter hardiness, butthe early and late stages of cold acclimation are equallyimportant. Also, breeders should pay attention to this whenscreening new plant material for cold hardiness.

Improved cold hardiness is one of the major objectives innumerous breeding projects throughout the world. Insteadof relying on natural selection following test winters, breed-ers use artificial cold stress selection methods to acceleratebreeding processes. Many breeding programs have beensuccessful in developing new cold hardy cultivars; hardyblueberries and grapes bred in Minnesota are an example(Luby 1991). The availability of cold hardy genotypes iscrucial for success in breeding. Germplasm maintenanceand evaluation, as well as collection and evaluation of wildgermplasm is of great importance.

Management and cultural techniques have been devel-oped which allow the production of sensitive crops in somecold areas, although the risk of injury is ever present. In thelong term, breeding new cultivars with improved hardinessoffers the best hope of success. Thus, it is important to eval-uate the complex processes of hardening and frost resis-tance, and the mechanisms involved.

This paper aims to give an overview of the current stateof cold hardiness research in fruit crops. Recently publishedstudies on cold hardiness of tree fruit and berry cropsincluding apple, pear, peach, nectarine, cherry, brambles,strawberry, blueberry, cranberry, currants and grape arereviewed. The emphasis is on more recent research but olderstudies have been included where they make a significantcontribution.

GENERALThe phenomenon of deep supercooling occurs in manydeciduous fruit crops, such as apple, apricot, blackberry,blueberry, cherry, grape, peach, pear, plum and raspberry(Quamme 1991). Most of these crops exhibit deep super-cooling in xylem tissues, and many in flower buds. Whentemperature is further lowered, the deep supercooled waterfinally freezes resulting in lethal injury to the tissue.Freezing of water releases heat causing a low temperature

exotherm (LTE), which can be detected by differential ther-mal analysis (DTA). Xylem hardiness can be estimated byDTA. Also, in dormant buds of many fruit species, the initi-ation point of the LTE indicates lethal injury to flower pri-mordia. The flower buds of apple and pear are an exception;they do not exhibit a LTE. However, vegetative bud hardi-ness and bark hardiness, which are considered to be morecrucial to survival, can not always be determined by thermalanalysis. Limited capacity to deep supercool restricts therange of many fruit crops. Given the current desire toexpand the production of these crops into colder regions, animproved knowledge of the mechanisms involved in deepsupercooling is desirable (Quamme 1991).

Ashworth and Wisniewski (1991) described how varioustissues of deciduous fruit trees respond to low temperatures.Low-temperature responses vary between different tissueswithin the same plant. Xylem tissues exhibit deep super-cooling while bark tissue undergoes extracellular freezing.Despite these different survival strategies both cell typesexhibit analogous seasonal changes in cell fine structure. Inflower buds, extra-organ freezing occurs; ice crystals growwithin the bud scales and the lower portion of axis tissue,but no ice is observed within developing floral organs. Inapple and pear, water is withdrawn from floral organs to theice crystals within the scales and axis, and buds are exten-sively dehydrated. In other species, such as grape, blueberryand several Prunus species, only a part of water is with-drawn, and the remaining undergoes supercooling.

RESEARCH TECHNIQUESStudying cold hardiness of woody plants is complicated,because freeze injury occurring in the field usually onlybecomes visible in spring when growth commences. Arange of different methods can be used to evaluate injuryafter artificial freezing in controlled conditions. Accordingto Stushnoff (1972), the most frequently used methods are1) regrowth test, 2) visual rating of injury, 3) electrical con-ductivity of diffused electrolytes (EC), 4) colour reactiontests, such as tetrazolium chloride test (TTC), 5) impedancemeasurement of intact tissues, and 6) exotherm analysisincluding DTA. Chlorophyll fluorescence measurement ofleaves has also been used (Brennan and Jefferies 1990).

The reliability of these methods depends on plant speciesand experimental conditions. They often give slightly dif-ferent lethal temperature (LT50) estimates. Visual rating ofinjury and EC of diffused electrolytes are the most fre-quently used methods for freeze injury assessment. The use-fulness of the TTC test is limited. One of the newermethods, electrical impedance measurement, appearspromising and has the advantage that it can be used withoutfreezing the plant material (Coleman 1989; Privé and Zhang1996). Chlorophyll fluorescence measurement may providea screening method for spring frost hardiness, as has beenreported for black currant by Brennan and Jefferies (1990).

In some cases, lethal temperatures cannot be estimatedusing LTEs detected in DTA. For example, LTEs in blue-berry stems are associated with xylem injury, but none ofthe LTEs is associated with injury to bark, which occurs ata much higher temperature (Quamme et al. 1972b).

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PALONEN AND BUSZARD — COLD HARDINESS RESEARCH ON FRUIT CROPS: REVIEW 401

Controlled freezing tests may also have a pitfall: blueberryflower primordia do not supercool under natural conditions,but water is withdrawn from the floret (Flinn and Ashworth1994). LTEs are, however, observed at faster cooling ratesin artificial freezing, and are probably caused by the exper-imental procedure rather than reflect natural conditions.

As an aid to studying freezing in a controlled environ-ment, Wample et al. (1990) described a computerized sys-tem that controls freezing rate at variable rates oftemperature decline and can collect, store and analyze datafrom multiple samples in LTE analysis. Wisniewski et al.(1990) described a microcomputer-based DTA system.Different freezing rates can be produced by programmingaluminium block heat sinks independently. Each sink con-tains five samples. Exotherms from both floral buds andxylem tissue can be detected by the system. Khanizadeh(1991) described an application of a computer software pro-gram for temperature regulation in a controlled environ-ment. It can control and record the temperature of theenvironment at selected time intervals. According toBrennan et al. (1993), nuclear magnetic resonance (NMR)imaging could be used to study the freezing events in blackcurrant flowers.

According to Lindén et al. (1996), logit models offer auseful alternative for analysis of qualitative freeze survivaldata. Major benefits are that LT50 is easily estimated withconfidence intervals, and that the effects of explanatoryvariables can be evaluated using model coefficients andodds ratios.

APPLE (MALUS 3 DOMESTICA)Apple trees (Malus × domestica Borkh.) suffer frequentlyfrom cold winter temperatures. In both British Columbiaand eastern Canada, severe freezes that kill apple trees orlower yields, occur every 5–7 yr (Coleman 1992; Hall andQuamme 1994). A severe winter in 1980–1981 caused sig-nificant apple tree losses in eastern Canada. For example, inQuebec about 25–30% of the apple trees either died or wereseverely injured (Brown and Blackburn 1987). The mostcommon low-temperature injury to apple trees is blackheartinjury, browning of the xylem tissue.

1. Cold Hardiness1.1. Cold Hardiness of Species, Cultivars and RootstocksIn South Sweden, frost damage to 129 apple cultivars wasstudied after a severe frost in April, which occurred whenapple flower buds were in the early tight cluster stage(Nybom 1992). Variation in injury was almost negligiblewithin cultivars, whereas between cultivars large variationswere observed. Early-flowering cultivars were more seri-ously damaged than late-flowering ones. Interestingly, arelationship was found between frost hardiness of flowerbuds and country of origin. Winter hardiness estimation ofcultivars from other studies reportedly did not correlate withthe bud injury data from this study. Flower bud hardinessdoes not seem to correspond to hardiness of woody tissue.Thus, cultivars that are extremely hardy in a continental cli-mate, may be subject to severe flower bud injury in latespring frosts of more variable maritime climates.

Imperial Red Mac/Antonovka was the hardiest andImperial Red Mac/MM.111 the most tender cultivar root-stock combination among nine apple cultivars studied in NewBrunswick by Coleman (1985). In March, LT50 for xylem tis-sue of apple cultivars Antonovka and Samo grown inSouthern Finland were –46 and –43°C, respectively (Lindénet al. 1996). Hardening treatments failed to increase the resis-tance of either cultivar, but dehardening at –14°C decreasedthe resistance by 12–15°C. The authors concluded that bothcultivars were close to their maximum possible hardiness.

In a study of Embree (1988), both root and trunk hardi-ness were greatest in rootstocks M.26, Ottawa 3 (O.3) andAlnarp 2 (A2). Also, root hardiness was good in rootstocksBudagovsky 118 (B.118), Budagovsky 490 (B.490) and aPolish rootstock (P.1), and trunk hardiness in BeautifulArcade. According to Quamme (1990), M.26 rootstock ishardier than M.9, whereas Callesen (1994) reported thatthey are equal in hardiness, but both agree that M.26 ishardier than MM.106. According to Aaltonen (1995), themost commonly used apple rootstocks in Finland, A2 andYltöinen Piikkiö (YP), do not differ in winter hardiness,both having an acceptable hardiness.

Root hardiness of several apple rootstocks and trunk har-diness of a tender and a hardy cultivar were compared byEmbree and McRae in 1991. Root survival did not differbetween the scions, but root regrowth of the tender cultivarGravenstein was greater than that of the hardy cultivarWealthy. Trunk survival was dependent on the rootstock.The results provide some evidence for the occurrence of rec-iprocal effects; that the rootstock may have an effect ontrunk hardiness and the scion an effect on root hardiness.Cultivars Sturdeespur Delicious and Empire with M.9 inter-stem had less scion and interstem wood injury on MM.111rootstock than on Antonovka and Ottawa 11 rootstocks(Domoto 1986). Frost damage evaluated as tip die-back ofbranches was worse on trees grafted on MM.106 rootstockthan on those grafted on M.9 or M.26 rootstocks (Callesen1994). Blackheart injury of Starkspur Supreme Deliciousapple trees growing on different rootstocks in different loca-tions in North America was evaluated by Warmund et al.(1996). Generally, trees on B.9, P.2, P.16 and P.22 weremore susceptible to blackheart injury than those on B.490,MAC.1, C.6 and MAC.39.

1.2. Cold Hardiness of Plant Parts and OrgansBud and bark tissues of apple are hardier than xylem in mid-winter, but in early autumn and late spring xylem and pithare hardier than buds and bark (Quamme et al. 1972a).Xylem becomes injured at –35 to –40°C, which is related tothe initiation of LTE and to minimum temperatures atNorthern limits of commercial production (Quamme 1976).Injury occurs in the shoot interior and spreads radially out-wards, the secondary xylem being most cold resistant(Ketchie and Kammereck 1987). Even if more than 50% ofthe xylem exhibits blackheart injury, it is possible for a treeto recover (Warmund et al. 1996). In the fall, hardening pro-ceeds from terminal shoots downwards; thus the lower partof the trunk is the last part to harden and the least cold tol-erant part of the tree.

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2. Physiology of Cold Hardiness2.1. Biophysical aspects of cold hardinessApple stem xylem ray parenchyma and pith cells avoidfreezing by deep supercooling, whereas bark tissue andflower buds do not deep supercool (Quamme 1976, 1991;Ashworth et al. 1988; Malone and Ashworth 1990). Cellcollapse next to voids formed by extracellular ice crystalswas observed in apple bark tissue, but did not occur inxylem ray parenchyma or pith tissues (Ashworth et al. 1988;Malone and Ashworth 1990). Cell collapse throughout thebark was not uniform (Ashworth et al. 1988). The reductionin cell volume following cell collapse was greater in corticalcells than in the cells in periderm, phloem and cambium.Ristic and Ashworth (1995) used freeze substitution andTEM to study the response of apple xylem ray parenchymacells to freezing stress. Two distinct responses wereobserved: formation of intracellular ice or fragmented pro-toplasm with indistinguishable cell ultrastructures, but therewas no evidence of intracellular ice formation. Apparently,injury to xylem can be caused either by intracellular ice orby cavitation.

