Skip to main content
SpringerLink
Log in
Book cover

Survival Strategies in Extreme Cold and Desiccation pp 129–147Cite as

Mechanism of Overwintering in Trees

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1081))

Abstract

Boreal trees possess very high freezing resistance, which is induced by short-day length and low temperatures, in order to survive severe subzero temperatures in winter. During autumn, cooperation of photoreceptors and circadian clock system perceiving photoperiod shortening results in growth cessation, dormancy development, and first induction of freezing resistance. The freezing resistance is further enhanced by subsequent low temperature during seasonal cold acclimation with concomitant changes in various morphological and physiological features including accumulation of sugars and late embryogenesis abundant proteins. The mechanism of adaptation to freezing temperatures differs depending on the type of tissue in boreal trees. For example, bark, cambium, and leaf cells tolerate freezing-induced dehydration by extracellular freezing, whereas xylem parenchyma cells avoid intracellular freezing by deep supercooling. In addition, dormant buds in some trees respond by extraorgan freezing. Boreal trees have evolved overwintering mechanisms such as dormancy and high freezing resistance in order to survive freezing temperatures in winter.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

ABA:

Abscisic acid

CCA1:

Circadian clock associated 1

CO:

Constans

CRY:

Cryptochrome

DREB1/CBF:

Dehydration-responsive element-binding 1/C-repeat binding factor

DTA:

Differential thermal analysis

EC:

Evening complex

ELF:

Early flowering

ER:

Endoplasmic reticulum

FT:

Flowering locus T

FTL:

Flowering locus T/terminal flower 1-like

LD:

Long day

LHY:

Late elongated hypocotyl

LT:

Low temperature

LTE:

Low-temperature exotherm

LUX:

Lux arrhythmo

MPL:

Multiplex lamellae

PHY:

Phytochrome

PRR:

Pseudo-response regulator

SD:

Short day

TOC1:

Timing of CAB2 expression 1

WT:

Wild type

XRPC:

Xylem ray parenchyma cells

References

  • Adams S, Manfield I, Stockley P, Carré IA (2015) Revised morning loops of the Arabidopsis circadian clock based on analyses of direct regulatory interactions. PLoS One 10:e0143943

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alabadí D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883

    Article  PubMed  Google Scholar 

  • Arora R, Wisniewski M (1994) Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch) II. A 60-kilodalton bark protein in cold-acclimated tissues of peach is heat stable and related to the dehydrin family of proteins. Plant Physiol 105:95–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci U S A 93:13404–13409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashworth EN, Abeles FB (1984) Freezing behavior of water in small pores and the possible role in the freezing of plant tissues. Plant Physiol 76:201–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashworth EN, Davis GA, Wisniewski ME (1989) The formation and distribution of ice within dormant and deacclimated peach flower buds. Plant Cell Environ 12:607–612

    Article  Google Scholar 

  • Avia K, Kärkkäinen K, Lagercrantz U, Savolainen O (2014) Association of FLOWERING LOCUS T/TERMINAL FLOWER 1-like gene FTL2 expression with growth rhythm in Scots pine (Pinus sylvestris). New Phytol 204:159–170

    Article  CAS  PubMed  Google Scholar 

  • Bassett CL, Wisniewski ME, Artlip TS, Norelli JL, Renaut J, Farrel RE Jr (2006) Global analysis of genes regulated by low temperature and photoperiod in peach bark. J Am Soc Hortic Sci 131:551–563

    CAS  Google Scholar 

  • Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner NP, Finn CE, Chen TH, Hurry V (2006) The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ 29:1259–1272

    Article  CAS  PubMed  Google Scholar 

  • Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, 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

