Abstract
The role of temperature during dormancy development is being reconsidered as more research emerges demonstrating that temperature can significantly influence growth cessation and dormancy development in woody plants. However, there are seemingly contradictory responses to warm and low temperature in the literature. This research/review paper aims to address this contradiction. The impact of temperature was examined in four poplar clones and two dogwood ecotypes with contrasting dormancy induction patterns. Under short day (SD) conditions, warm night temperature (WT) strongly accelerated timing of growth cessation leading to greater dormancy development and cold hardiness in poplar hybrids. In contrast, under long day (LD) conditions, low night temperature (LT) can completely bypass the short photoperiod requirement in northern but not southern dogwood ecotypes. These findings are in fact consistent with the literature in which both coniferous and deciduous woody plant species’ growth cessation, bud set or dormancy induction are accelerated by temperature. The contradictions are addressed when photoperiod and ecotypes are taken into account in which the combination of either SD/WT (northern and southern ecotypes) or LD/LT (northern ecotypes only) are separated. Photoperiod insensitive types are driven to growth cessation by LT. Also consistent is the importance of night temperature in regulating these warm and cool temperature responses. However, the physiological basis for these temperature effects remain unclear. Changes in water content, binding and mobility are factors known to be associated with dormancy induction in woody plants. These were measured using non-destructive magnetic resonance micro-imaging (MRMI) in specific regions within lateral buds of poplar under SD/WT dormancing inducing conditions. Under SD/WT, dormancy was associated with restrictions in inter- or intracellular water movement between plant cells that reduces water mobility during dormancy development. Northern ecotypes of dogwood may be more tolerant to photoinhibition under the dormancy inducing LD/LT conditions compared to southern ecotypes. In this paper, we propose the existence of two separate, but temporally connected processes that contribute to dormancy development in some deciduous woody plant: one driven by photoperiod and influenced by moderate temperatures; the other driven by abiotic stresses, such as low temperature in combination with long photoperiods. The molecular changes corresponding to these two related but distinct responses to temperature during dormancy development in woody plants remains an investigative challenge.
Similar content being viewed by others
References
Abeles FB, Forrence FE (1970) Temporal and hormonal control of β-1, 3-Glucanase in Phaseolus vulgaris L. Plant Phys 45:395–400
Allona I, Ramnos A, Ibanez C, Contreras A, Casado R, Aragoncillo C (2008) Molecular control of dormancy establishment in trees. Span J Agric Res 6:201–210
Ashworth EN (1982) Properties of peach flower buds which facilitate supercooling. Plant Phys 70:175–179
Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AH, Jansson S, Strauss SH, Nilsson O (2006) CO/FT Regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043
Butler WL, Lane HC (1965) Dark transformation of phytochrome in vivo II. Plant Phys 40:13–17
Castillon A, Shen H, Huq E (2007) Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci 12:514–521
DeFay E, Vacher V, Humbert F (2000) Water-related phenomena in winter buds and twigs of Picea abies L. (Karst.) until bud-burst: a biological, histological and NMR study. Ann Bot 86:1097–1100
Dijkwel PP, Huijser C, Weisbeek PJ, Chua NH, Smeekens SCM (1997) Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell 9:583–595
Dormling I (1989) The role of photoperiod and temperature in the induction and release of dormancy in Pinus sylvestris L. seedlings. Ann For Sci 46:228–232
Dormling I, Gustafsson A, von Wettstein D (1968) The experimental control of the life cycle in Picea abies (L.) Karst. Silvae Genet 17:44–64
Downs RJ, Bevington JM (1981) Effect of temperature and photoperiod on growth and dormancy of Betula papyrifera. Am J Bot 68:795–800