Vertucci and Stushnoff (1992) studied the interactionbetween sensitivity to desiccation and the presence ofunfreezable water in acclimating vegetative apple buds.Buds were most hardy in January, and this characteristicwas associated with maximum tolerance to desiccation. Theamount of unfrozen water correlated with hardiness. In budsthat survived –45°C, the intracellular water content wasreduced, but sufficient moisture content to avoid desiccationdamage was maintained. Vertucci and Stushnoff (1992)concluded that hardening of vegetative apple buds includesan increase in tolerance to dehydration and an increase inthe quantity of unfreezable water in the cell. According toQuamme et al. (1982a), the dehydration resistance in applewood may involve both nonliving and living elements of thewood.

According to Faust et al. (1991), converting water in budsfrom bound to free form is involved in satisfying the chill-ing requirement. When water is absent during dormancy,apple buds are endodormant, and when water is in a freeform, buds are ecodormant. Faust et al. (1995) used mag-netic resonance imaging to estimate the amount of boundversus free water in dormant vegetative buds of two applecultivars differing in their chilling requirement. Beforechilling exposure most of the tissue water was in the boundstate. Bound water was converted to free water incremental-ly during chilling, the rate of change being cultivar depen-dent. Before growth is resumed, about 70% or more of thewater is in a free state. This required 400 h of chilling inbuds of the cultivar Anna and 3000 h of chilling in buds ofthe cultivar Northern Spy.

Ultrastructural changes in cortical cells of apple (Maluspumila Mill.), associated with cold hardiness were studiedby Kuroda and Sagisaka (1993). During cold acclimation,the volume of cytoplasm increased and microvacuolationoccurred. Organelles involved in protein synthesis, such asER, polysomes, vesicles and dictyosomes became temporar-ily abundant both during acclimation and deacclimation.With maximum cold hardiness, starch granules disappeared.

During deacclimation, the changes observed were thereverse of those observed during acclimation.

2.2. Biochemical aspects of cold hardinessDuring cold acclimation, membrane lipids and proteinsundergo changes that alter the physical behaviour of theplasmalemma. Specific activity of plasmalemma ATPasewas found to increase during cold acclimation in apple barktissues (Mattheis and Ketchie 1990). However, according tothe authors, enhanced low temperature metabolism ratherthan frost hardiness itself may account for these changes inATPase activity.

Cold hardiness of Red King Delicious apple tree shootswas related to high levels of sorbitol in the sap, and to highlevels of sucrose and total sugars in bark and wood (Raeseet al. 1978). According to Stushnoff et al. (1993), cold har-diness in Red Delicious apple cortical tissues and buds cor-related with sorbitol, total sugars and raffinose familyoligosaccharides (RFO), but contrary to Raese et al. (1978),not with sucrose. Khanizadeh et al. (1989, 1992) studied theeffect of crop load on hardiness, carbohydrate, protein andamino acid content of apple flower buds. The absence offruit in the previous year increased the cold hardiness ofbuds. Water-soluble reducing sugar content increased inapple flower buds from July to April-May, and starchincreased during cold acclimation and decreased during latewinter and early spring. Deblossomed trees had higher con-tents of glucose, sorbitol and starch in flower buds, than nor-mally cropped trees (Khanizadeh et al. 1989). Also, thecontents of hydrophilic and acidic amino acids fromOctober to April were found to be higher in the flower budsof non-cropped trees (Khanizadeh et al. 1992).

Coleman et al. (1992) studied the effects of temperatureon cold hardiness and carbohydrates separately by usingplant growth regulators that alter the cold hardiness and car-bohydrate status of apple shoots. A mixture of paclobutra-zol, thidiazuron and flurprimidol was used. Treatmentgenerally increased the hardiness of shoots, but the contentsof sucrose or sorbitol in bark or wood were not related tohardiness levels. Air temperature had a clear effect on shoothardiness, but to a much lesser degree on carbohydrate con-tents. Results indicate that the temperature effects on sor-bitol or soluble sugar contents and on hardiness may beindependent, and can be experimentally separated by apply-ing growth regulators.

When in vitro MM.106 apple shoot cultures were grownon media with elevated concentrations of sucrose (3–14%),they had reduced shoot moisture content and were up to 6°Chardier than control shoots (Caswell et al. 1986). Whetherhardening was caused by enhanced sucrose uptake of plantsor by osmotic stress, was not determined.

3. Evaluating Cold HardinessKetchie et al. (1972) found a close correlation between elec-trolyte leakage and survival of apple seedlings after naturalfrost. Apple bud survival was evaluated by visual observa-tion, forcing and grafting by Spotts and Chen (1984). Testresults from all these methods agreed to within 2.9°C.However, the forcing method for viability testing after

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freezing is generally prefered. Root hardiness of apple root-stocks and trunk hardiness of cultivars were compared usingtwo methods, tissue examination and regrowth measure-ment by Embree and McRae in 1991. The regrowth mea-surement used less labour and was found to be moreobjective than tissue examination. Calculating the ratio ofdiscoloured xylem to total xylem area on a weight basis, wasfound to be a useful method in comparing the amount ofblackheart injury among apple trees grafted on differentrootstocks (Warmund et al. 1996).

Four exotherms were detected in apple twigs (Quamme etal. 1972a). The fourth exotherm arose from the xylem andpith tissues and was associated with lethal injury to xylemray and pith parenchyma (Quamme et al. 1973, 1982a).Ketchie and Kammereck (1987), also observed fourexotherms, but according to them, the third exotherm arosefrom the xylem and indicated injury to xylem. The third andfourth exotherms emerged during maximum hardiness inmidwinter.

Electrical impedance measurement can be used to predicthardiness in apple wood throughout the winter period with-out freezing the material (Coleman 1989). By detectingchanges in the cell wall fluids, impedance test reflectschanges in membrane permeability of complex tissues.Privé and Zhang (1996) compared TTC, vital staining, ECand electrical impedance (Z) in assessing freezing injury ofBeautiful Arcade field vs. cold stored roots. Electricalimpedance was found to have the best ability to detectchanges in cell viability with increasing cold stress, TTChaving the worst. Z provided more detailed information thanEC or TTC about the response of the roots to cold stress, andit may also provide some insight into freeze-thaw historybefore injury assessment.

4. Factors Affecting Cold Hardiness4.1. Endogenous Cold hardiness of apple buds depends on the stage of dor-mancy (Spotts and Chen 1984; Coleman 1985). Accordingto Ketchie (1985) cold resistance of xylem and bark of appletrees is related to both temperature and physiological stage,while cold resistance of leaves is more related to age thanany other factor. Late-maturing cultivars suffered moredamage in Eastern Canada during a severe winter in1980–1981 than early-maturing ones (Brown and Blackburn1987). The absence of fruit in the previous year was foundto increase the cold hardiness of apple buds (Khanizadehet al. 1992).

4.2. Cultural and environmental Growing Lobo and Transparent Blanche apple trees onraised beds covered with black plastic improved their wintersurvival, probably because of the improved moisture condi-tions and soil temperature compared with flat beds (Säköand Laurinen 1986). Quamme and Brownlee (1989) report-ed that apple trees closest to sprinklers suffered less winterinjury to roots than those more distant from sprinklers.Probably low temperatures developed in dry regions of thesoil because of its lower heat capacity, resulting in rootinjury.

Hall and Quamme (1994) discussed the climate effects onapple trees in the Okanagan Valley, British Columbia. Therelationships of temperature, precipitation and winterfreezes to Pacific/North America (PNA) and ElNiño/Southern Oscillation (ENSO) weather patterns wereinvestigated. The PNA weather pattern is pronounced onlyin winter. Also a reverse PNA (r-PNA) pattern may occur.The ENSO is the best known teleconnection in the world.An r-PNA pattern combined with either a neutral or a coldevent ENSO was related to the occurrance of fall and winterfreezes. The authors concluded that the risk for winterfreezes is low during ENSO warm events and high during anr-PNA pattern.

Kaukovirta and Syri (1985) analysed winter injury toapple trees in Finland during this century, and Coleman(1992) in New Brunswick, in an attempt to identify the envi-ronmental variables that lead to winter injury, and to providea classification that would allow winter injury to be predict-ed. In both studies, the most important factor affecting theoccurrence and severity of winter injury was mild weatherduring mid-winter, especially February, followed by lowtemperatures. According to Coleman (1992), low tempera-ture itself in December, January and February did not causeinjury, whereas Kaukovirta and Syri (1985) concluded thatsevere frosts during November and December destroyflower and leaf buds and prolonged spells of severe frostinjure xylem tissue. Also higher than average mean air tem-peratures in October, during the hardening-off process con-tributed to the incidence of injury in New Brunswick(Coleman 1992).

Mildew infected terminal apple buds were less hardy thanhealthy buds (Spotts and Chen 1984). This may be due todrying of bud scales in infected buds, which may influencetheir freezing pattern.

4.3. Growth regulatorsCold hardiness of apple trees can be influenced by growthregulators. Autumn foliar application of 2000 ppm paclobu-trazol increased the fruit set of Vista Bella apple, and maybe used for spring frost protection (Kolodziejczak andHamer 1985). Alar-85 and Dupont surfactant WK reducedfreezing injury to Spur Mac/MM.111 apple, even thougheffects were not consistent from year to year (Coleman andEstabrooks 1985). Thidiazuron with or without VaporGardapplied in September increased cold hardiness of SpurMac/MM.106 apple trees (Coleman and Estabrooks 1988).A mixture of paclobutrazol, thidiazuron and flurprimidolgreatly increased hardiness of shoots throughout the fall,winter and spring. The pattern of seasonal changes in hardi-ness level was not affected, although treated shoots wereless sensitive to temperature fluctuations during the winterperiod (Coleman and Estabrooks 1992).

PEAR (PYRUS SPP.)Due to its limited cold hardiness, pear cultivation is restrict-ed to middle regions of North America (Quamme 1976).The nucleation temperature of supercooled water in pearxylem is related to minimum temperatures in the northernlimit of pear production (Quamme 1976, 1977). Physical

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limits of deep supercooling may impose a physiological bar-rier to improving cold hardiness of pear and the expansionof its production.

1. Cold Hardiness1.1. Cold hardiness of species, cultivars and rootstocksAccording to Granger (1982), it would be possible to estab-lish a local pear industry in Quebec, Canada using coldresistant cultivars with acceptable commercial value, suchas Flemish Beauty, Clapp’s Favorite, Miney, Parker andGuyot. The most cold hardy cultivars tested in Quebec wereGaspar and Moe (Granger and Rousselle 1984). CultivarsFlemish Beauty and Harrow(HW)601 were very hardy atone test location but only fairly hardy at the other. CultivarsBeurre d’Anjou, O.291, Kentville 14-24-15, Phileson,O.301, HW 606, and Harvest Queen were also hardy.Flemish Beauty has, however, been found to be susceptibleto spring frost injury (Lamb 1982). Early-blooming pearcultivars tend to be more severely injured by spring frost,although wide differences between cultivars within date-of-full-bloom classes occur (Lamb 1982).

