Abstract
In woody species cycling between growth and dormancy must be precisely synchronized with the seasonal climatic variations. Cessation of apical growth, resulting from exposure to short photoperiod (SD) and altered light quality, is gating the chain of events resulting in bud dormancy and cold hardiness. The relative importance of these light parameters, sensed by phytochromes and possibly a blue light receptor, varies with latitude. Early in SD, changes in expression of light signaling components dominate. In Populus active shoot elongation is linked to high expression of FLOWERING LOCUS T (FT) resulting from coincidence of high levels of CONSTANS and light at the end of days longer than a critical one. In Picea, PaFT4 expression increases substantially in response to SD. Thus, in contrast to Populus-FT, PaFT4 appears to function in inhibition of shoot elongation or promotion of growth cessation. Accordingly, different FT-genes appear to have opposite effects in photoperiodic control of shoot elongation. Reduction in gibberellin under SD is involved in control of growth cessation and bud formation, but not further dormancy development. Coinciding with formation of a closed bud, abscisic acid activity increases and cell-proliferation genes are down-regulated. When dormancy is established very few changes in gene expression occur. Thus, maintenance of dormancy is not dependent on comprehensive transcriptional regulation. In some species low temperature induces growth cessation and dormancy, in others temperature affects photoperiod requirement. The temperature under SD affects both the rate of growth cessation, bud formation and depth of dormancy. As yet, information on the molecular basis of these responses to temperature is scarce.


Similar content being viewed by others
References
Baldwin B, Bandara MS, Tanino K (2000) Bud scale maturation in Saskatoon berry (Amelanchier alnifolia Nutt). Plantlets following in vitro hormonal treatments. Acta Horticult 520:203–208
Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner A, Jansson S, Strauss S, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043
Borthwick HA, Hendricks SB, Parker MW, Toole EH, Toole VK (1952) A reversible photoreaction controlling seed germination. Proc Natl Acad Sci USA 38:662–666
Bowe LM, Coat G, de Pamphilis CW (2000) Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proc Natl Acad Sci USA 97:4092–4097
Bünning E (1936) Die endogene tagesrhythmik als grundlage der photoperiodischen reaktion. Ber Dtsch Bot Ges 54:590–607
Castillon A, Shen H, Huq E (2007) Phytochrome interacting factors: Central players in phytochrome-mediated light signaling networks. Trends Plant Sci 12:514–521
Clapham D, Dormling I, Ekberg I, Eriksson G, Qamaruddin M, Vince-Prue D (1998a) Latitudinal cline of requirement for far-red light for the photoperiodic control of bud set and extension growth in Picea abies (Norway spruce). Physiol Plant 102:71–78
Clapham D, Ekberg I, Dormling I, Eriksson G, Qamaruddin M, Vince-Prue D (1998b) Dormancy: night timekeeping and day timekeeping for the photoperiodic control of bud set in Norway spruce. In: Lumsden PJ, Millar AJ (eds) Biological rhythms and photoperiodism in plants. BIOS Scientific Publishers, Oxford, pp 195–209
Clapham D, Kolukisaoglu HÜ, Larsson CT, Qamaruddin M, Wiegmann-Eirund C, Schneider-Poetsch HAW, von Arnold S (1999) Phytochrome types in Picea and Pinus. Expression patterns of PHYA-related types. Plant Mol Biol 40:669–678
Clapham D, Ekberg I, Eriksson G, Norell L, Vince-Prue D (2002) Requirement for far-red light to maintain secondary needle extension growth in northern but not southern populations of Pinus sylvestris (Scots pine). Physiol Plant 114:207–212
Conti L, Bradley D (2007) Terminal flower 1 is a mobile signal controlling Arabidopsis architecture. Plant Cell 19:767–778
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033
Dole JM, Wilkins HF (2005) Floriculture. Principles and species, 2nd edn. Pearson, New Jersey
Dormling I, Gustafsson Å, Wettstein D (1968) The experimental control of the life cycle in Picea abies (L.) Karst. Silvae Genet 17:44–64
Druart N, Johansson A, Baba K, Schrader J, Sjödin 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
Eriksson ME (2000) The role of phytochrome A and gibberellins in growth under long and short day conditions. Studies in hybrid aspen. Acta Universitatis Agriculturae Sueciae, Silvestria 164. Dissertation, Swedish Agricultural University
