Abstract
As observed for most stresses, tree frost resistance can be split into two main processes: avoidance and tolerance. Avoidance of freezing is achieved by introducing species only in the climatic context in which the probability of freezing events is very low for the sensitive stages of buds or stems; i.e., when good synchronism exists between the annual cycle and the critical climatic periods. Buds become able to grow only after chilling requirements have been satisfied (endodormancy released) during winter; they subsequently break after heat requirements have been completed (end of ecodormancy) in early spring. Actually, this period is often subject to more or less severe freezing events. Trees are also able to adjust their freezing tolerance by increasing their capacity of extracellular freezing and decreasing the possibility of intracellular freezing through the process of frost acclimation. Both freezing resistance processes (avoidance and tolerance) are environmentally driven (by photoperiod and temperature), but there are also genotypic effects among species or cultivars. Here, we evaluated the degree to which differences in dormancy release and frost acclimation were related to environmental and genetic influences by comparing trees growing in common garden conditions. This investigation was carried out for two winters in lowland and mountain locations on different walnut genotypes differing significantly for budburst dates. Chilling requirement for endodormancy release and heat requirement during ecodormancy were evaluated in all situations. In addition, frost acclimation was assessed by the electrolyte leakage method on stems from the same trees before leaf fall through budburst. No significant differences were observed in chilling requirements among genotypes. Moreover, frost acclimation dynamics were similar between genotypes or locations when expressed depending on chilling units accumulated since 15 September as a time basis instead of Julian day. The only exception was for maximal frost hardiness observed during winter with the timber-oriented being significantly more resistant than fruit-oriented genotypes. Heat requirement was significantly different among genotypes. Thus, growth was significantly faster in fruit-oriented than in wood-oriented genotypes. Furthermore, among wood-oriented genotypes, differences in growth rate were observed only at cold temperatures. Frost acclimation changes differed significantly between fruit- and wood- walnuts from January through budburst. In conclusion, from September through January, the acclimation dynamic was driven mainly by environmental factors whereas from January through budburst a significant genotype effect was identified in both frost tolerance and avoidance processes.
Similar content being viewed by others
Abbreviations
- CU:
-
Chilling units
- LT50 :
-
Lethal temperature for 50% of cells
- MTB:
-
Mean time until bud break
References
Aitken SN, Adams WT (1997) Spring cold hardiness under strong genetic control in Oregon populations of Pseudotsuga menziesii var. menziesii. Can J For Res 27:1773–1780
Anderson JL, Richardson EA, Kesner CD (1986) Validation of chill unit and flower bud phenology models for "Montmorency" sour cherry. Acta Hortic 184:71–78.
Anekonda TS, Adams WT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC (2000) Genetics of cold hardiness in a cloned full-sib family of coastal Douglas-fir. Can J For Res 30:837–840
Arnold CY (1959) The determination and significance of the base temperature in a linear heat unit system. Proc Am Soc Hortic Sci 74:430–445
Aronsson A (1975) Influence of photo- and thermoperiod on the initial stages of frost hardening and dehardening of phytotron-grown seedlings of scots pine (Pinus sylvestris L.) and Norway spruce (Picea abies L. Karst.). Stud For Suec 128
Aslamarz AA, Vahdati K, Rahemi M, Hassani D (2010) Evaluation of chilling-heat requirements of some Persian walnut cultivars. Acta Hortic 861:317–320.
Bidabe B (1967) Action de la température sur l'évolution des bourgeons de pommier et comparaison de méthodes de contrôle de l'époque de floraison. Ann Physiol Veg 9:65–86
Bogdanov P (1931) Ueber Photoperiodismus beiden Holzarten. Mitt Staatsinst Wiss Forsch Gebiet Forstwirtsch Holzind 10:21–55
Bower AD, Aitken SN (2006) Geographic and seasonal variation in cold hardiness of whitebark pine. Can J For Res 36:1842–1850
Campbell RK, Sugano AI (1975) Phenology of bud burst in Douglas-fir related to provenance, photoperiod, chilling, and flushing temperature. Bot Gaz 136:290–298
Cannell MGR, Smith RI (1983) Thermal time, chill days and prediction of budburst in Picea sitchensis. J Appl Ecol 20:951–963
Cannell MGR, Sheppard LJ, Smith RI, Murray MB (1985) Autumn frost damage on young Picea sitchensis 2. Shoot frost hardening, and the probability of frost damage in Scotland. Forestry 58:145–166
Charrier G, Améglio T (2011) The timing of leaf fall affects cold acclimation by interactions with air temperature through water and carbohydrate contents. Environ Exp Bot 72:351–357.