1.2. Cold hardiness of plant parts and organsAs in apple, xylem is the most susceptible tissue in peartrees, followed by bark and buds (Quamme 1976). Fruitbuds of Abbé Fétel pear were investigated after a cold spell(below –20°C) in January in Italy by Filiti and Neri (1989).The number of tannin cells, and cells with calcium oxalatecrystals in fruit buds was increased by frost. Cellular lysiswas observed in the pith. Injuries extended to the spur at thebud base and parenchyma rays, as well as the bark and theborder layers of phloem. Lamb (1982) found that pistilswere the most commonly injured organs, when survival ofpear blossoms in the “bud burst” to “green cluster” stagewas studied after a –5°C frost.

2. Physiology of Cold Hardiness2.1. Biophysical aspects of cold hardinessPear flower buds do not deep supercool (Quamme 1991).Xylem exhibits deep supercooling and the initiation of LTEin fully hardened twigs is –33 to –38°C, which corresponds toannual temperature minima at northern limits of commercialpear production (–28.9 to –34.4°C) (Quamme 1976, 1977). Instems of P. nivalis (Jacq.), P. cordata ((Desv.) Schneider) andP. elaeagrifolia (Pall.), supercooled water was found in bothxylem and bark tissues (Rajashekar et al. 1982). LTEs detect-ed in flower buds of some Pyrus species were likely to arisefrom the stem tissues associated with the buds.

2.2. Biochemical aspects of cold hardinessWhen suspension-cultured pear (P. communis Bartlett) cellswere cold acclimated at 2°C, changes in soluble extracellu-lar polysaccharides occurred (Wallner et al. 1986).Extracellular accumulation of a relatively small, neutralpolysaccharide was increased, and a larger molecularweight pectic polysaccharide decreased. The decrease in apectic polysaccharide may have been due to inhibition ofsynthesis at low temperatures or to low-temperature-induced degradation. Also, the deposition of callose in the

cell wall was observed, which may stabilize this regionagainst stress induced disturbances.

3. Evaluating Cold HardinessKetchie et al. (1972) found a close correlation between elec-trolyte leakage and survival of pear seedlings evaluatedvisually by tissue browning. According to Quamme (1976),the LTE detected in DTA indicates injury to the xylem.Montano et al. (1987) also reported that the initiation of thefirst LTE corresponded with accuracy of ±3°C to the tem-perature of incipient injury to the xylem in tests.

4. Factors Affecting Cold Hardiness4.1. Cultural and environmental In Bartlett pear trees, bloom delay through evaporative cool-ing reduced hardiness of flower buds and flowers, comparedwith controls at the same floral development stages (Stranget al. 1980).

Montesinos and Vilardell (1989) pointed out the importantrole of Pseudomonas syringae in frost susceptibility of peartrees in Catalunya. Forty percent of the P. syringae strainsisolated from buds were ice nucleation active (Montesinosand Vilardell 1991). Mean nucleation temperatures (NT50) ofdetached flower buds were dependent on population levels ofP. syringae ranging from –2.7 to –6°C. According toProebsting and Gross (1988), however, the population of icenucleation active (INA) bacteria has no influence on frostinjury to pear fruit buds, flowers or fruits, when buds areattached to the stem, because the intrinsic wood-associatedice nucleus is a source of ice nucleation at about –2°C.

4.2. Growth regulatorsIn a study by Ketchie and Murren (1976), polyvinylpyroli-done K-30, glycerol, ethylene glycol and dimethyl sulphox-ide in several concentrations and combinations, applied byterminal feeding, failed to increase the frost resistance of ahardy pear cultivar d’Anjou, but increased the resistance ofthe less hardy cultivar Bartlett.

PEACH, NECTARINE, APRICOT AND CHERRY(PRUNUS SPP.)

The most susceptible tissues of Prunus species avoid freez-ing by deep supercooling, and are injured by temperaturesthat are closely related to the average minimum tempera-tures at the northern limits of their distribution (Quamme etal. 1982b). The degree of deep supercooling may be a limit-ing factor for northern commercial production of thesespecies. In Ontario, low temperatures cause some bud kill inpeach (Prunus persica [L.] Batsch.) every winter (Brownand Blackburn 1987). Wood damage occurs less frequentlyand is usually significant only in temperatures below –25°C.An article on breeding cold hardy peaches and nectarines byLayne (1992) gives a good overview of cold hardiness inthese species.

1. Cold Hardiness1.1. Cold hardiness of species, cultivars and rootstocksArora et al. (1992) studied the seasonal pattern of cold har-diness in bark and xylem in related deciduous and evergreen

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peach genotypes. Deciduous trees acclimated sooner, and ina fully dormant state, the bark and xylem of deciduous treeswere almost 30 and 20°C hardier, respectively, than the barkand xylem in evergreen trees.

Twenty-four peach and fourteen nectarine cultivars werescreened for hardiness after a temperature drop from 5 to–11°C within 12 h on 2 November in Oklahoma (Smith etal. 1994). Fantasia and Sunfre nectarines were least injured.Three nectarine cultivars Armking, Mayfire and Sungemwere killed by the freeze. Of all the peach cultivars evaluat-ed, Sentinel had the least damage, and Sam Houston was theonly peach cultivar of which all the trees were killed. Newpeach cultivars Harson, Harrow Beauty and Harcrest, devel-oped in a breeding program in Ontario, are equal or superi-or to Redhaven in flower bud and xylem hardiness (Layne1989).

Flower bud hardiness in peach is influenced by rootstockthrough its influence on both timing and rate of flower buddevelopment. Redhaven peach bud survival was greatest onCitation and Damas rootstocks, and lowest on GF655-2 andAmandier rootstocks among eight rootstocks studied byBrown and Cummins (1988). The influence of seven root-stocks on flower bud hardiness of Redhaven peach wasevaluated during 2 yr by Durner (1990a). Flower bud sur-vival was influenced by rootstock in both years but mar-ketable yield was affected in only 1 yr. Siberian C rootstockwas superior to all others in both years. The rootstock has aninfluence on both the time and the rate of flower bud devel-opment in peach (Durner and Goffreda 1992). In some cul-tivars, delayed bud development and late bloom avoidedspring frost injury and resulted in an increased yield, whilein other cultivars, no relationship between bloom delay andenhanced yield was found. Harber et al. (1992) found thatrootstock affected the dormancy status of Redhaven peachslightly. However, effects on dormancy were not consistentwith effects on cold hardiness.

For cherry, P. mahaleb (Mahaleb) rootstocks are usuallyhardier than P. avium (Mazzard) (Westwood 1993). Howelland Perry (1990) found sweet cherry (P. avium L.) scioncultivars on the rootstock Colt (P. pseudocerasus × P.avium) less hardy than on either Mazzard or M × M 39(Mazzard × Mahaleb). Scion cultivars on M × M 39 root-stock were hardier than on Mazzard or Mahaleb rootstocks.However, the influence of scion cultivar may still be moreimportant; cultivar Gold was ranked as hardiest when grownon Mazzard and Colt. According to Strauch and Gruppe(1985), Colt was more frost sensitive and responded morereadily to dehardening treatments in February than othergenotypes.

1.2. Cold hardiness of plant parts and organsFlower buds and xylem are the most frost sensitive tissuesin Prunus species (Quamme et al. 1982b). Cold hardiness ofpeaches and nectarines was evaluated following a test win-ter by Layne (1982). There was no correlation betweenflower bud and xylem hardiness, indicating that cold hardi-ness of these tissues may be inhereted independently.However, for 27 apricot (P. armeniaca L.) genotypes,flower bud hardiness seemed to correlate with shoot xylem

hardiness (Layne and Gadsby 1995). On average, shootxylem in midwinter was hardier (LT50 = –35.3°C) thanflower buds (LT50 = –28.7°C).

2. Physiology of Cold Hardiness2.1. Biophysical aspects of cold hardinessFreezing injury to xylem and flower buds of Prunus speciesis avoided by deep supercooling (Quamme 1974, 1978;Ashworth 1982; Quamme et al. 1982b; Ashworth et al.1983). Bark tissues freeze extracellularly, and injury to barkis caused by extracellular ice formation and cellular hydra-tion (Ashworth et al. 1983). The population of INA bacteriadid not affect the temperature at which ice formed in peachshoots (Ashworth et al. 1985), flower buds, flowers or fruitsof several Prunus species (Proebsting and Gross 1988). Anintrinsic non-bacterial wood-associated ice nucleus, whichis the primary source of ice nucleation and limits supercool-ing to about –2°C, has been found in stem tissue of severalPrunus species (Gross et al. 1984; Ashworth et al. 1985;Proebsting and Gross 1988).

In peach flower buds, ice is formed in the bud scales andbud axis, but not in the flower primordium (Quamme 1978).It is proposed that the cuticle or epidermis prevents icenucleation from the surface of the flower primordium, and adry region at the base prevents ice from spreading into theprimordium from the bud axis. In deacclimated peachflower buds exposed to –5°C, ice crystals were alsoobserved within the developing floral organs (Ashworth etal. 1989). Deep supercooling in Prunus flower buds is relat-ed to vascular development (Ashworth 1982, 1984;Ashworth and Rowse 1982; Callan 1990). In supercoolingbuds, procambial cells have not yet differentiated into xylemvessel elements. Thus, the lack of xylem continuity betweenthe primordium and the adjacent tissues is the morphologi-cal feature that allows deep supercooling. When xylem con-tinuity is established during dehardening, buds lose theirability to deep supercool.

In Redhaven and Siberian C peaches, whole bud moisturecontent was not related to supercooling capacity (Quamme1983). This is in accordance with findings of Warmund andGeorge (1990) for brambles. Instead, the water content ofthe flower primordium and vascular traces was related to thelevel of supercooling. Water migrated from these tissues tobud scales and even to the exterior of the bud during freez-ing, and returned after thawing. However, at the same watercontent, the hardy cultivar Siberian C supercooled to lowertemperatures than the less-hardy cultivar Redhaven. Also insweet cherry, the ability to deep supercool was related to thewater content of flower primordia and to a preceding mini-mum air temperature (Andrews and Proebsting 1987). Thepeach flower primordium in dormant buds has a lowerosmotic potential than other parts, possibly as a conse-quence of high sucrose levels (Quamme and Gusta 1987).Lower water potential of the flower primordium may beinvolved in the recovery of water content of flower bud afterfreezing.

The extent of deep supercooling of living and dead flowerbuds of several Prunus species (almond (P. dulcis Mill.),peach, apricot (P. armeniaca L.) and cherry) was examined

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by Kadir and Proebsting (1993). When flower buds werekilled by freezing, the DTA response of the dead flower pri-mordia remained normal for more than 2 wk after the killingfrost, indicating that dead flower primordia retained theirability to supercool. When living buds started to swell, theability of dead buds to deep supercool was decreased andgradually lost. The authors concluded that when a dormantflower primordium is killed by freezing, the growth of icecrystals is prevented, because the tissue water remains com-partmentalized.