Eriksson M (2007) Low levels of phytochrome A expression alters circadian rhythm and change levels of flowering locus T leading to early bud set in Populus. Comp Biochem Physiol Part A 146:S231
Eriksson M, Millar J (2003) The circadian clock. A plant`s best friend in a spinning world. Plant Physiol 132:732–738
Eriksson ME, Moritz T (2002) Daylength and spatial expression of a gibberellin-20-oxidase isolated from hybrid aspen (Populus tremula L × P. tremuloides Michx). Planta 214:920–930
Franklin K (2009) Light and temperature signal crosstalk in plant development. Curr Opin Plant Biol 12:63–68
Frewen BE, Chen THH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845
Goffinet MC, Larson PR (1981) Structural changes in Populus deltoides terminal buds and in the vascular transition zone of the stems during dormancy induction. Amer J Bot 68:118
Gyllenstrand N, Clapham D, Källman T, Lagercrantz U (2007) A Norway spruce FLOWERING LOCUS T homolog is implicated in control of growth rhythm in conifers. Plant Physiol 144:248–257
Håbjørg A (1972) Effects of light quality, light intensity and night temperature on growth and development of three latitudinal populations of Betula pubescens. Ehrh Meld Norges landbrukshøgsk 51:1–17
Halliday KJ, Whitelam GC (2003) Changes in photoperiod or temperature alters the functional relationships between phytochromes and reveal roles for phyD and phyE. Plant Physiol 131:1913–1920
Halliday KL, Salter MG, Thingnæs E, Whitelam GC (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J 33:1–11
Hansen E, Olsen JE, Junttila O (1999) Gibberellins and subapical cell divisions in relation to bud set and bud break in Salix pentandra. J Plant Growth Regul 18:167–170
Hedman H, Källman T, Lagercrantz U (2009) Early evolution of the MFT-like gene family in plants. Plant Mol Biol 70:359–369
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 warming. Tree Physiol 23:931–936
Heide OM (2008) Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species. Scientia Hort 115:309–314
Heide OM, Prestrud K (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol 25:109–114
Heschel MS, Selby J, Butler C, Whitelam GC, Sharrock RA, Donohue K (2007) A new role for phytochromes in temperature-dependent germination. New Phytol 174:735–741
Holefors H, Rosnes AKR, Opseth L, Fossdal CG, Olsen JE (2009) Cloning and characterisation of CONSTANS like genes affected by photoperiod in Norway spruce. Plant Physiol Biochem 47:105–115
Holliday JA, Ralph SG, White R, Bohlmann J, Aitken SN (2008) Global monitoring of autumn gene expression within and among phenotypically divergent populations of Sitka spruce (Picea sitchensis). New Phytol 178:103–122
Horvath DP, Anderson JV, Chao WS, Foley M (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 11:534–540
Horvath DP, Chao WP, Suttle J, Thimmapuram J, Anderson JV (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions in leafy spurge (Euphorbia esula L.). BMC Genomics 9:536–552
Howe GT, Gardner G, Hackett WP, Furnier GR (1996) Phytochrome control of short-day-induced bud set in black cottonwood. Physiol Plant 97:95–103
Howe GT, Bucciaglia PA, Furnier GR, Hackett WP, Cordonnier-Pratt MM, Gardner G (1998) Evidence that the phytochrome gene family in black cottonwood has one PHYA locus and two PHYB loci, but lacks members of the PHYC/F and PHYE subfamilies. Mol Biol Evol 15:160–175
Huertz M, De Paoli E, Kallman T, Larsson H, Jurman I, Mortante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce (Picea abies (L.) Karst). Genetics 174:2095–2150
Igasaki T, Watanabe Y, Nishiguchi M, Kotoda N (2008) The FLOWERING LOCUS T/TERMINAL FLOWER 1 family in Lombardy poplar. Plant Cell Physiol 49:291–300
Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S (2006) Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European Aspen (Populus tremula, Salicaceae). Genetics 178:2217–2226
Junttila O (1976) Apical growth cessation and shoot tip abscission in Salix. Physiol Plant 38:278–286
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 (2007) Regulation of annual shoot growth cycle in northern tree species. In: Taulavuori E, Taulavuori K (eds) Physiology of northern plants under changing environment. Res Signpost, Kerala, pp 177–210
Junttila O, Jensen E (1988) Gibberellins and photoperiodic control of shoot elongation in Salix. Physiol Plant 74:371–376