    Article  PubMed  CAS  Google Scholar 

  • Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GT, Batschauer A, Ahmad M (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Tian Q, Pang T, Jiang L, Wu R, Xia X, Yin W (2014) Deep-sequencing transcriptome analysis of low temperature perception in a desert tree, Populus euphratica. BMC Genomics 15:326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow BY, Sanchez SE, Breton G, Pruneda-Paz JL, Krogan NT, Kay SA (2014) Transcriptional regulation of LUX by CBF1 mediates cold input to the circadian clock in Arabidopsis. Curr Biol 24:1518–1524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christersson L (1978) The influence of photoperiod and temperature on the development of frost hardiness in seedlings of Pinus sylvestris and Picea abies. Plant Physiol 44:288–294

    Article  Google Scholar 

  • Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45

    Article  CAS  PubMed  Google Scholar 

  • Cloix C, Kaiserli E, Heilmann M, Baxter KJ, Brown BA, O'Hara A, Smith BO, Christie JM, Jenkins GI (2012) C-terminal region of the UV-B photoreceptor UVR8 initiates signaling through interaction with the COP1 protein. Proc Natl Acad Sci U S A 109:16366–16370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooke JE, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728

    Article  CAS  PubMed  Google Scholar 

  • Crowe JH, Crowe LM, Carpenter JF, Rudolph AS, Wistrom CA, Spargo BJ, Anchordoguy TJ (1988) Interaction of sugars with membranes. Biochim Biopys Acta 947:367–384

    Article  CAS  Google Scholar 

  • Dong MA, Farré EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci U S A 108:7241–7246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drira M, Saibi W, Brini F, Gargouri A, Masmoudi K, Hanin M (2013) The K-segments of the wheat dehydrin DHN-5 are essential for the protection of lactate dehydrogenase and β-glucosidase activities in vitro. Mol Biotechnol 54:643–650

    Article  CAS  PubMed  Google Scholar 

  • El Kayal W, Allen CC, Ju CJ, Adams E, King-Jones S, Zaharia LI, Abrams SR, Cooke JE (2011) Molecular events of apical bud formation in white spruce, Picea glauca. Plant Cell Environ 34:480–500

    Article  PubMed  CAS  Google Scholar 

  • Endoh K, Kasuga J, Arakawa K, Ito T, Fujikawa S (2009) Cryo-scanning electron microscopic study on freezing behaviors of tissue cells in dormant buds of larch (Larix kaempferi). Cryobiology 59:214–222

    Article  PubMed  Google Scholar 

  • Endoh K, Kuwabara C, Arakawa K, Fujikawa S (2014) Consideration of the reasons why dormant buds of trees have evolved extraorgan freezing as an adaptation for winter survival. Environ Exp Bot 106:52–59

    Article  Google Scholar 

  • Fernández M, Troncoso V, Valenzuela S (2015) Transcriptome profile in response to frost tolerance in Eucalyptus globulus. Plant Mol Biol Rep 33:1472–1485

    Article  CAS  Google Scholar 

  • Frewen BE, Chen TH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD Jr (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujikawa S (2016) Plant responses to freezing. eLS. Wiley, Chichester, pp 1–9. https://doi.org/10.1002/9780470015902.a0023719

    Book  Google Scholar 

  • Fujikawa S, Kuroda K (2000) Cryo-scanning electron microscopic study on freezing behavior of xylem ray parenchyma cells in hardwood species. Micron 31:669–686

    Article  CAS  PubMed  Google Scholar 

  • Fujikawa S, Miura K (1986) Plasma membrane ultrastructural changes caused by mechanical stress in the formation of extracellular ice as a primary cause of slow freezing injury in fruit-bodies of Basidiomycetes (Lyophyllum ulmarium (Fr.) Kuhner). Cryobiology 23:371–382

    Article  Google Scholar 

  • Fujikawa S, Steponkus PL (1990) Freeze-induced alterations in the ultrastructure of the plasma membrane of rye protoplasts isolated from cold acclimated leaves. Cryobiology 27:665–666

    Google Scholar 

  • Fujikawa S, Takabe K (1996) Formation of multiplex lamellae by equilibrium slow freezing of cortical parenchyma cells of mulberry and its possible relationship to freezing tolerance. Protoplasma 190:189–203