The number of LTEs in sweet cherry selections and thecultivar Bing did not always correspond to the number offlorets, the percentage of LTE per primordium being 75 to90% (Kadir and Proebsting 1994). Due to earlier bud devel-opment in spring, flower primordia of tender selectionsceased to supercool first. An increase in the LTE tempera-ture, and an increased variation in LTE temperatures withina bud have been observed in deacclimating flower buds ofsweet cherry (Andrews and Proebsting 1987), and sour cher-ry (P. cerasus L.) (Callan 1990). In sour cherry, all primor-dia within a bud ceased to deep supercool simultaneously(Callan 1990). Callan (1990) associated flower primordiumdeep supercooling after deacclimation with flower budendodormancy, because deacclimated flower primordiaceased to deep supercool earlier when chill unit accumula-tion was accelerated.

According to Andrews et al. (1983), a frost-tolerant peri-od occurs in peach and sweet cherry buds after the ability tosupercool is lost during early bud swell in spring until petaltip emergence. During that period it is possible to reducefreezing injury by increasing the ice nucleating temperature.This was done either by wetting peach flower buds or byinoculating sweet cherry buds with INA P. syringaebacteria.

Despite their different mechanisms of cold hardiness,xylem parenchyma and cortical cells in peach twigs showedsimilar ultrastructural changes associated with changes incold hardiness (Wisniewski and Ashworth 1986). Duringacclimation and deacclimation, plasmalemma infoldingsand complex membrane aggregates were observed. Duringthe period of maximum hardiness in midwinter, cells had acentrally located nucleus, many small vacuoles and nostarch grains.

Schaffer and Wisniewski (1989) studied the developmentof an amorphous layer in the xylem of apple and peach(deep supercooling) and willow (extracellular freezing).They concluded that compositional differences may exist inthis amorphous layer, which leads to the different freezingresponses of these species. Wisniewski et al. (1991) studiedthe effect of externally applied cell-wall-degrading enzymeson the freezing profile and structure of the pit membraneand amorphous layer, and the relationship between theseportions of the cell wall and the ability to deep supercool incurrent year twigs of peach. Macerase, an enzyme mixturerich in pectinase, caused a nearly complete digestion of thepit membrane and partial degrading of the underlying amor-phous layer. Deep supercooling was almost completely pre-vented. Cellulysin caused a digestion of only the outermostlayer of the pit membrane and reduced the ability to deep

supercool. When a sodium phosphate buffer was applied, avery slight decrease in the ability to deep supercool wasobserved. The authors concluded that the pit membranetogether with the underlying amorphous layer form a barri-er to water movement and growth of ice crystals, which is aprerequisite for deep supercooling, and that pectins may reg-ulate the permeability of that portion of the cell wall.

2.2. Biochemical aspects of cold hardinessThe total sugar and soluble protein contents in peach budsare correlated with frost resistance (Lasheen et al. 1970;Burak and Eris 1992), as also reported for apple (Raese et al.1978; Khanizadeh et al. 1989, 1992; Stushnoff et al. 1993).Low total free amino acids were also associated with hardi-ness (Lasheen et al. 1970). Highest total lipid levelsoccurred in February and were concurrent with the lowestair temperatures and the highest bud survival of the peachcultivars (Burak and Eris 1992).

In related deciduous and evergreen peach genotypes sea-sonal changes in protein contents were quite similar in thetwo genotypes (Arora et al. 1992). Cold hardiness was high-ly correlated with seasonal fluctuations of three proteins (19,70 and 80 kDa) in xylem of both genotypes. A 19-kDapolypeptide accumulated in bark of both genotypes duringfall and decreased in spring, but the accumulation was lessin evergreen trees. The accumulation of a 16-kDa proteinwas observed during fall in the deciduous genotype but notin the evergreen type.

3. Evaluating Cold HardinessThe LTE detected in the stem tissue of 13 Prunus speciesand interspecific hybrids was closely related to xylem injury(Quamme et al. 1982b). According to Kadir and Proebsting(1994), the DTA was consistent with visual field observa-tions of hardiness of sweet cherry genotypes and can thus beused for screening populations for floral bud hardiness. Thepossibility of LTE artifacts from dead flower primordia mayaffect the cold hardiness estimations of field collected sam-ples and should be taken into account (Kadir and Proebsting1993). Arora et al. (1992) found a close correlation betweenLTE and LT50 assessed by electrolyte leakage in relateddeciduous and evergreen peach genotypes.

4. Factors Affecting Cold Hardiness4.1. Endogenous Byrne (1986) studied the reasons for the superior fruit set ofTexstar peach under spring freeze conditions. Large num-bers of flowers, long bloom period and late bloom were thefactors contributing to spring freeze injury avoidance.Differences in tissue moisture content explained about one-half of the constant hardiness difference between sweetcherry selections, the other half being associated withunknown factors (Kadir and Proebsting 1994).

4.2. Cultural and environmentalAccording to Seeley et al. (1992), defoliation of trees in latesummer inhibited flower bud hardening and reducedendodormancy intensity, whereas prolonged leaf retentionin the autumn increased the dormancy intensity and extend-

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ed the dormant period. Harber et al. (1992) found that root-stock, time of pruning and soil fumigation affected the dor-mancy status of Redhaven peach slightly. However, effectson dormancy status were not consistent with effects on coldhardiness. Pruning peach trees after rest completion inJanuary reduced flower bud hardiness, because pistils frompruned trees did not reharden after a thaw (Durner 1990b).Whitewashing entire peach trees in January reduced the sizeof pistils, delayed bud development, enhanced flower budhardiness during bloom and enhanced yield, but did notaffect bud hardiness in winter (Durner and Gianfagna 1992).

Lu and Rieger (1993) studied the effect of temperaturepreconditioning on freezing tolerance of fully opened peachflowers. The ovaries of cultivars Junegold and Loring treesgrown in a cold regime were slightly hardier than those oftrees grown in a warm regime. No differences in hardinessof ovaries between cold-grown and warm-grown cultivarRedhaven trees were detected. While leaves and stems ofcold-grown Junegold peach were more than 3°C hardierthan those of warm-grown trees, the difference in the LT50of ovaries was only 0.38°C.

Bloom delay through evaporative cooling increased thehardiness of peach buds until early March, but decreased thehardiness and the number of viable buds by late March(Bauer et al. 1976). Byers and Marini (1994) found thatblossom thinning and fruit thinning of peach trees to mod-erately light crop densities can enhance the cold tolerance offlower buds in late winter. This is in agreement with thefindings of Khanizadeh et al. (1992) for apple. In peach,there was a negative relationship between the percent livebuds after a spring freeze and crop load in the previous sea-son (Byers and Marini 1994). Blossom thinning was moreefficient in enhancing cold tolerance than hand-thinningtrees 38 d after full bloom.

Cytospora canker caused by Leucostoma personii had anegative effect on cold hardiness in peach (Chang et al.1989).

4.3. Growth regulatorsNumerous attempts have been made to increase cold hardi-ness of peach by application of growth regulators. Ethephonapplied in the fall increases the hardiness of peach buds,delays bloom and enhances yield (Durner and Gianfagna1988; Gianfagna et al. 1989). Ethephon enhances flowerbud hardiness and prolongs dormancy of flower buds byincreasing the chilling requirement, thus delaying late win-ter deacclimation and bloom in spring (Durner andGianfagna 1991a). When dormant peach flower buds weretreated with ethephon, buds on ethephon-treated trees grewmore slowly than buds in control trees. Ethephon increasedthe ability of pistils to supercool, increased the number ofbuds that supercooled after deacclimation treatment and alsoretarded deacclimation. These effects were associated withincreased pistil sorbitol and sucrose contents, reduced mois-ture content, pistil size and growth rates during deacclima-tion following ethephon application (Durner and Gianfagna1991b).

Fall application of ethephon (100 ppm) to peach treesdelayed bloom by 6 d, and whitewashing entire trees in

January delayed bloom by an additional 1 to 2 d (Durner andGianfagna 1990, 1992). Flower bud hardiness on ethephon-treated trees was slightly enhanced. In February, the meanLTE was –18.5°C for treated and –17.7°C for non-treatedtrees, but by March, no effects on hardiness were detected.The whitewashing of trees in January delayed pistil elonga-tion in buds from non-ethephon-treated trees, but had noeffect on ethephon-treated buds. Ethephon treatment did notprevent dehardening of pistils of trees pruned after rest com-pletion in January, but it facilitated their rehardening after athaw (Durner 1990b).

Gianfagna (1991) compared the effect of LAB 173711, acompound with ABA-like activity, and ethephon on time offlowering and cold hardiness of peach flower buds. Ingreenhouse experiments, LAB 173711 delayed bloom moreeffectively, when it was applied after a dormancy-breakingtreatment. Ethephon was more effective when appliedbefore the chilling requirement was satisfied, and causedflower bud abscission, if applied after the chilling require-ment was complete. In field experiments, LAB 173711delayed flowering by 2–3 d, but this was not long enough toavoid spring frost injury. Ethephon delayed flowering by6–7 d, and no flower bud injury occurred on treated trees at–4.3°C, while 25% of flower buds in control trees weredamaged at this temperature. According to Blanco (1990),paclobutrazol treatment advanced bloom the year after treat-ment, and at the same time enhanced the flower frost hardi-ness resulting in almost a doubling of yield. Prebloomdormant oil application had no positive effects on peachflower bud hardiness, on the contrary; apparently because ofdecreased blossom hardiness, yield was reduced when com-pared to the control (Durner and Gianfagna 1992).

Seeley et al. (1992) reported that NAA delayed leafsenescence and increased Johnson Elberta peach flower budhardiness, while no hardiness increase was observed foreither Montmorency cherry or Redhaven peach. Decreasedflower size may account for the increased cold hardinessafter NAA treatment. However, GA treatment alsoincreased hardiness to some extent although it did not affectflower size. NAA treatment applied to one side of the treeonly prolonged leaf retention on the treated side, but affect-ed the hardiness of the entire tree. Results provide evidencefor the existence of a translocatable cold-hardiness promot-er produced in leaves under hardening conditions.

Dormex (calcium cyanamid) did not enhance flower budhardiness of peach (Durner and Gianfagna 1988). The effec-tiveness of two commercial low-temperature protectants,Frost-Free (Plant Products, Vero Beach, FL) and Vapor Gard(Miller Chemical & Fertilizer, Hanover, PA) was examined(Aoun et al. 1993). Neither chemical was found to providefrost protection for peach flowers or developing fruits.

BRAMBLES (RUBUS SPP.)Ideal conditions for red raspberry are cool summers andmoderate winters. Despite this, raspberry is grown widely indifferent parts of the world. In colder climates, some loss ofcanes or flower buds usually occurs during winter (canedieback), and injury to buds near the snow line is common(Brown and Blackburn 1987). Because of their late bloom,

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raspberries do not usually suffer from spring frosts.Primocane fruiting cultivars avoid winter injury problems.Blackberry is more susceptible to cold than raspberry.Blackberry canes are injured at temperatures below –23°C(Moore and Skirvin 1990).

1. Cold Hardiness1.1. Cold hardiness of species and cultivarsWinter hardiness of 11 red raspberry cultivars was tested inFinland during a 4-yr trial (Dalman et al. 1991). CultivarVille, which is a cross between cultivar Ottawa and aFinnish wild raspberry strain (Rubus idaeus L.), proved tobe the hardiest, followed by the Canadian cultivars Ottawa,Muskoka and Boyne. The Scottish cultivars Glen Isla andGlen Clova were the most cold sensitive. Red raspberry cul-tivars and selections, including eight indigenous NorwegianRubus idaeus L. populations, were screened for cold toler-ance in Norway (Nestby 1992). In this study, the indigenousR. idaeus selections were no more hardy than the Norwegiancultivars and selections, so they can not be considered as auseful source of potential germplasm for freeze tolerance.