Junttila O, Kaurin Å (1985) Climatic control of apical growth cessation in latitudinal ecotypes of Salix pentandra L. In: Kaurin Å, Junttila O, Nilsen J (eds) Plant production in the north. Norwegian University Press, Oslo, pp 83–91
Junttila O, Nilsen J, Igeland B (2002) Effect of temperature in the induction of bud dormancy in various ecotypes of Betula pubescens and B. pendula. 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 23:971–979
Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam G, Franklin K (2009) High temperature-mediated adaptations in plant architecture requires the bHLH transcription factor PIF4. Curr Biol 19:408–413
Kramer PJ, Kozlowski TT (1979) Physiology of woody plants. Academic press, New York
Kvaalen H, Johnsen Ø (2008) Timing of bud set in Picea abies is regulated by a memory of temperature during zygotic and somatic embryogenesis. New Phytol 177:49–59
Kvifte G, Hegg K, Hansen V (1983) Spectral distribution of solar radiation in the Nordic countries. J Climate Appl Meteorol 22:143–152
Kyriacou CP, Peixoto AA, Sandrelli F, Costa R, Tauber E (2007) Clines in clock genes: fine-tuning circadian rhythms to the environment. Trends Genetics 24:124–132
Lagercrantz U (2009) At the end of the day: a common molecular mechanism for photoperiod responses in plants? J Exp Bot 60:2501–2525
Lang GA (1987) Dormancy: a new universal terminology. HortScience 22:817–820
Matsuo T, Okamoto K, Onai K, Niwa Y, Shimigawara K, Ishiura M (2008) A systematic forward genetic analysis identified components of the Chlamydomonas circadian system. Genes Dev 22:918–930
Millington WF, Chanye WR (1973) Shedding of shoots and branches. In: Kozlowski TT (ed) Shedding of plant parts. Academic Press, New York, pp 149–204
Mølmann JA, Berhanu AT, Stormo SK, Ernstsen A, Junttila O, Olsen JE (2003) The 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
Mølmann JA, Asante DK, Jensen JB, Krane MN, 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 hybrid aspen. Plant Cell Environ 28:1579–1588
Mølmann JA, Junttila O, Johnsen Ø, Olsen JE (2006) Effects of red, far-red and blue light in maintaining growth in latitudinal populations of Norway spruce (Picea abies). Plant Cell Environ 29:166–172
Moritz T (1995) Biological activity, identification and quantification of gibberellins in seedlings of Norway spruce (Picea abies) grown under different photoperiods. Physiol Plant 95:67–72
Nienstaedt H (1967) Chilling requirements in seven Picea species. Silvae Genet 16:65–68
Nilsen J (1985) Light climate in northern areas. In: Junttila O, Nilsen J (eds) Plant production in the North (Kaurin Å. Tromsø, Norwegian University Press
Nitsch JP (1957) Photoperiodism in woody plants. Proc Am Soc Hort Sci 70:526–544
Okada R, Kondo S, Satbhai SB, Yamaguchi N, Tsukuda M, Aoki S (2009) Functional characterization of CCA1/LHY homolog genes PpCCA1a and PpCCA1b, in the moss Physcomitrella patens. Plant J. doi: 10.1111/j.1365-313X.2009.03979.x
Olsen JE, Jensen E, Junttila O, Moritz T (1995a) Photoperiodic control of endogenous gibberellins in seedlings of Salix pentandra. Physiol Plant 93:639–644
Olsen JE, Junttila O, Moritz T (1995b) A localised decrease of GA1 in shoot tips of Salix pentandra seedlings precedes cessation of shoot elongation under short photoperiod. Physiol Plant 95:627–632
Olsen JE, Junttila O, Nilsen J, Eriksson ME, Martinussen I, Olsson O, Sandberg G, Moritz T (1997a) Ectopic expression of oat phytochrome A in Hybrid aspen changes critical daylength for growth and prevents cold acclimatization. Plant J 12:1339–1350
Olsen JE, Junttila O, Moritz T (1997b) Long day-induced bud break in Salix pentandra is associated with transiently elevated levels of GA1 and gradual increase in IAA. Plant Cell Physiol 38:536–540
Ophir R, Pang X, Halaly T, Venkateswari J, Lavee S, Galbraith, Or E (2009) Gene expression profiling of grape bud response to two alternative dormancy-release stimuli expose possible links between impaired mitochondrial activity, hypoxia, ethylene-ABA interplay and cell enlargement. Plant Mol Biol. doi: 10.1007/s11103-009-9531-9
Pauley SS, Perry TO (1954) Ecotypic variation of the photoperiodic response in Populus. J Arnold Arboretum 35:167–188
Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628
Ramos A, Perez-Solis E, Ibanez C, Casado R, Collada C, Gomez L, Aragoncillo C, Allona I (2005) Winter disruption of the circadian clock in chestnut. Proc Natl Acad Sci 102:7037–7042
Rohde A, Bhalerao R (2007) Dormancy in the perennial context. Trends in Plant Sci 12:217–223