Christersson L (1978) The influence of photoperiod and temperature on the development of frost hardiness in seedlings of Pinus silvestris and Picea abies. Physiol Planta 44:288–294
Chuine I, Morin X, Bugmann H (2010) Warming, photoperiods, and tree phenology. Science 329:277–278
Citadin I, Raseira MCB, Herter FG, Silva JBd (2001) Heat requirement for blooming and leafing in peach. HortScience 36:305–307
Clark RM, Thompson R (2010) Predicting the impact of global warming on the timing of spring flowering. Int J Climatol 30:1599–1613
Couvillon GA, Erez A (1985) Effect of level and duration of high temperatures on rest in the peach. J Am Soc Hortic Sci 110:579–581
Dantuma G, Andrews JE (1960) Differential response of certain barley and wheat varieties to hardening and freezing during sprouting. Can J Bot 38:133–151
Dennis FG Jr (1987) Producing temperate-zone fruits at low latitudes: an overview. Hortscience 22:1226–1227
Dennis FG Jr (1994) Dormancy. What we know (and don't know). Hortscience 29:1249–1255
Derory J, Scotti-Saintagne C, Bertocchi E, Le Dantec L, Graignic N, Jauffres A, Casasoli M, Chancerel E, Bodenes C, Alberto F, Kremer A (2009) Contrasting relations between diversity of candidate genes and variation of bud burst in natural and segregating populations of European oaks. Heredity 105:401–411
Derory J, Leger P, Garcia V, Schaeffer J, Hauser MT, Salin F, Luschnig C, Plomion C, Glossl J, Kremer A (2006) Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytol 170:723–738
Druart N, Johansson A, Baba K, Schrader J, Sjodin A, Bhalerao RR, Resman L, Trygg J, Moritz T, Bhalerao RP (2007) Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J 50:557–573
Essiamah S, Eschrich W (1985) Changes of starch content in the storage tissues of deciduous trees during winter and spring. IAWA Bulletin:97–106
Fishman S, Erez A, Couvillon GA (1987a) Thetemperature dependence of dormancy breaking inplants : mathematical analysis of a two-step modelinvolving a co-operative transition, J Theor Biol124:473–483
Fishman S, Erez A, Couvillon GA (1987b) Thetemperature dependence of dormancy breaking inplants : computer simulation of processes studiedunder controlled temperatures. J Theor Biol 126:309–321
Fuchigami LH, Weiser CJ, Kobayashi K, Timmis R, Gusta LV (1982) A degree growth stage (degree GS) model and cold acclimation in temperate woody plants. In: Li PH, Sakai A (eds) Plant cold hardiness and freezing stress. Mechanisms and crop implications, vol 2. Academic, New York, pp 93–116
Germain E, Prunet JP, Garcin A (1999) Le Noyer Editions. CTIFL, Paris
Glerum C (1973) Annual trends in frost hardiness and electrical impedance for seven coniferous species. Can J Plant Sci 53:881–889
Greer DH, Warrington IJ (1982) Effect of photoperiod, night temperature, and frost incidence on development of frost hardiness in Pinus radiata. Aust J Plant Physiol 9:333–342
Guy CL, Huber JLA, Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low-temperature. Plant Physiol 100:502–508
Hannerz M (1999) Evaluation of temperature models for predicting bud burst in Norway spruce. Can J For Res 29:9–19
Hanninen H (1990) Modelling bud dormancy release in trees from cool and temperate regions. Acta For Fenn 213:1–47.