Hummer et al. (1995) screened more than 80 raspberryand 42 blackberry genotypes for cold hardiness with con-trolled laboratory freezing in January. Most red raspberrieswere found to be hardier than black raspberries (R. occiden-talis L.) or blackberries (R. allegheniensis Porter, R. ursinusCham & Schldl.), while purple raspberries (R. neglectusPeck.) were intermediate between red and black raspberries.Burnetholm and Canby were the hardiest red raspberry cul-tivars, their canes having the LT50 values of –34°C and–30°C, respectively. Brandywine and Royalty were thehardiest purple raspberry cultivars. The hardiest blackberrycultivar in this study was Black Satin. Its canes had the LT50value of –23°C and buds –19°C. Warmund and George(1990) found that among 11 blackberry (Rubus subgen.Eubatus) cultivars, floral buds of Darrow were found to bemost hardy, with 45% of the primordia in primary buds sur-viving –33°C in January. In the study of Hummer et al.(1995) Darrow buds only survived –13°C. Among 10 redraspberry (R. idaeus L.) cultivars studied by Warmund andGeorge (1990), Canby and Chilliwack had good primarybud hardiness in January, and they retained their hardinesslonger than other cultivars, which may be associated withtheir longer rest requirement.

Zatylny et al. (1993) studied the cold hardiness of red rasp-berry in vitro. Tissue cultured red raspberry plantlets wereacclimated before controlled freezing. As also reported byWarmund et al. (1989b), the apical meristems were found tobe the most cold hardy, and the older leaves the least coldhardy, when freezing injury was assessed by visual rating oftissue browning. Lowest survival temperatures varied from–12.5°C to –16.0°C for acclimated shoots, and from –11.0°Cto –11.5°C for nonacclimated. Acclimated shoots exhibitedvarietal differences, which correspond to their known rela-tive hardiness in the field. Cultivars in order of decreasinghardiness were Boyne, Gu72, Gu63 and Comox.

1.2. Cold hardiness of plant parts and organsIn most Rubus genotypes studied by Hummer et al. (1995),

canes were about 2 to 15°C hardier than buds. Usually thebud base was less hardy than the bud tissues inside thescales. According to Doughty et al. (1972), the vascular tis-sue at the base of the buds is the most susceptible tissue.Secondary buds of red raspberry and blackberry were foundto be hardier than primary buds (Warmund and George1990). In Shawnee blackberry, phloem tissue was injured atwarmer temperatures than xylem (Warmund and George1989). When the freezing tolerance of micropropagatedRubus plants grown in a greenhouse was tested, it was foundthat older leaves were more susceptible to injury thanyounger leaves (Warmund et al. 1989b). The apical meris-tem was the hardiest plant part surviving at least –8°C.

1.3. Genetics of cold hardinessWhen offspring from 12 raspberry cultivars were examinedin Norway, cultivars Zeva 1, Schönemann 3-6, and II-2LPGgave rise to the highest number of winterhardy progenies(Redalen 1982). In breeding Rubus species in Finland, thegene pools of wild raspberry (R. idaeus L.) have beenexploited to obtain winter hardy selections (Hiirsalmi 1989).Cold hardiness of 12 seedling populations of complexhybrids of tetraploid blackberries was evaluated by Bourneand Moore (1992). Significant population effects werenoted for xylem, phloem and bud cold hardiness. Seedlingpopulations having cultivar Darrow as a parent were gener-ally hardy. Populations having cultivar Brison as a parentwere less hardy, except one population resulting from across between cultivars Brison and Darrow, which had con-sistently good hardiness. The authors conclude that cold har-diness is inherited quantitatively, but that dominance effectsmay also be involved in determining the cold hardiness ofblackberries.

2. Physiology of Cold Hardiness2.1. Biophysical aspects of cold hardinessAccording to Kraut et al. (1986), in Smoothstem andDirksen blackberries, stem tissue does not supercool.However, Warmund and George (1989) found that Shawneeblackberry stem xylem tissue can avoid freezing by super-cooling. The floral primordia in primary buds of both rasp-berries and blackberries are known to survive freezing bysupercooling (Kraut et al. 1986; Warmund et al. 1988, 1992;Warmund and George 1989, 1990). Supercooling has alsobeen observed in some secondary buds of Dirksen black andReveille red raspberry (Warmund and George 1990).Warmund et al. (1992) examined extracellular ice formationin differentiating buds of eastern thornless blackberry.Large extracellular ice crystals did not form in the inflores-cence axis or in developing floral primordia. Instead, extra-cellular voids formed by freezing were observed in thescales surrounding the inflorescence and in the bud axis.Among 10 red raspberry and 11 blackberry cultivars, whole-bud moisture content was not related to supercooling capac-ity, except in cultivar Nordic, which had very large LTEswhen water content was high (Warmund and George 1990).

Only a single freezing event was observed in floral budsof Dirksen blackberry (Kraut et al. 1986). When Darrowblackberry buds were at an early stage of development, only

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one LTE was detected, but when floral differentiation pro-gressed, individual primordia froze independently and asmany as 10 LTEs could be detected (Warmund et al. 1988).However, only one to four LTEs were detected in overwin-tering Black Satin and Hull thornless blackberry buds(Warmund et al. 1992) and one to three LTEs in Shawneeblackberry buds (Warmund and George 1989), indicatingthat several flower primordia froze simultaneously in budsthat had multiple primordia. The possible explanation fordifferent freezing characteristics may be that xylem devel-opment within the raceme of blackberry affects the freezingcharacteristics of floral buds (Warmund and George 1989)as is the case in Prunus (Ashworth 1984).

3. Evaluating Cold HardinessTissue browning was found to be a better screening methodfor freeze injury evaluation of red raspberry in midwinterthan bud growth, which is more accurate and recommendedin late winter when dormancy is extinguished (Nestby1992). The field evaluation of freeze injury in May byobservation of tissue browning is a convenient method andless time consuming than laboratory regrowth tests, but issubject to climatic fluxes.

The LTEs detected in primary buds of blackberry (Rubussubgen. Eubatus), and red raspberry (Rubus idaeus L.) cul-tivars are correlated with freezing injury, but the number ofLTEs and the number of differentiated floral primordia sel-dom correspond (Warmund and George 1989, 1990). Thehardiness of red raspberry buds determined from LTE val-ues did not always correspond to earlier data about culti-vars’ performance in the field (Warmund and George 1990).A LTE detected in stem tissue of Shawnee blackberry esti-mated the temperature of xylem injury with accuracy of±3.2°C, but bark injury was not associated with a LTE(Warmund and George 1989).

4. Factors Affecting Cold Hardiness 4.1. EndogenousIn Cherokee blackberry, rest was found to play a major rolein the deacclimation of both generative and vegetative tis-sues (Warmund et al. 1989a). During dormancy, floral pri-mordia were hardier and did not deacclimate as rapidly in16°C as after cold treatment was fulfilled. Phloem andxylem were also hardier before rest completion than after. Inphloem the rate of deacclimation was slow regardless of thestage of rest, whereas in xylem, deacclimation rate increasedafter rest was completed.

In red raspberry, early growth cessation is positively cor-related with winter hardiness (Jennings et al. 1972; Säkö andHiirsalmi 1980). In three eastern thornless blackberry culti-vars, the retention of leaves in the fall was negatively corre-lated with bud survival (Kraut et al. 1986). However,premature defoliation reduces photosynthetic activity andphotoinduction responses, and decreases mid-winter hardi-ness of stem tissue (Kraut et al. 1986), and bud tissue byreducing sugar and starch reserves (Doughty et al. 1972).Jennings and Cormack (1969) observed that prematuredefoliation prevented the water content of raspberry canesfrom dropping to the low level of untreated plants.

4.2. Cultural and environmentalCultural practices that reduce vegetative growth may offer apossibility to improve winter survival of raspberry canes.Chemical primocane suppression early in the seasonimproved winter survival of Festival, Latham andNewburgh raspberries, which may be due to the reducedlength of primocanes (Buszard 1986). Cane thinning treat-ments were also found to affect winter survival advanta-geously; winter dieback seemed to correlate with canedensity.

The effect of different levels of broadcast and fertigatednitrogen and raised beds on yield and freeze injury of Vetenred raspberry was studied by Nestby and Kongsrud (1993).Fertigation resulted in better exploitation of nitrogen leadingto higher leaf nitrogen content and increased primocaneheight. Freeze tolerance was negatively correlated with canegrowth and with leaf nitrogen content. As also reported forapple (Säkö and Laurinen 1986), raspberry plants on raisedbeds were found to suffer less winter injury than plants onflat beds, which could be an effect of the higher air volumein the soil and thus improved root conditions. Root rot(Phytophtora fragariae var. rubi) infection had no effect oncold hardiness of buds or canes in Willamette raspberry(Bristow and Hummel 1993).

4.3. Growth regulatorsOnly a few of the attempts to improve cold hardiness ofraspberries or blackberries by using growth regulators haveproved successful. Alar (N-dimethylamino succinic acid)(1000 ppm and 2000 ppm) reduced cane dieback of Lathamand Trent raspberries, early application in June or July beingmore effective than later application in August (Granger andHogue 1968). Succinic acid-2,2-dimethylhydrazide appliedas 1000 and 2000 ppm sprays during growing season had noeffect on bud survival or yield of Trent and Canby raspber-ries (Craig and Aalders 1973). ABA and benzyladenineincreased the regeneration ability of Malling Promise canesafter frost injury (Zraly 1978).

Veten red raspberries treated with 1500 ppm paclobutra-zol had an earlier growth cessation, leaf fall and entered thedormant state early; however, paclobutrazol had little or noeffect on winter injury (Maage 1986). Ethephon (1500 ppm)or ethephon with CaCl2 (2%) also hastened leaf abscissionof three eastern thornless blackberry cultivars, but had noeffect on shoot dieback or yield (Kraut et al. 1986).Mefluidide spray (5 mg L–1) did not enhance cold hardinessof 7-cm-tall micropropagated Shawnee blackberry plantsgrown in a greenhouse and exposed to controlled freezing(Warmund et al. 1989b).

STRAWBERRY (FRAGARIA 3 ANANASSA)Strawberry (Fragaria × ananassa Duch.) is a semihardyevergreen and has relatively low tolerance to cold tempera-tures. It is widely grown despite its low cold tolerance, andis usually protected from cold by snow or other protectivemulches, such as straw to enable it to survive the winter incolder climates (Brown and Blackburn 1987). Frost damageoccurring during bloom is also a common problem.

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1. Cold Hardiness1.1. Cold hardiness of species and cultivarsFlower frost tolerance of 21 strawberry cultivars variedacross a range of 3°C, and was not related to the origin ofthe cultivar (Ourecky and Reich 1976). Everbearing straw-berry blossoms were found to be 2°C hardier in Octoberthan in September or during bloom in June (Boyce andMarini 1978). In June, the hardiness of blossoms was equalin both everbearing and June bearing cultivars. The hardi-ness of mother and daughter crowns of Redcoat strawberrywere compared under field conditions and controlled freez-ing conditions (Turner et al. 1993). Crown placement in thesoil may affect cold hardiness. Daughter plants were consis-tently hardier than mother plants under field conditions, butin controlled freezing tests the mother plants were as hardyor hardier than the daughter plants.