Rohde A, Prinsen E, De Rycke R, Engler G, van Montagu M, Boerjan W (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in Poplar. Plant Cell 14:1885–1901
Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58:4047–4060
Romero JM, Valverde F (2009) Evolutionary conserved photoperiod mechanisms in plants. Plant Signaling Behaviour 4:642–644
Ruonala R, Rinne PLH, Baghour M, Moritz T, Tuominen H, Kangasjärvi J (2006) Transitions of the functioning of the shoot apical meristem in birch (Betula pendula) involve ethylene. Plant J 46:628–640
Ruonala R, Rinne PLH, Kangasjärvi J, van der Schoot C (2008) CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. Plant Cell 20:59–74
Ruttink T, Arend M, Morreell K, Storme V, Rombauts S, Fromm J, Bhalerao R, Boerjan W, Rohde A (2007) A molecular time table for apical bud formation and dormancy induction in Poplar. Plant Cell 19:2370–2390
Sachs RM (1965) Stem elongation. Annu Rev Plant Physio l16:73–96
Serrano G, Herrera-Palau R, Romero JM, Serrano A, Coupland G, Valverde F (2009) Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Curr Biol 19:359–368
Shimizu M, Ichikawa K, Aoki S (2004) Photoperiod-regulated expression of the PpCOL1 gene encoding a homolog of CO/COL proteins in the moss Physcomitrella patens. Biochem Biophys Res Comm 324:1296–1301
Kalcsits L, Silim S, Tanino K (2009b) Temperature influence on dormancy induction in woody plants. In: Gusta LV, Wisniewski M, Tanino K (eds) Plant cold hardiness from the laboratory to the field. CABI press, Wallingford, UK, pp 108–118
Søgaard G, Johnsen Ø, Nilsen J, Junttila O (2008) Climatic control of bud burst in young seedlings of nine provenances of Norway spruce. Tree Physiol 28:311–320
Stavang JA, Ernsten A, Lindgård B, Lid S, Moe R, Olsen JE (2005) Thermoperiodic regulation of shoot elongation is mediated by transcriptional regulation of GA inactivation in pea. Plant Physiol 138:2344–2353
Stavang JA, Junttila O, Moe R, Olsen JE (2007) Differential temperature regulation of GA metabolism in light and darkness. J Exp Bot 58:3061–3069
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 60:589–601
Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120
Svendsen E, Wilen R, Liu R, Tanino KK (2007) A molecular marker associated with dormancy induction in northern and southern ecotypes of red-osier dogwood. Tree Physiol 27:385–397
Swain SM, Singh DP (2005) Tall tales from sly dwarfs: novel functions of gibberellins in plant development. Trends Plant Sci 10:1360–1385
Sylven N (1939) Long and short day types of Swedish forest trees. Svensk Papperstidning 43:317–354
Takata N, Saito S, Tanaka-Saito C, Nanjo T, Shinohara K, Uemura M (2009) Molecular phylogeny and expression of poplar circadian clock genes, LHY1 and LHY2. New Phytol 181:808–819
Thomas B, Vince-Prue D (1995) Do long-day plants and short-day plants perceive daylength in the same way? Flowering Newslett 20:50–57
Thomas B, Vince-Prue D (1997) Photoperiodism in plants. Academic Press, London
Vaartaja O (1959) Evidence of photoperiodic ecotypes in trees. Ecol Monogr 29:91–111
Vidal AM, Ben-Cheikh W, Talon M, Garcia-Martinez JL (2003) Regulation of gibberellin 20-oxidase and gibberellin content in citrus by temperature and cirtrus exocortis viroid. Planta 217:442–448
Vince Prue D (1984) Contrasting types of photoperiodic response in the control of dormancy. Plant Cell Environ 7:507–513
Vince-Prue D, Clapham DH, Ekberg I, Norell L (2001) Circadian timekeeping for the photoperiodic control of budset in Picea abies (Norway spruce) seedlings. Biol Rhytm Res 32:479–487
Weiser CJ (1970) Cold resistance and injury in woody plants. Science 169:1269–1278
Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181
Welling A, Palva ET (2008) Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol 147:1199–1211
Westergaard L, Eriksen EN (1997) Autumn temperature affects the induction of dormancy in first-year seedlings of Acer platanoides L. Scand J For Res 12:11–16
Worrall J, Mergen F (1967) Environmental and genetic control of dormancy in Picea abies. Physiol Plant 20:733–745
Zobell O, Coupland G, Reiss B (2005) The family of CONSTANS-like genes in Physcomitrella patens. Plant Biol 7:266–275
Acknowledgments
The Norwegian Research Council (grant 191455) is acknowledged for financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Olsen, J.E. Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Mol Biol 73, 37–47 (2010). https://doi.org/10.1007/s11103-010-9620-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-010-9620-9