    Article  Google Scholar 

  • Fujikawa S, Ukaji N, Nagao M, Yamane K, Takezawa D, Arakawa K (2006) Functional role of winter-accumulating proteins from mulberry tree in adaptation to winter-induced stresses. In: Chen THH, Uemura M, Fujikawa S (eds) Cold hardiness in plants: molecular genetics, cell biology and physiology. CABI, Wallingford, pp 181–202

    Google Scholar 

  • Fujikawa S, Kasuga J, Takata N, Arakawa K (2009) Factors related to change of deep supercooling capability in xylem parenchyma cells of trees. In: Gusta LV, Wisniewski ME, Tanino KK (eds) Plant cold hardiness: from the laboratory to the field. CABI, Wallingford, pp 29–42

    Chapter  Google Scholar 

  • Galindo González LM, El Kayal W, Ju CJ, Allen CC, King-Jones S, Cooke JE (2012) Integrated transcriptomic and proteomic profiling of white spruce stems during the transition from active growth to dormancy. Plant Cell Environ 35:682–701

    Article  PubMed  CAS  Google Scholar 

  • George MF, Burke MJ, Pellet HM, Johnson AG (1974) Low temperature exotherms and woody plant distribution. Hortscience 9:519–522

    Google Scholar 

  • George MF, Becwar MR, Burke MJ (1982) Freezing avoidance by deep supercooling of tissue water in winter-hardy plants. Cryobiology 19:628–639

    Article  CAS  PubMed  Google Scholar 

  • Gordon-Kamm WJ, Steponkus PL (1984) Lamellar-to-hexagonal II phase transitions in the plasma membrane of isolated protoplasts after freeze-induced dehydration. Proc Natl Acad Sci U S A 81:6373–6377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gusta LV, Tyler NJ, Chen THH (1983) Deep undercooling in woody taxa growing north of the −40°C isotherm. Plant Physiol 72:122–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gyllenstrand N, Karlgren A, Clapham D, Holm K, Hall A, Gould PD, Källman T, Lagercrantz U (2014) No time for spruce: rapid dampening of circadian rhythms in Picea abies (L. Karst). Plant Cell Physiol 55:535–550

    Article  CAS  PubMed  Google Scholar 

  • Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav 6:1503–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298

    CAS  PubMed  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657–662

    Article  CAS  PubMed  Google Scholar 

  • Heide OM (1974) Growth and dormancy in Norway spruce ecotypes (Picea abies) I. Interaction of photoperiod and temperature. Physiol Plant 30:1–12

    Article  Google Scholar 

  • Howell GS, Weiser CJ (1970a) The environmental control of cold acclimation in apple. Plant Physiol 45:390–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howell GS, Weiser CJ (1970b) Fluctuations in the cold resist ace of apple twigs during spring dehardening. J Am Soc Hortic Sci 95:190–192

    Google Scholar 

  • Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM et al (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci U S A 108:10756–10761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Jiang Y, Han X, Wang H, Pan J, Yu D (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J Exp Bot 68:1361–1369

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Pérez-García P, Pokhilko A, Millar AJ, Antoshechkin I, Riechmann JL, Mas P (2012) Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator. Science 336:75–79

    Article  CAS  PubMed  Google Scholar 

  • Ibañez C, Ramos A, Acebo P, Contreras A, Casado R, Allona I, Aragoncillo C (2008) Overall alteration of circadian clock gene expression in the chestnut cold response. PLoS One 3:e3567

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ibáñez C, Kozarewa I, Johansson M, Ogren E, Rohde A, Eriksson ME (2010) Circadian clock components regulate entry and affect exit of seasonal dormancy as well as winter hardiness in Populus trees. Plant Physiol 153:1823–1833

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ingvarsson PK, García MV, Hall D, Luquez V, Jansson S (2006) Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172:1845–1853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa M, Ishikawa M, Toyomasu T, Aoki T, Price WS (2015) Ice nucleation activity in various tissues of Rhododendron flower buds: their relevance to extraorgan freezing. Front Plant Sci 6:149