Heide OM (1993a) Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Planta 88:531–540
Heide OM (1993b) Dormancy release in beech buds (Fagus sylvatica) requires both chilling and long days. Physiol Planta 89:187–191
Heide OM, Prestrud AK (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol 25:109–114
Howell GS, Weiser CJ (1970) The environmental control of cold acclimation in apple. Plant Physiol 45:390–394
Irving RM, Lanphear FO (1968) Regulation of cold hardiness in Acer negundo. Plant Physiol 43:9–13
Jermstad KD, Bassoni DL, Wheeler NC, Anekonda TS, Aitken SN, Adams WT, Neale DB (2001) Mapping of quantitative trait loci controlling adaptive traits in coastal Douglas-fir. II. Spring and fall cold-hardiness. Theor Appl Genet 102:1152–1158
Kalberer SR, Wisniewski M, Arora R (2006) Deacclimation and reacclimation of cold-hardy plants: current understanding and emerging concepts. Plant Scie 171:3–16
Karlsson PS, Bylund H, Neuvonen S, Heino S, Tjus M (2003) Climatic response in the mountain birch at two areas in northern Fennoscandia and possible responses to global change. Ecography 26:617–625
Kellomaki S, Vaisanen H, Hanninen H, Kolstrom T, Lauhanen R, Mattila U, Pajari B (1992) A simulation model for the succession of the boreal forest ecosystem. Silva Fenn 26:1–18
Korner C, Basler D (2010a) Phenology under global warming. Science 327:1461–1462
Korner C, Basler D (2010b) Warming, photoperiods, and tree phenology response. Science 329:278
Landsberg JJ (1974) Apple fruit bud development and growth. Analysis and an empirical model. Ann Bot 38:1013–1023
Lang GA, Early JD, Martin GC, Darnell RL (1987) Endo-, para- and ecodormancy: physiological terminology and classification for dormancy research. Hortscience 22:371–377
Larcher W (1995) Physiological plant ecology. Ecophysiology and stress physiology of functional groups. Springer, Berlin
Larcher W, Mair B (1968) Das kälteresistenzverhalten von Quercus pubescens. Ostrya carpinifolia und Fraxinus ornus auf drei thermisch unterschiedlichen standorten. Oecol Planta 3:255–270
Legave JM, Farrera I, Almeras T, Calleja M (2008) Selecting models of apple flowering time and understanding how global warming has had an impact on this trait. J Hortic Sci Biotechnol 83:76–84
Leinonen I (1996) A simulation model for the annual frost hardiness and freezing damage of scots pine. Ann Bot 78:687–693
Linkosalo T, Carter TR, Hakkinen R, Hari P (2000) Predicting spring phenology and frost damage risk of Betula spp. under climatic warming: a comparison of two models. Tree Physiol 20:1175–1182
Linkosalo T, Hakkinen R, Terhivuo J, Tuomenvirta H, Hari P (2009) The time series of flowering and leaf bud burst of boreal trees (1846–2005) support the direct temperature observations of climatic warming. Agric For Meteorol 149:453–461
Linsley Noakes GC, Allan P (1994) Comparison of two models for the prediction of rest completion in peaches. Sci Hortic 59:107–113
Luedeling E, Zhang MH, McGranahan G, Leslie C (2009) Validation of winter chill models using historic records of walnut phenology. Agric For Meteorol 149:1854–1864
Mauget JC (1981) Modification des capacités de croissance des bourgeons du noyer par application d'une température de 4 degrés C à différents moments de leur période de repos apparent. C R Acad Sci Paris III 292:1081–1084
Mauget JC, Germain E (1980) Dormance et précocité de débourrement des bourgeons chez quelques cultivars de Noyer (Juglans regia L.). C R Acad Sci Paris D 290:135–138
Meier U (2001) Stades phénologiques des mono-et dicotylédones cultivées. BBCH Monographie. Centre Fédéral de Recherche Biologiques pour l’Agriculture et les Forêts. http://www.jki.bund.de/fileadmin/dam_uploads/_veroeff/bbch/BBCH-Skala_franz%C3%B6sisch.pdf. 166 pp
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kubler K, Bissolli P, Braslavska O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A, Filella Y, Jatcza K, Mage F, Mestre A, Nordli O, Penuelas J, Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski FE, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Global Change Biol 12:1969–1976
Moshkov BS (1935) Photoperiodismus und Frosthärte ausdauernder Gewächse. Planta 23:774–803
Myking T (1999) Winter dormancy release and budburst in Betula pendula Roth and B. pubescens Ehrh. ecotypes. Phyton 39:139–146