Exposure of Catskill strawberry plants to nonlethal lowtemperatures caused abnormal growth of leaves, early emer-gence of runners and browning of crown tissue (Marini andBoyce 1979). Blossom numbers were also decreased andflowering delayed. Bolduc and Paquin (1987) also reportedthat flowering may be affected by low nonlethal tempera-tures. Low temperature decreased total yield and fruit size inElsanta runner plants lifted in late winter, although no visi-ble frost injury symptoms were observed (Zurawicz andDominikowski 1993).

1.2. Cold hardiness of plant parts and organsVascular tissue in a strawberry crown is the most resistant tofreezing injury and most crucial to plant survival, cortex andmedulla tissues being the most susceptible (Marini andBoyce 1977). In Redcoat and Bounty strawberries, vegeta-tive buds were 3.8°C hardier than flower buds in January(Paquin et al. 1989). In September and May, vegetative andflower buds possessed equal levels of hardiness. Fruits aremore susceptible to low temperature damage than flowers orbuds (Ourecky and Reich 1976).

Ki and Warmund (1992) studied the susceptibility to lowtemperature injury of styles, anthers and receptacles of Earli-glow and Honeoye strawberry flowers. Styles and receptacleswere found to be more susceptible to cold than anthers. Stylesand receptacles of primary flowers were more susceptiblethan those of tertiary flowers. Anthers in primary flowerswere more susceptible than in secondary or tertiary flowers.

2. Physiology of Cold Hardiness2.1. Biophysical aspects of cold hardinessWarmund (1993) characterized the distribution of extracel-lular ice in Earliglow strawberry crowns and tissue recoveryafter exposure to sublethal temperatures. Crown structurewas disrupted temporarily at –5°C, but plants were not per-manently injured. Voids formed by extracellular ice near thebase of peduncle and vascular system remained in the tissueafter thawing. After 15 wk incubation in a greenhouse, onlyvery few and small voids were observed in crowns. Celldivision and enlargement occurred near the voids. Due tothe rosette morphology of a strawberry plant, a thermal icepropagation barrier sometimes occurs in the crown leadingto independent freezing of individual leaves and flowers(Anderson and Whitworth 1993).

2.2. Biochemical aspects of cold hardinessA relationship between strawberry crown sugar content andcold hardiness was reported by Paquin et al. (1989).Sucrose, reducing and total sugars increased in the crownsof Redcoat and Bounty strawberries during cold hardeningand reached a maximum level in January, concurrently withmaximum hardiness. Proline content also changed duringhardening and dehardening, but the relationship with hardi-ness was not clear. The effect of fall fruiting on the cold tol-erance of crowns of day neutral (DN) strawberry cultivars,and the importance of carbohydrate and nitrogen reserves onwinter survival was studied by Gagnon et al. (1990). Coldhardiness was correlated with percent dry weight, accumu-lation of starch, total accumulation of carbohydrates andtotal nitrogen in roots. Root nitrogen content increased whenfruits were removed on 15 or 30 September. Starch accu-mulation and total carbohydrate content were increased byremoving fruits on 15 September.

3. Evaluating Cold HardinessAccording to Harris (1973), the electrical conductivity andthe recovery method were both reliable in determining rela-tive hardiness of four strawberry genotypes with stress tem-perature of –9°C in October, and a sequence of temperaturesof –9°C, –10.5°C and –12°C in January and March. Theelectrical conductivity is preferred by the author, because itis quick and not affected by the differences in dormancy.Marini and Boyce (1977) reported that TTC reduction andtissue browning could both be used in evaluating strawber-ry crown tissue viability after freeze stress. Bolduc andPaquin (1987) suggested that evaluation of tissue browningshould be combined with evaluation of regrowth and flow-ering to increase the reliability.

4. Factors Affecting Cold Hardiness4.1. Cultural and environmentalThe level of potassium (K) influenced significantly the har-diness of strawberry plants (Bédard and Therrien 1970). Theratio of nitrogen (N), phosphorus (P) and potassium (K) maybe more important for hardiness than the absolute levels ofsingle elements (Zurawicz and Stushnoff 1977). High P/Kratio correlated with hardiness of Redcoat strawberries indifferent fertilization treatments, whereas high P/N ratio didnot. Plant survival had a positive correlation with P/K ratioin root and crown tissue, and a negative correlation withK/N ratio in same tissues. Nutrient deficiencies and high Nwith low P and K resulted in poor hardiness.

Removing fruits in September enhanced cold hardiness ofthe plants during the fall (Gagnon et al. 1990). When thehardiness of mother and daughter crowns of Redcoat straw-berry were compared, mulching enhanced mother plant sur-vival, but had no effect on daughter plant survival (Turner etal. 1993). Midway and Catskill strawberry plants on raisedbeds suffered more winter injury than plants grown on flatbeds (Boyce and Reed 1983).

4.2. Growth regulatorsThe effect of Frost Gard (Custom Chemicides, Fresno, CA)on supercooling of strawberry plants in the presence and

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absence of INA bacteria was evaluated by Anderson andWhitworth (1993). The supercooling of flowering Arkingstrawberry plants was not enhanced by Frost Gard, regard-less of the presence or absence of INA bacteria. There wasa negative linear relationship between the freezing tempera-tures of Frost Gard — infiltrated detached leaves and FrostGard concentration. In leaves vacuum-infiltrated with 20%Frost Gard, the supercooling was enhanced by 1.7°C com-pared to control leaves.

Four cryoprotectants, Frost Free (Plant Products, VeroBeach, FL), Kocide (Griffin Corporation, Valdosta, GA),Cryoban (Great Lakes Chemical Corporation, WestLafayette, IN) and Frost Gard had no effect on the percent-age of blossoms injured by low temperature, yield or berrysize in Earliglow and Lateglow strawberries (Goulart andDemchak 1994).

Biological control of frost injury to strawberry blossomshas also been studied (Lindemann and Suslow 1987). Icenucleation-deficient (INA–) strain of Pseudomonassyringae protected strawberry blossoms against freezinginduced by other P. syringae strains, but was not able to pro-tect against INA+ P. fluorescens. INA– P. fluorescens wasa more effective inhibitor of P. syringae strains than of otherP. fluorescens strains. Inhibition of one bacterial strain byits near-isogenic counterpart depended on dose rather thanon strain. Strawberry blossoms sprayed with INA+ strainFG3 nucleated at –2°C, whereas the antagonistic strain FF1lowered the nucleation point to –5°C (Leonardi et al. 1989).In the open field the FF1 strain could survive on sprayedplants for about 30 d.

BLUEBERRY (VACCINIUM SPP.)In Northern climates, blueberry is subject to winter injury(dieback), spring frost injury to flower buds and blossoms,and also frost injury to fruit (Brown and Blackburn 1987).Highbush blueberry (Vaccinium corymbosum L.) is about ashardy as peach and may be killed by temperatures of –29°C(Westwood 1993). However, blueberry may escape frost byprotective snowcover. A minimum of 30 cm of snow is nec-essary to insure fruit production of half-high blueberry cul-tivars in Northern Minnesota (Wildung and Sargent 1989).In 1968, in the Lac St. Jean area in Quebec, 50% of blue-berry plants were destroyed because of dieback (Brown andBlackburn 1987).

1. Cold Hardiness1.1. Cold hardiness of species and cultivars All clones of lowbush blueberry (Vaccinium angustifoliumAit.) reached their maximum cold hardiness in January orFebruary (Cappiello and Dunham 1994). A selection of V.angustifolium and natural hybrids of V. angustifolium and V.corymbosum were found to be hardier than highbush culti-vars (Quamme et al. 1972b). Southern highbush blueberry(Vaccinium spp.) and northern highbush blueberry(Vaccinium corymbosum) cultivars were found to have lesswinter freeze and spring frost damage in flower buds andflowers than rabbiteye (Vaccinium ashei Reade) blueberrycultivars (Patten et al. 1991).

When comparing five rabbiteye blueberry cultivars, flow-ers of cultivar Southland were found to be most tolerant to

frost (Gupton 1983). When highbush blueberry cultivarswere evaluated for their cold hardiness in Poland, all plantsshowed winter injury symptoms (Smolarz 1989). The hardi-est cultivars were Concord, Rancocas and Weymouth. Olderplants were found to be hardier than younger ones.

1.2 Cold hardiness of plant parts and organsIn a Finnish blueberry cultivar Aron (cultivar Rancocas ×(V. uliginosum L. × cv. Rancocas)), shoots were only slight-ly injured after a severe winter, whereas all flower budswere damaged (Hiirsalmi and Hietaranta 1989). In lowbushblueberry, stem tissue was equally or more hardy than budtissue (Cappiello and Dunham 1994). Cold hardiness of veg-etative buds was equal to that of floral ones in rabbiteyeblueberry cultivars Tifblue and Woodard (Spiers 1978).Rabbiteye blueberry flower buds, formed on fall wood, werehardier than buds formed on spring wood (Patten et al.1991). Injury to flower buds increased as bud developmentadvanced.

In highbush blueberries, V. corymbosum (Biermann et al.1979; Hancock et al. 1987) and V. australe (Bittenbenderand Howell 1976), lateral buds are hardier than terminalones. In lowbush blueberry, the two buds at the stem tipwere more sensitive than buds 3 and 4 (Cappiello andDunham 1994). Lowest survival temperatures varied from–25 to –35°C for the uppermost bud, and from –35 to –40°Cfor the fourth bud. Flower primordia at the stem tip alsodehardened earlier and responded more readily to springwarming than flower primordia in lower buds. According toCappiello and Dunham (1994), in major lowbush blueberrygrowing regions freeze damage is unlikely to occur in anyother tissues than floral tissues in the uppermost bud.

In highbush blueberry, apical florets were found to be lesshardy than median or basal florets within each bud(Biermann et al. 1979). Ovaries were the critical cold sensi-tive tissue (Bittenbender and Howell 1976). In rabbiteyeblueberry cultivars, frost during bloom caused damage topistils, thus reducing fruit set (Gupton 1983).

1.3. Genetics of cold hardinessFear et al. (1985) examined several Vaccinium species andinterspecific hybrids and found that the heritability estimatefor winter injury was low over years but high for individualyears. In the inheritance of cold tolerance, additive varianceis more important than nonadditive variance. In lowbushblueberry, general combining ability effects for winterinjury were high in years with good snow cover but low inyears without snow cover suggesting that lowbush blueber-ry clones are not inherently cold tolerant but depend onsnow cover for their winter survival.

2. Physiology of cold hardiness2.1. Biophysical aspects of cold hardinessBlueberry xylem tissue exhibits deep supercooling(Quamme et al. 1972b). Contrasting reports exist about theability of flower buds to deep supercool. LTEs have beenobserved in blueberry flower buds by Bittenbender andHowell (1976) and by Biermann et al. (1979). But accordingto Flinn and Ashworth (1994), blueberry flower primordia

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do not supercool under natural conditions, but water is with-drawn from the floret towards ice sinks in the scales orbracts. LTEs observed at faster cooling rates in artificialfreezing may be caused by the experimental procedurerather than reflect natural conditions.