Downs RJ, Borthwick HA (1956) Effects of photoperiod on growth of trees. Bot Gaz 117:310–326
Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44
Erez A, Faust M, Line MJ (1998) Changes in water status in peach buds in induction, development and release from endodormancy. Sci Hortic 73:111–123
Eriksson ME (2000) The role of phytochrome A and gibberellins in growth under long and short day conditions: studies in hybrid aspen. PhD thesis, Swedish Univ Agric Sci, Umeå, Sweden
Faust M, Liu D, Line MJ, Stutte GW (1995) Conversion of bound water to free water in endodormant buds of apple is an incremental process. Acta Hort 395:113–117
Foley ME, Anderson JV, Horvath DP (2009) The effects of temperature, photoperiod, and vernalization on regrowth and flowering competence in Euphorbia esula (Euphorbiaceae) crown buds. Botany 87(10):986–992
Fuchigami LH, Weiser CJ, Evert DR (1971) Induction of cold acclimation in Cornus stolinifera Michx. Plant Phys 47:98–103
Garner WW, Allard HA (1923) Further studies in photoperiodism, the response of the plant to relative length of day and night. J Agric Res 23:871–920
Granhus A, Fløistad IS, Søgaard G (2009) Bud burst timing in Picea abies seedlings as affected by temperature during dormancy induction and mild spells during chilling. Tree Phys 29:497–503
Grindal G, Junttila O, Reid JB, Moe R (1998) The response to gibberellin in Pisum sativum grown under alternating day and night temperature. J Plant Grow Regul 17:161–167
Håbørg A (1972) Effects of photoperiod and temperature on growth and development of three latitudinal and three altitudinal populations of Betula pubescens Ehrh. Agric U Norway, Dept Dendrol & Nursery Manag, Report #51(2), 27 p
Halliday KJ, Salter MG, Thingnaes E, Whitelam GC (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of floral integrator FT. Plant J 33:875–885
Hänninen H, Kramer K (2007) A framework for modelling the annual cycle of trees in boreal and temperate regions. Silva Fenn 41:167–205
Heide OM (1974) Growth and dormancy in Norway spruce ecotypes (Picea abies). I. Interaction of photoperiod and temperature. Physiol Plant 30:1–12
Heide OM (2003) High autumn temperature delays spring bud burst in boreal trees, counterbalancing the effect of climatic warning. Tree Phys 23:931–936
Heide OM (2008) Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species. Sci Hort 115:309–314
Heide OM, Pestrud AK (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Phys 25:109–114
Hennig L (2006) Phytochrome degradation and dark reversion. In: Schäfer E, Nagy F (eds) Photomorphogenesis in plants and bacteria, 3rd edn. Springer, Dordrecht, pp 131–153
Hennig L, Schäfer E (2001) Both subunits of the dimeric plant photoreceptor phytochrome require chromophore for stability of the far-red light absorbing form. J Bio Chem 276:7913–7918
Horvath DP, Chao WS, Anderson JV (2002) Molecular analysis of signals controlling dormancy and growth in underground adventitious buds of leafy spurge. Plant Phys 128:1439–1446
Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540
Horvath DP, Anderson JV, Chao WS (2009a) Cloning, characterization, regulation, and function of dormancy-associated MADS-BOX genes from Leafy Spurge. Weed Sci Soc Am Meeting Abstract #276
Horvath DP, Sung S, Kim D (2009b) Cloning, characterization, regulation, and function of dormancy-associated MADS-box genes from Leafy Spurge. In: 4th Inter symp plant dorm, Fargo ND Abstract Book. p 18
Hou JQ, Kendall EJ, Simpson GM (1997) Water uptake and distribution in non-dormant and dormant wild oat (Avena fatua L.) caryopses. J Exp Bot 48:683–692
Howe GT, Saruul P, Davis J, Chen THH (2000) Quantitative genetics of bud phenology, frost damage, and winter survival in an F2 family of hybrid poplar. Theor Appl Genet 101:632–642
Jansen E, Rivier L, Junttila O, Crozier A (1986) Identification of abscisic acid from shoots of Salix pentandra. Physiol Plant 66:406–408
Jian LC, Li PH, Sun LH, Chen THH (1997) Alterations in ultrastructure and subcellular localization of Ca2+ in poplar apical bud cells during the induction of dormancy. J Exp Bot 48:1195–1207
Jonkers H (1979) Bud dormancy of apple and pear in relation to the temperature during the growth period. Scientia Hort 10:149–154