Nilsson JE, Walfridsson EA (1995) Phenological variation among plus-tree clones of Pinus sylvestris (L.) in northern Sweden. Silvae Genet 44:20–28
O'Neill GA, Aitken SN, Adams WT (2000) Genetic selection for cold hardiness in coastal Douglas-fir seedlings and saplings. Can J For Res 30:1799–1807
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Perry TO (1971) Dormancy of trees in winter. Science 171:29–36
Pogosyan KS, Sakai A (1969) Freezing resistance in grape vines. Low Temperature Science Series B 27:125–142
Poirier M, Lacointe A, Améglio T (2010) A semi-physiological model of cold hardening and dehardening in walnut stem. Tree Physiol 30:1555–1569
Pouget R (1964) Observations sur la vitesse de débourrement de cépages de Vitis vinifera L. après levée artificielle de la dormance. C R Acad Sci Paris 258:4333–4335
Rea R, Eccel E (2006) Phenological models for blooming of apple in a mountainous region. Int J Biometeorol 51:1–16
Repo T, Lappi J (1989) Estimation of standard error of impedance-estimated frost resistance. Scand J For Res 4:67–74
Richardson EA, Seeley SD, Walker DR (1974) A model for estimating the completion of rest for Redhaven and Elberta peach trees. Hortscience 9:331–332
Ruiz D, Campoy JA, Egea J (2007) Chilling and heat requirements of apricot cultivars for flowering. Environ Exp Bot 61:254–263
Sakai A, Larcher W (eds) (1987) Frost survival of plants. Responses and adaptation to freezing stress. Ecological studies series. Springer, Berlin
Sarvas R (1974) Investigations on the annual cycle of development of forest trees. 2. Autumn dormancy and winter dormancy. Commun Inst For Fenn 84:101
Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187
Schwarz Wv (1970) Der einfluss der photoperiode auf das austreiben, die frosthärte und die hitzeresistenz von zirben und alpenrozen. Flora 159:258–285
Scorza R, Okie WR (1990) Peaches (Prunus). Acta Hortic 290:175–231
Sutinen ML, Palta JP, Reich PB (1992) Seasonal differences in freezing stress resistance of needles of Pinus nigra and Pinus resinosa: evaluation of the electrolyte leakage method. Tree Physiol 11:241–254
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426
Thomson AJ, Moncrieff SM (1982) Prediction of bud burst in douglas-fir by degree-day accumulation. Can J For Res 12:448–452
Topp BL, Sherman WB, Raseira MCB (2008) Low-chill cultivar development. In: Layne DR, Bassi D (eds) The peach: botany, production and uses. Cabi, Wallingford, UK, pp 106–138
Vitasse Y, Delzon S, Bresson CC, Michalet R, Kremer A (2009) Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Can J For Res 39:1259–1269
Wang JV (1960) A critique of the heat unit approach to plant response studies. Ecology 41:785–790
Weinberger JH (1950) Prolonged dormancy of peaches. Proc Am Soc Hortic Sci 56:129–133
Weiser CJ (1970) Cold resistance and acclimation in woody plants. In: Larsen RP (ed) Cold hardiness, dormancy and freeze protection of fruit crops. Pullman, WA, pp 403–410
Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Planta 127:167–181
Welling A, Kaikuranta P, Rinne P (1997) Photoperiodic induction of dormancy and freezing tolerance in Betula pubescens. Involvement of ABA and dehydrins. Physiol Planta 100:119–125
Witt W, Sauter JJ (1994a) Enzymes of starch metabolism in poplar wood during fall and winter. J Plant Physiol 143:625–631
Witt W, Sauter JJ (1994b) Starch metabolism in poplar wood ray cells during spring mobilization and summer deposition. Physiol Planta 92:9–16
Xing WB, Rajashekar CB (2001) Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Environ Exp Bot 46:21–28
Zhang MIN, Willison JHM (1987) An improved conductivity method for the measurement of frost hardiness. Can J Bot 65:710–715
Acknowledgments
This work was supported in part by INRA—Department of Agronomy and Environment and by a MRES PhD grant to G.C.. We are grateful to Christian Bodet and Christophe Serre for their help with data collection of LT50. We would like also thank the two anonymous reviewers for their comments, which helped us to improve the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Charrier, G., Bonhomme, M., Lacointe, A. et al. Are budburst dates, dormancy and cold acclimation in walnut trees (Juglans regia L.) under mainly genotypic or environmental control?. Int J Biometeorol 55, 763–774 (2011). https://doi.org/10.1007/s00484-011-0470-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-011-0470-1