    Article  PubMed  PubMed Central  Google Scholar 

  • Ito S, Song YH, Imaizumi T (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol Plant 5:573–582

    Article  PubMed  CAS  Google Scholar 

  • Johansson M, Ramos-Sánchez JM, Conde D, Ibáñez C, Takata N, Allona I, Eriksson ME (2015) Role of the circadian clock in cold acclimation and winter dormancy in perennial plants. In: Anderson J (ed) Advances in dormancy. Springer, New York, pp 51–74

    Google Scholar 

  • Jung J-H, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S, Kumar M, Grant A, Locke JCW, Schäfer E, Jaeger KE, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354:886–889

    Article  CAS  PubMed  Google Scholar 

  • Junttila O (1980) Effect of photoperiod and temperature on apical growth cessation in two ecotypes of Salix and Betula. Physiol Plant 48:347–352

    Article  Google Scholar 

  • Junttila O, Kaurin Å (1990) Environmental control of cold acclimation in Salix pentandra. Scand J For Res 5:195–204

    Article  Google Scholar 

  • Kalcsits L, Silim S, Tanino K (2009) Warm temperature accelerates short photoperiod-induced growth cessation and dormancy induction in hybrid poplar (Populus × spp.). Trees 23:973–979

    Article  Google Scholar 

  • Karimi R, Ershadi A (2015) Role of exogenous abscisic acid in adapting of ‘Sultana’ grapevine to low-temperature stress. Acta Physiol Plant 37:151

    Article  CAS  Google Scholar 

  • Karlgren A, Gyllenstrand N, Källman T, Sundström JF, Moore D, Lascoux M, Lagercrantz U (2011) Evolution of the PEBP gene family in plants: functional diversification in seed plant evolution. Plant Physiol 156:1967–1977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karlgren A, Gyllenstrand N, Clapham D, Lagercrantz U (2013a) FLOWERING LOCUS T/TERMINAL FLOWER1-like genes affect growth rhythm and bud set in Norway spruce. Plant Physiol 163:792–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karlgren A, Gyllenstrand N, Källman T, Lagercrantz U (2013b) Conserved function of core clock proteins in the gymnosperm Norway spruce (Picea abies L. Karst). PLoS One 8:e60110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasuga J, Arakawa K, Fujikawa S (2007) High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytol 174:569–579

    Article  CAS  PubMed  Google Scholar 

  • Kasuga J, Hashidoko Y, Nishioka A, Yoshiba M, Arakawa K, Fujikawa S (2008) Deep supercooling xylem parenchyma cells of katsura tree (Cercidiphyllum japocum) contain flavonol glycosides exhibiting high anti-ice nucleation activity. Plant Cell Environ 31:1335–1348

    Article  CAS  PubMed  Google Scholar 

  • Kasuga J, Endoh K, Yoshiba M, Taido I, Arakawa K, Uemura M, Fujikawa S (2013) Roles of cell walls and intracellular contents in supercooling capability of xylem parenchyma cells of boreal trees. Physiol Plant 148:25–35

    Article  CAS  PubMed  Google Scholar 

  • Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36:141–154

    Article  CAS  PubMed  Google Scholar 

  • Kim JY, Song HR, Taylor BL, Carré IA (2003) Light-regulated translation mediates gated induction of the Arabidopsis clock protein LHY. EMBO J 22:935–944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koster KL, Webb MS, Bryant G, Lynch DV (1994) Interactions between soluble sugars and POPC (1-palmitoyl-2-oleoylphosphatidylcholine) during dehydration: vitrification of sugars alter the phase behavior of the phospholipid. Biochim Biophys Acta 1193:143–150

    Article  CAS  PubMed  Google Scholar 

  • Kozarewa I, Ibáñez C, Johansson M, Ogren E, Mozley D, Nylander E, Chono M, Moritz T, Eriksson ME (2010) Alteration of PHYA expression change circadian rhythms and timing of bud set in Populus. Plant Mol Biol 73:143–156