Juntilla O, Jensen E, Ernstsen A (1991) Effects of prohexadione (BX-112) and gibberellins on shoot elongation in Salix. Physiol Plant 83:17–21
Junttila O (1980) Effect of photoperiod and temperature on apical growth cessation in two ecotypes of Salix and Betula. Physiol Plant 48:347–352
Junttila O (1982) The cessation of apical growth in latitudinal ecotypes and ecotype crosses of Salix pentandra L. J Exp Bot 33(136):1021–1029
Junttila O, Jensen E (1988) Gibberellins and photoperiodic control of shoot elongation in Salix. Physiol Plant 74:371–375
Junttila O, Nilsen J, Igeland B (2003) Effect of temperature on the induction of bud dormancy in ecotypes of Betula pubescens and Betula pentandra. Scan J For Res 18:208–217
Kalcsits L, Silim S, Tanino K (2009a) Warm temperature accelerates short photoperiod-induced growth cessation and dormancy induction in hybrid poplar (Populus × spp.). Trees 23:973–979
Kalcsits L, Kendall E, Silim S, Tanino K (2009b) Magnetic resonance micro-imaging (MRMI) indicates water diffusion is correlated with axillary bud dormancy induction in hybrid poplar (Populus × spp.). Tree Phys 29:1269–1277
Kalcsits L, Silim S, Tanino K (2009c) The influence of temperature on dormancy induction and plant survival in woody plants. In: Gusta L, Wisniewski M, Tanino K (eds) Plant cold hardiness: from the laboratory to the field. CABI International, London, pp 108–118
Kim HJ, Kim YK, Park JY, Kim J (2002) Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. Plant J 29:693–704
Koski V, Sievänen R (1985) Timing of growth cessation in relation to the variations in the growing season. In: Tigerstedt PMA, Puttonen P, Koski V (eds) Crop physiology of forest trees. Helsinki Univ Press, Helsinki, pp L67–L93
Kramer PJ (1936) Effect of variation in length of day on growth and dormancy of trees. Plant Phys 11:127–137
Kramer PJ (1957) Some effects of various combinations of day and night temperatures and photoperiod on the height growth of loblolly pine seedlings. For Sci 3:45–55
Le Bris M, Michaux-Ferrière N, Jacob Y, Poupet A, Barthe P, Guigonis JM, Le Page Degivry MT (1999) Regulation of bud dormancy by manipulation of ABA in isolated buds of Rosa hybrida cultured in vitro. Aust J Plant Phys 26:273–281
Levitt J (1980) Responses of plants to environmental stresses, vol 1. Academic Press, New York
Malcolm DC, Pymar CF (1975) The influence of temperature on the cessation of height growth of Sitka spruce (Picea sitchensis Bong. Carr.). Silvae Genet 24:5–6
Moe R (1990) Effect of day and night temperature alternations and of plant growth regulators on stem elongation and flowering of the long-day plant Campanula isophylla Moretti. Sci Hortic 43:291–305.
Mölmann JA, Berhanu AT, Stormo SK, Ernstsen A, Junttila O, Olsen JE (2003) Metabolism of gibberellin A19 is under photoperiodic control in Populus, Salix and Betula, but not in daylength-insensitive Populus overexpressing phytochrome A. Physiol Plant 119:278–286
Mölmann JA, Asante DKA, Jensen JB, Krane MN, Ernstsen A, Junttila O, Olsen JE (2005) Low night temperature and inhibition of gibberellin biosynthesis override phytochrome action and induce bud set and cold acclimation, but not dormancy in PHYA overexpressors and wild-type of hybrid aspen. Plant Cell Environ 28:1579–1588
Myster J, Junttila O, Lindgaard B, Moe R (1997) Temperature alternations and the influence of gibberellins and indoleacetic acid on elongation growth and flowering of Begonia × hiemalis Fotsch. Plant Grow Regul 21:135–144
Nitsch JP (1957) Photoperiodism in woody plants. Am Soc Hort Sci 70:526–544
Olsen JE, Jensen E, Junttila O, Moritz T (1995) Photoperiodic control of endogenous gibberellins in roots and shoots of elongating Salix pentandra seedlings. Physiol Plant 90:378–381
Olsen JE, Junttila O, Nilsen J, Eriksson ME, Martinussen I, Olsson O, Sandberg G, Moritz T (1997) Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimation. Plant J 12:1339–1350
Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Ann Rev Plant Biol 54:329–355
Palonen P (2006) Vegetative growth, cold acclimation, and dormancy as affected by temperature and photoperiod in six red raspberry (Rubus idaeus L.) cultivars. Eur J Hort Sci 72:6
Partanen J, Beuker E (1999) Effects of photoperiod and thermal time on the growth rhythm of Pinus sylvestris seedlings. Scand J For Res 14:487–497