2.2. Biochemical aspects of cold hardinessIn floral buds of Bluecrop and Tifblue blueberries, chilling-responsive 65-, 60-, and 14-kDa polypeptides which wereidentified as dehydrins or dehydrin like proteins, accumulat-ed during cold acclimation (Muthalif and Rowland 1994).The largest increase in the level of polypeptides occurred atthe same time as the largest increase in the level of cold har-diness. The maximum level of hardiness and the maximumlevel of chilling-responsive polypeptides was higher inBluecrop than in Tifblue. However, chilling responsivepolypeptides may also be related to the development of dor-mancy rather than the development of hardiness.

3. Evaluating Cold HardinessAccording to Bittenbender and Howell (1976), visual eval-uation of browning of the ovary after controlled freezing atslow cooling rates successfully discriminates between hardyand susceptible blueberry plants.

LTEs in blueberry stems are associated with xyleminjury, but none of the LTEs is associated with injury tobark, which occurs at a much higher temperature (Quammeet al. 1972b). Thus, DTA is not useful in determining stemhardiness of blueberry. According to Bittenbender andHowell (1976), estimating flower bud hardiness of sevenhighbush blueberry cultivars was less accurate by usingexotherms than by using visual rating of tissue browning.According to Biermann et al. (1979) the DTA profile wasrate dependent, each floret within an intact blueberry budexhibiting one rate-dependent LTE that was correlated tolethal injury at slow cooling rates. Flinn and Ashworth(1994) found that blueberry (V. corymbosum) flower budhardiness was not reliably estimated by the DTA in the cul-tivar Berkeley. The number of LTEs did not correspond tothe number of injured florets. DTA profiles of excisedflower buds were different from those of intact buds. Theappearance of a DTA profile was also affected by the cool-ing rate. In attached buds cooled at 2°C per hour, no LTEswere detected.

Impedance measurement could be used to evaluate thehardiness of woody tissue in V. corymbosum blueberries butdid not always detect differences in bud hardiness amongcultivars (Doughty and Hemerick 1975).

4. Factors Affecting Cold Hardiness4.1. Cultural and environmentalBlueberry shoots infected with blueberry canker caused byfungus Fusicoccum putrefaciens Shear. were more suscepti-ble to frost than healthy shoots (Hiirsalmi and Hietaranta1989). Because rabbiteye blueberry flower buds formed onfall wood were found to be hardier than buds formed onspring wood, in southern regions it might be beneficial toenhance the production of fall wood by summer pruningafter harvest (Patten et al. 1991).

4.2. Growth regulatorsWhen cryoprotectants are applied, a protective effect of thecryoprotectant may be completely masked by a negativereaction to the surfactant (Robbins and Doughty 1980).Flowers and flower buds treated with surfactants X-77(Chevron Chemical Company, Ortho Division, SanFransisco, CA) and Surfactant WK (E. I. DuPontWilmington, DE) were more susceptible to cold than con-trols. Multifilm (Colloidal Products, Petaluma, CA) had noeffect.

CRANBERRY (VACCINIUM MACROCARPON)Cranberry (Vaccinium macrocarpon Ait.) is grown in bogs,and due to its growth habit and growing sites is prone tofrost injury. Plants survive in Northern climates becausethey are covered by water or snow in winter, and by waterduring frosts in the growing season. Only a few reports deal-ing with cold hardiness of cranberry were found. For exam-ple, there is no information about factors affecting itshardiness. Clearly, more research on cold hardiness of thisquickly expanding crop is needed.

1. Cold Hardiness in GeneralAbdallah and Palta (1989) studied the frost resistance ofSearles cranberry leaves, flower buds and fruits by con-trolled freezing. The lowest survival temperature of flowerbuds was –22°C in early November and changed sharplyfrom –18°C in mid-April to –2°C in early to mid-May.Flowers and small fruits were only hardy to 0°C. Frost har-diness of fruits increased, as their anthocyanin contentincreased and chlorophyll content decreased. Leaves werethe hardiest plant part studied, being hardier than –24°C inmid-December and losing their hardiness rapidly from lateApril (<–24°C) to early May (–7°C). In native cranberryplants injured by frost in June, flower primordia develop-ment was delayed and the number of flower primordia andtheir final degree of development in the fall was lessened(Hall and Newbery 1972).

2. Physiology of Cold Hardiness2.1. Biochemical aspects of cold hardinessLarger increases occurred in non-reducing than in reducingsugars during cold hardening in cranberry leaves(Sieckmann and Boe 1978). Total sugar concentrationsincreased from 44 to 77 mg g–1 fresh weight in 6 d in lowtemperature and short day conditions. Reducing sugarsincreased from 22 to 33 mg g–1 fresh weight.

3. Evaluating Cold HardinessOnly one report comparing methods to evaluate cold hardi-ness in cranberry was found. According to Eaton and Mahrt(1977), LTEs detected from DTA indicated greater hardi-ness than evaluating injury to cranberry buds visuallythrough a dissecting microscope.

CURRANTS (RIBES SPP.)Black currant (Ribes nigrum L.) and red currant (Ribessativum [Rchb.] Syme) are generally very hardy and can begrown in areas with very cold winter temperatures.

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However, spring frosts during bloom may sometimes be aproblem.

1. Cold Hardiness in General1.1. Cold hardiness of species and cultivarsSince midwinter hardiness is not usually a problem for cur-rants, it has not been a frequent subject in research. After asevere winter in Skierniwice, Poland, there was extensiveflower bud damage to all currant cultivars (Gwozdecki1989). The least damaged black currant cultivars wereKarakol, Matchless, Pensylvanskaya, Ri 1715, Smuglyankaand Typ 3 van Gotz. The least damaged red currants wereDevinska, Velkoplodna, London Market, NeapolskyCerveny and Pomona. Warmund et al. (1991) used themedian LTE to estimate the LT50 of red and black currantbuds in Minnesota. LT50 temperatures for buds of cultivarRed Lake in November, January and March were –21.0,–18.1 and –22.1°C, respectively. For buds of cultivar Dankathe corresponding temperatures were –26.7, –23.6 and–26.5°C, respectively. Black currant flower buds were ableto reharden in winter (Dale and Heiberg 1984). However,this ability weakened as growth progressed. High springtemperatures caused flower buds to be less hardy at samestage of growth than low temperatures.

More research has been directed towards spring frost tol-erance. Mather et al. (1980) studied differences in resistanceto spring frost in an early-flowering black currant progenyand observed segregation of factors conferring frost resis-tance. Frost resistance was probably derived from the maleparent, a selfed progeny of a Finnish wild black currant.According to Mather et al. (1980), good winter hardiness ispossibly associated with spring frost resistance. Dale andHeiberg (1984) studied cultivars Baldwin, Ben Lomond andBen More, and found a relationship between winterhardi-ness and spring frost tolerance, possibly because less hardycultivars began to grow and deharden sooner. Cultivarsrelated to Ben More and Öjebyn were tolerant to –4.5°Cfrost until after first flower, Baldwin and Magnus losingtheir tolerance at the grape stage, and Ben Lomond and itsrelatives being intermediate (Dale 1981). Consequently, cul-tivars should be tested for spring frost tolerance at severalstages of growth. Night frosts in March and April damagedearly- and midseason flowering black currant cultivars moreseverely than late-flowering ones (Keep et al. 1983).

The frost tolerance at flowering of 12 black currant geno-types of different origin, genetic background and times offlowering was studied in the United Kingdom (Brennan1991). Scottish cultivars Ben Alder, Ben Tirran andSwedish cultivars Öjebyn and Stor Klas were found to behardiest at flowering. Cultivars Baldwin and Narjadnajawere the least hardy at flowering. Narjadnaja is a derivativeof Ribes nigrum sibiricum, the wild genotype regarded as adonor of winter hardiness of the vegetative parts. Contraryto the findings of Mather et al. (1980) and Dale and Heiberg(1984), Brennan (1991) concludes that the genes controllingspring frost tolerance and the genes controlling winter har-diness are not linked. In fact, using extremely hardy geno-types in breeding may increase spring frost susceptibilitysince, in milder climates, flowering and bud break may be

advanced. This is in accordance with the findings ofJefferies and Brennan (1994). In their study, three black cur-rant cultivars were exposed to low temperatures abovefreezing and low light intensity at the onset of growth. Themore cold tolerant cultivar, Ben Lomond had lower basetemperatures for leaf appearance and growth than the morecold sensitive cultivars Baldwin and Ben More. The prima-ry effects of low temperature and low light intensity werereduced rates of leaf appearance and leaf expansion. Theeffects of low temperature on photosynthetic rate wereminor. Dale (1987) found that frost tolerance at first flowerwas inherited additively and that Öjebyn and Goliath con-tributed highest parental values of tolerance.

1.2. Cold hardiness of plant parts and organsBrennan et al. (1993) used NMR imaging to study the freez-ing events in black currant flowers. The stigma, style andthe ovarian tissues showed significantly increased signals inNMR images from freeze-damaged flowers. The water con-tent of these parts was increased, probably as a consequenceof tissue disruption after freezing. The authors conclude thatstigma, style and ovarian regions are the most frost sensitiveparts of the flower and the probable sites of spring frostdamage leading to flower death and yield losses.

2. Physiology of Cold Hardiness2.1. Biophysical aspects of cold hardinessFreezing of supercooled water in the floral primordia wasfound to cause tissue injury in floral buds of Danka black andRed Lake red currants (Warmund et al. 1991). Floral budshad multiple, abrupt LTEs which were associated with injuryto the inflorescence. As also observed in raspberry (Warmundand George 1990; Warmund et al. 1992), there was no rela-tionship between the number of LTEs and the number ofracemes or flowers per bud. Presumably several flowers frozesimultaneously. Contrary to the findings of Warmund et al.(1991) and Takeda et al. (1993), Stone et al. (1993) found asignificant relationship between the number of secondaryexotherms resulting from lethal freezing of flower primordiaand the number of racemes within black currant buds. FromDTA profiles, it was concluded that the largest primordia inthe base of the raceme froze first, followed by the smallerones. Accumulation of needle ice was observed beneath themeristematic crown. The authors suggest that the crown is anice nucleation barrier, but allows the migration of water fromthe primordia to facilitate their supercooling.

2.2. Biochemical aspects of cold hardinessIn Red Lake red currant, RFOs, raffinose and stachyose,were the only sugars that correlated with season-long coldhardiness (Stushnoff et al. 1993).

3. Evaluating Cold HardinessAccording to Mather et al. (1980), frost room tests on singleflowering nodes was economical on plant material and effec-tive in testing genotypes with different resistance to springfrost. Injury was evaluated visually. Keep et al. (1983) foundthat response of buds and flowers to frost was dependent oncooling rate. A cooling rate of –0.025°C min–1 with mini-

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mum temperature of –3.25°C would satisfactorily differenti-ate between types with different frost responses. Since frosttolerance is dependent on the developmental stage, the stageof development should be determined carefully beforeinduced frost, and cultivars should be tested at similar stagesto get comparable results (Dale 1987). If cultivars areexposed to frost at the same growth stage, they can be reli-ably ranked for their spring frost tolerance irrespective ofvariations in weather conditions (Dale and Heiberg 1984).