    Article  CAS  PubMed  Google Scholar 

  • Kuroda K, Kasuga J, Arakawa K, Fujikawa S (2003) Xylem ray parenchyma cells in boreal hardwood species respond to subfreezing temperatures by deep supercooling that is accompanied by incomplete desiccation. Plant Physiol 131:736–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuwabara C, Kasuga J, Wang D, Fukushi Y, Arakawa K, Koyama T, Inada T, Fujikawa S (2011) Changes of supercooling capability in solutions containing different kinds of ice nucleators by flavonol glycosides from deep supercooling xylem parenchyma cells in trees. Cryobiology 63:157–163

    Article  CAS  PubMed  Google Scholar 

  • Kuwabara C, Wang D, Kasuga J, Fukushi Y, Arakawa K, Koyama T, Inada T, Fujikawa S (2012) Freezing activities of flavonoids in solutions containing different ice nucleators. Cryobiology 64:279–285

    Article  CAS  PubMed  Google Scholar 

  • Larcher W (2003) Physiological plant ecology, 4th edn. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Legris M, Klose C, Burgie ES, Rojas CC, Neme M, Hiltbrunner A, Wigge PA, Schäfer E, Vierstra RD, Casal JJ (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354:897–900

    Article  CAS  PubMed  Google Scholar 

  • Leyva-Pérez MD, Valverde-Corredor A, Valderrama R, Jiménez-Ruiz J, Muñoz-Merida A, Trelles O, Barroso JB, Mercado-Blanco J, Luque F (2015) Early and delayed long-term transcriptional changes and short-term transient responses during cold acclimation in olive leaves. DNA Res 22:1–11

    Article  CAS  Google Scholar 

  • Li FW, Mathews S (2016) Evolutionary aspects of plant photoreceptors. J Plant Res 129:115–122

    Article  CAS  PubMed  Google Scholar 

  • Li C, Puhakainen T, Welling A, Viherä-Aarnio A, Ernstsen A, Junttila O, Heino P, Palva T (2002) Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes. Physiol Plant 116:478–488

    Article  CAS  Google Scholar 

  • Li C, Junttila O, Ernstsen A, Heino P, Palva ET (2003a) Photoperiodic control of growth, cold acclimation and dormancy development in silver birch (Betula pendula) ecotypes. Physiol Plant 117:206–212

    Article  CAS  Google Scholar 

  • Li C, Junttila O, Heino P, Palva ET (2003b) Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application. Tree Physiol 23:481–487

    Article  CAS  PubMed  Google Scholar 

  • Li C, Welling A, Puhakainen T, Viherä-Aarnio A, Ernstsen A, Junttila O, Heino P, Palva ET (2005) Differential responses of silver birch (Betula pendula) ecotypes to short-day photoperiod and low temperature. Tree Physiol 25:1563–1569

    Article  CAS  PubMed  Google Scholar 

  • Li FW, Villarreal JC, Kelly S, Rothfels CJ, Melkonian M, Frangedakis E, Ruhsam M, Sigel EM, Der JP, Pittermann J et al (2014) Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. Proc Natl Acad Sci U S A 111:6672–6677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li FW, Melkonian M, Rothfels CJ, Villarreal JC, Stevenson DW, Graham SW, Wong GK, Pryer KM, Mathews S (2015) Phytochrome diversity in green plants and the origin of canonical plant phytochromes. Nat Commun 6:7852

    Article  CAS  PubMed  Google Scholar 

  • Liu LJ, Zhang YC, Li QH, Sang Y, Mao J, Lian HL, Wang L, Yang HQ (2008) COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20:292–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maestrini P, Cavallini A, Rizzo M, Giordani T, Bernardi R, Durante M, Natali L (2009) Isolation and expression analysis of low temperature-induced genes in white poplar (Populus alba). J Plant Physiol 166:1544–1556