Penfield S (2008) Temperature perception and signal transduction in plants. New Phyt 179:615–628
Rinne PLH, Van der Schoot C (2003) Plasmodesmata at the crossroads between development, dormancy and defense. Can J Bot 81:1182–1197
Rinne PLH, Kaikuranta P, Van der Schoot C (2001) The shoot apical meristem restores its symplastic organization during chilling-induced release from dormancy. Plant J 26:249–264
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trend Plant Sci 12:217–223
Rohde A, Van Montagu M, Inze D, Boerjan W (1997) Factors regulating the expression of cell cycle genes in individual buds of Populus. Planta 201:43–52
Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Bhalerao R, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390
Sarvas R (1972) Investigations on the annual cycle of development of forest trees. Active period. Comm InstForest Fenn 76:1–110
Sarvas R (1974) Investigations on the annual cycle of development of forest trees. II. Autumn dormancy and winter dormancy. Comm Inst Forest Fenn 84:1–101
Schäfer E, Schmidt W (1974) Temperature dependence of phytochrome dark reversions. Planta 116:257–266
Short TW (1999) Overexpression of Arabidopsis phytochrome B inhibits phytochrome A function in the presence of sucrose. Plant Phys 119:1497–1506
Smithberg MH, Weiser CJ (1968) Patterns of variation among climatic races of red-osier dogwood. Ecology 49:495–505
Søgaard G, Johnsen Ø, Nilsen J, Junttila O (2008) Climatic control of bud burst in young seedlings of nine provenances of Norway spruce. Tree Phys 28:311–320
Stavang JA, Gallego-Bartolomé J, Yoshida S, Asami T, Olsen JE, Garcia-Martinez JL, Alabadi D, Blazquez MA (2009) Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J 60(4):589–601
Svendsen E, Wilen R, Stevenson R, Liu R, Tanino K (2007) A molecular marker associated with low-temperature induction of dormancy in red osier dogwood (Cornus sericea). Tree Phys 27:385–397
Tanino K (2004) The role of hormones in endodormancy induction. J Crop Impr 10:157–199
Tanino KK, Fuchigami LH, Chen THH, Gusta LV, Weiser CJ (1989) Dormancy-breaking agents on acclimation and deacclimation of dogwood. HortSci 24:353–354
Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006
Van der Toorn A, Zemah H, Van As H, Bendel P, Kamentsky R (2000) Regulation of growth, development and whole organism physiology: developmental changes and water status in tulip bulbs during storage: visualization by NMR imaging. J Exp Bot 51:1277–1287
Van der Veen R (1951) Influence of daylength on the dormancy of some species of the genus Populus. Physiol Plant 4:35–40
Weiser CJ (1970) Cold resistance and injury in woody plants. Science 169:1269–1278
Went FW (1948) Thermoperiodicity. In: Verdoorn F (ed) Vernalization and photoperiodism—a symposium. Chronica Botanica Co, Waltham, MA, USA
Went FW (1953) The effect of temperature on plant growth. Ann Rev Plant Phys 4:347–362
Westergaard L, Eriksen EN (1997) Autumn temperature affects the induction of dormancy in first-year seedlings of Acer platanoides L. Scan J For Res 12:11–16
Yooyongwech S, Horigane AK, Yoshida M, Yamaguchi M, Sekozawa Y, Sugaya S, Gemma H (2008) Changes in aquaporin expression and magnetic resonance imaging of water status in peach tree flower buds during dormancy. Physiol Plant 134:522–533
Acknowledgments
Funding is gratefully acknowledged from the Agroforestry Division, Agriculture Agri-Food Canada without which the poplar experiments would not have been possible. Several students contributed to the photoinhibition work including Kirk Cherry, Jillian (Baerr) Kriger and William Hrycan. Best personal thanks to Heikki Hanninen for scanning and sending the pdf’s of 4 long articles from journals which were inaccessible to the corresponding author. The hard work of the early pioneers of this field of study (Table 1) is also respectfully acknowledged and deeply appreciated.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tanino, K.K., Kalcsits, L., Silim, S. et al. Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol Biol 73, 49–65 (2010). https://doi.org/10.1007/s11103-010-9610-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-010-9610-y