Takeda et al. (1993) compared the suitability of the TTCreduction test and the fluorescein diacetate (FDA) stainingtechnique to assess the viability of excised black currant flo-ral primordia after controlled freezing. Freeze injury inintact buds was difficult to detect because of the lack of vis-ible browning. As also observed in apple (Privé and Zhang1996), the TTC-reduction test was not successful in currantseither. When excised flower primordia were used, viableand injured primordia could be distinguished after incuba-tion in TTC. FDA was not found to be suitable for assessingcold injury.

According to Warmund et al. (1991) floral buds had mul-tiple, abrupt LTEs which were associated with injury to theinflorescence. Also Takeda et al. (1993) detected multipleLTEs in DTA of black currant floral buds. The LT50 tem-perature for flower primordia correlated with the lowestLTE-temperature better (r2 = 0.62) than with the medianLTE-temperature (r2 = 0.56). According to Takeda et al.(1993), the use of DTA alone for assessing freeze injury inblack currant floral buds is not reliable until more is knownabout the origin of LTEs.

Flower and leaf osmotic potentials were associated withfrost tolerance in spring (Jones and Higgs 1983). Correlationwas not strong enough, however, to provide a screeningmethod for frost tolerance.

According to Brennan and Jefferies (1990) chlorophyllfluorescence can provide a rapid screening technique forassessing spring frost hardiness in black currant (Ribesnigrum L.). This technique measures changes in chlorophylla fluorescence caused by stress. Minimum fluorescence (F0)was reduced by low temperatures in all genotypes. Variablefluorescence (FV) was not affected by freezing stress. BothF0 and FV varied between genotypes, but no interactionbetween temperature and genotype was found. Instead, thetime taken for FV to decay to half its maximum value (q1/2),was significantly increased by freezing stress, and this effectvaried between genotypes. The increase in q1/2 was greatestin cultivar Baldwin, which is sensitive to spring frost, andleast in a hardy accession Ri-74020-6. The authors concludethat increase in q1/2 indicates PSII changes during freezingstress and corresponds to a decrease in hardiness.

GRAPES (VITIS SPP.)An extensive review article on cold hardiness in grapevineshas been published by Seyedbagheri and Fallahi in 1994.Thus, only studies post dating that article have been includ-ed here.

1. Cold Hardiness1.1. Cold hardiness of species and cultivarsPrimary bud hardiness of four genotypes of grapes (Vitis

spp.) developed in Arkansas was evaluated by DTA (Bourneet al. 1991). The buds of the two genotypes with the great-est component of V. vinifera parentage acclimated moreslowly in the fall and had less ultimate midwinter bud har-diness than two other genotypes with the greatest compo-nent of V. labrusca in their ancestry. Cultivar Mars releasedfrom this program is a V. labrusca type and hardier thanSaturn, which resembles V. vinifera cultivars (Bourne andMoore 1991). The lowest temperature recorded during thestudy was –25°C in January and it did not cause apparentbud or cane damage to any genotype (Bourne et al. 1991).The data from laboratory tests in this study were in goodagreement with long-term observations of winter survival inthe field. Maximum hardiness in Seyval Blanc grape wasachieved in December; LT50 of primary buds being –23°C,50% browning in phloem occurring at –27°C and onlyminor xylem injury at –30°C (Slater et al. 1991).

2. Physiology of Cold Hardiness2.1. Biochemical aspects of cold hardinessIn Cabernet Sauvignon grape (Vitis vinifera), soluble carbo-hydrate content was related to changes in air temperatureand to the dormancy status of the tissues, increasing in budsand current-season stem pieces during winter, and decreas-ing again from late February through budbreak (Wampleand Bary 1992). Starch content was inversely related to sol-uble carbohydrate content. In Chardonnay and Rieslinggrape (V. vinifera) buds and cortical tissues, high levels ofglucose, fructose, raffinose and stachyose correlated withcold hardiness (Hamman et al. 1996). According to theauthors, with cold tender grape cultivars, a high monosac-charides to disaccharide ratio is a better indicator of coldhardiness than levels of RFOs.

3. Evaluating Cold HardinessLTEs detected in DTA corresponded to temperatures atwhich grape (Vitis vinifera L.) buds were injured (Quamme1986). Sometimes a second LTE associated with injury tosecondary buds was observed. Wolf and Cook (1994) com-pared DTA estimates of grape bud cold hardiness to fieldsurvival observations after a severe frost. It was found thatDTA can confidently be used to estimate not only the rela-tive hardiness but also absolute cold hardiness of buds. Forseven of the nine cultivars, cold hardiness measured byDTA corresponded well to actual bud hardiness evaluatedby visual examination of buds after a severe frost. In onecultivar, the differences were possibly due to primary budshaving been previously destroyed by bud necrosis, which isa common phenomenon in grape. Thus, there is a possibili-ty of misinterpreting exotherms from samples that have asignificant number of previously destroyed buds.

4. Factors Affecting Cold Hardiness4.1. EndogenousSlater et al. (1991) determined the relationship between dor-mancy and winter hardiness in Seyval Blanc grape buds andstem tissues. The buds did not seem to be fully dormant atany test date, but the number of days required for budbreakdecreased as winter progressed. In January and February,

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primary buds, phloem and xylem deacclimated whenexposed to +16°C. Two warming episodes did not enhancethe deacclimation of tissues more than one warmingepisode.

4.2. Cultural and environmental Photoperiod influences on cold acclimation of Vitis labrus-cana Bailey and Vitis riparia Michx. were studied byFennell and Hoover (1991). Short photoperiod causedreductions in growth, greater periderm development andonset of bud dormancy in both species, but only a little coldacclimation. V. riparia plants exposed to short days had 2 to3°C, and V. labruscana 1°C greater freezing tolerance thancontrol plants. It is generally expected that delayed harvestor leaving fruit on the vine would reduce cane and bud car-bohydrate reserves and decrease bud cold hardiness, but inV. vinifera grapes Cabernet Sauvignon (Wample and Bary1992), and Chardonnay and Riesling (Hamman et al. 1996),cold hardiness or carbohydrate reserves were not affected byearly, late or no harvest treatments compared to normal har-vest.

4.3. Growth regulatorsThe potential cryoprotectant activity of several chemicals ongrapevine (Vitis labruscana Bailey) dormant buds and grapeleaf tissue was determined by Himelrick et al. (1991).Chemicals included Dupont Surfactant WK (DEPEG)(DuPont de Nemours, Wilmington, DE), ethylene glycol(Fisher Chemical, Rochester, NY), BRIJ 35 (ICI Americas,Wilmington), Frost Gard (Custom Chemicides, Fresno, CA)and Frost Free (Plants Products Corp., Vero Beach, FL).Results indicated that cryoprotectant chemicals have poten-tial to increase winter hardiness of dormant buds and devel-oping shoots. For example, in April, BRIJ 35 and SurfactantWK were superior to others, LTEs in treated buds being14.1°C and 12.1°C lower than in controls.

SUMMARYA wide variety of different types of studies relating to coldhardiness of fruit crops have been published. Prunusspecies, especially peach, have been studied quite intensive-ly. No studies on cold hardiness of plum were found in theliterature.

Evaluation of cold hardiness of existing cultivars or newselections has been carried out in almost all the crops dis-cussed in this paper. This information is useful for breedingprograms. However, ability to withstand low winter temper-atures often does not correlate with cold hardiness of flowerbuds in spring, as these characteristics do not seem to becontrolled by the same mechanisms. Only in raspberry andapple has cold hardiness been studied in vitro, a techniquewhich in future may offer an alternative to the time con-suming field evaluations of cold hardiness.

Physical limits of deep supercooling may be a limitingfactor for expanding the production of many fruit crops.Supercooling characteristics were studied in apple and pearstem tissues, stem and bud tissues of several Prunus species,stem and flower buds of blackberry, raspberry and blueber-ry, and in flower buds of currants and grapes. Usually the

DTA was found to offer an estimation of cold hardiness inthese tissues. Contradictory reports occur about the reliabil-ity of DTA in estimating cold hardiness of blueberry buds.Interestingly, in Prunus species, dead flower primordia werefound to deep supercool, and their DTA response remainednormal after a killing freeze.

Biochemical changes occur in plants during cold acclima-tion. The relationship between contents of some substancesand cold hardiness has been studied in apple, pear, peach,strawberry, blueberry, cranberry, currant and grapes. Totalsugars are related to season-long hardiness clearly in apple,where sorbitol makes up the bulk of total sugar and is relat-ed to hardiness. Total carbohydrates were associated withincrease in hardiness also in peach, strawberry, cranberry andgrape. Raffinose and stachyose are also related to hardiness.Contents of hydrophilic and acidic amino acids were associ-ated with increase in hardiness in apple buds, soluble proteincontents and low total free amino acids in peach buds, and65-, 60-, and 14-kDa polypeptides in blueberry buds. Totallipids in peach buds reached the maximum in midwinter. Instrawberry, total nitrogen in roots correlated with cold hardi-ness, whereas, in raspberry there was a negative relationshipbetween frost tolerance and leaf nitrogen.

Cold hardiness is determined primarily by genotype, butmay be enhanced by different methods of management. Theeffects of cultural practices were studied in most of thecrops discussed in this paper. Rootstock was found to havean effect on scion cultivar cold hardiness in apple, sweetcherry and peach. Heavy crop load had a negative effect onhardiness in both apple and peach. Whitewashing of treesprovided protection to peach flower buds during spring.Raspberry plants and apple trees on raised beds suffered lesswinter injury than plants on flat beds, but for strawberry, theeffect was reverse. Removing fruits in the fall enhancedwinter survival of DN strawberry cultivars but had no influ-ence on hardiness of grapevine.

Application of growth regulators is one possible way ofenhancing cold hardiness. Understanding mechanisms bywhich growth regulators affect the plant hardiness level wouldbe important for further development of these techniques. Theeffects of growth regulators vary between plant species andeven between cultivars. Paclobutrazol, thidiazuron and flur-primidol enhanced the cold hardiness of apple, while ethep-hon seems to have many beneficial effects on peach coldhardiness, including increased flower bud hardiness duringbloom. Also, paclobutrazol enhanced peach flower frost har-diness. NAA had a positive effect in some peach cultivars, butnot in others. Several cryoprotectant chemicals had a positiveeffect on grape cold hardiness. Controlling INA bacteria pop-ulations in apple, pear and Prunus species does not seem toprotect them from frost injury, since the intrinsic ice nucleusin the stem is still present.

Much research has been done on cold hardiness of fruitand berry crops. However, cold hardiness is an extremelycomplex phenomenon; species and cultivars vary in theirresponse to low temperatures depending on location andother environmental factors. Since genotype is the most crit-ical factor in determining hardiness, developing cold hardycultivars for different climatic conditions is essential. To

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speed and facilitate long-term breeding the possibility ofevaluating cold hardiness in laboratory conditions, such asscreening for cold hardiness in vitro, should be studied care-fully, and new techniques that could provide more rapidresults must be developed. These may include chlorophyllfluorescence and electrical impedance. This would reducethe time-consuming and expensive field testing of selec-tions. Cultural practices have a minor effect on cold hardi-ness but can be used to further enhance hardiness, once theappropriate cultivar is available.

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Current state of cold hardiness research on fruit crops · Current state of cold hardiness research...

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