    Article  CAS  PubMed  Google Scholar 

  • Makino S, Matsushika A, Kojima M, Oda Y, Mizuno T (2001) Light response of the circadian waves of the APRR1/TOC1 quintet: when does the quintet start singing rhythmically in Arabidopsis? Plant Cell Physiol 42:334–339

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Los DA (1997) Membrane fluidity and temperature perception. Plant Physiol 115:875–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagel DH, Kay SA (2012) Complexity in the wiring and regulation of plant circadian networks. Curr Biol 22:R648–R657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T (2005) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46:686–698

    Article  CAS  PubMed  Google Scholar 

  • Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50:447–462

    Article  CAS  PubMed  Google Scholar 

  • Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin YC, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A et al (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584

    Article  CAS  PubMed  Google Scholar 

  • 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 acclimatization. Plant J 12:1339–1350

    Article  CAS  Google Scholar 

  • Pallardy SG (2008) Physiology of woody plants, 3rd edn. Elsevier, Burlington

    Google Scholar 

  • Pauley SS, Perry TO (1954) Ecotypic variation of the photoperiodic response in Populus. J Arnold Arbor 35:167–188

    Google Scholar 

  • Pearce RS, Willison JHM (1985) A freeze-etch study of the effects of extracellular freezing on cellular membranes of wheat. Planta 163:304–316

    Article  CAS  PubMed  Google Scholar 

  • Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8:574

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Preston JC, Sandve SR (2013) Adaptation to seasonality and the winter freeze. Front Plant Sci 4:1–18

    Google Scholar 

  • Quamme H, Stushnoff C, Weiser CJ (1972) The relationship of exotherms to cold injury in apple stem tissues. J Am Soc Hortic Sci 97:608–613

    Google Scholar 

  • Ramos A, Pérez-Solís E, Ibáñez C, Casado R, Collada C, Gómez L, Aragoncillo C, Allona I (2005) Winter disruption of the circadian clock in chestnut. Proc Natl Acad Sci U S A 102:7037–7042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renaut J, Hausman J-F, Bassett C, Artlip T, Cauchie H-M, Witters E, Wisniewski M (2008) Quantitative proteomic analysis of short photoperiod and low-temperature responses in bark tissues of peach (Prunus persica L. Batsch). Tree Genet Genomes 4:589–600

    Article  Google Scholar 

  • Rinne P, Welling A, Kaikuranta P (1998) Onset of freezing tolerance in birch (Betula pubescens Ehrh.) involves LEA proteins and osmoregulation and is impaired in an ABA deficient genotype. Plant Cell Environ 21:601–611

    Article  CAS  Google Scholar 

  • Rizzini L, Favory JJ, Cloix C, Faggionato D, O'Hara A, Kaiserli E, Baumeister R, Schäfer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106

    Article  CAS  PubMed  Google Scholar 

  • Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223

    Article  CAS  PubMed  Google Scholar 

  • Sagisaka S, Asada M, Ahn YH (1990) Ultrastructure of poplar cortical cells during the transition from growing to wintering stages and vice versa. Trees 4:120–127

    Article  Google Scholar 

  • Sakai A (1966) Studies of frost hardiness in woody plants. II. Effect of temperature on hardening. Plant Physiol 41:353–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai A (1982) Freezing tolerance of shoot and flower primordia of coniferous buds by extraorgan freezing. Plant Cell Physiol 23:1219–1227

    Article  Google Scholar 

  • Sakai A, Larcher W (1987) Frost survival in plants: responses and adaptations to freezing stress. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Sauter JJ, Wisniewski M, Witt W (1996) Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus × canadensis Moench <robusta>) wood. J Plant Physiol 149:451–461

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Singh RK, Svystun T, AlDahmash B, Jönsson AM, Bhalerao RP (2017) Photoperiod- and temperature-mediated control of phenology in trees – a molecular perspective. New Phytol 213:511–524

    Article  CAS  PubMed  Google Scholar 

  • Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584

    Article  CAS  Google Scholar 

  • Steponkus PL, Webb MS (1992) Freeze-induced dehydration and membrane destabilization in plants. In: Somero GN, Osmond CB, Bolis CL (eds) Water and life: comparative analysis of water relationships at the organismic, cellular and molecular level. Springer, Berlin, pp 338–362

    Chapter  Google Scholar 

  • Steponkus PL, Uemura M, Webb MS (1993) A contrast of the cryostability of the plasma membrane of winter rye and spring oat. Two species that widely differ in their freezing tolerance and plasma membrane lipid composition. In: Steponkus PL (ed) Advances in low-temperature biology, vol 2. JAI Press, London, pp 211–312

    Google Scholar 

  • Suárez-López 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

    Article  PubMed  Google Scholar 

  • Suzuki I, Los DA, Kanesaki Y, Mikami K, Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19:1327–1334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takata N, Kasuga J, Takezawa D, Arakawa K, Fujikawa S (2007) Gene expression associated with increased supercooling capability in xylem parenchyma cells of larch (Larix kaempferi). J Exp Bot 58:3731–3742

    Article  CAS  PubMed  Google Scholar 

  • Takata N, Saito S, Saito CT, Nanjo T, Shinohara K, Uemura M (2009) Molecular phylogeny and expression of poplar circadian clock genes, LHY1 and LHY2. New Phytol 181:808–819

    Article  CAS  PubMed  Google Scholar 

  • Takata N, Saito S, Saito CT, Uemura M (2010) Phylogenetic footprint of the plant clock system in angiosperms: evolutionary processes of pseudo-response regulators. BMC Evol Biol 10:126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tanino KK, Kalcsits L, Silim S, Kendall E, Gray GR (2010) 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

    Article  CAS  PubMed  Google Scholar 

  • Taulavuori K, Taulavuori E, Sarjala T, Savonen E-M, Pietiläinen P, Lähdesmäki P, Laine K (2000) In vivo chlorophyll fluorescence is not always a good indicator of cold hardiness. J Plant Physiol 157:227–229

    Article  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF, Gilmour SJ, Stockinger EJ, Jaglo-Ottosen KR, Zarka DG (2001) Role of the Arabidopsis CBF transcriptional activators in cold acclimation. Physiol Plant 112:171–175

    Article  CAS  Google Scholar 

  • Uemura M, Yoshida S (1984) Improvement of plasma membrane alterations in cold acclimation of winter rye seedlings (Scale cereal L. cv. Puma). Plant Physiol 75:818–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uemura U, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wallner SJ, Wu MT, Anderson-Krengel SJ (1986) Changes in extracellular polysaccharides during cold acclimation of cultured pear cells. J Am Soc Hortic Sci 111:769–773

    CAS  Google Scholar 

  • Wang ZY, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93:1207–1217

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Kasuga J, Kuwabara C, Endoh K, Fukushi Y, Fujikawa S, Arakawa K (2012) Presence of supercooling-facilitating (anti-ice nucleation) hydrolyzable tannins in deep supercooling xylem parenchyma cells in Cercidiphyllum japonicum. Planta 235:747–759

    Article  CAS  PubMed  Google Scholar 

  • Weiser CJ (1970) Cold resistance and injury in woody plants: knowledge of hardy plant adaptations to freezing stress may help us to reduce winter damage. Science 169:1269–1278

    Article  CAS  PubMed  Google Scholar 

  • Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181

    Article  CAS  Google Scholar 

  • Welling A, Kaikuranta P, Rinne P (1997) Photoperiodic induction of dormancy and freezing tolerance in Betula pubescens. Involvement of ABA and dehydrins. Physiol Plant 100:119–125

    Article  CAS  Google Scholar 

  • Welling A, Moritz T, Palva ET, Junttila O (2002) Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen. Plant Physiol 129:1633–1641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wingler A (2015) Comparison of signaling interactions determining annual and perennial plant growth in response to low temperature. Front Plant Sci 5:794

    Article  PubMed  PubMed Central  Google Scholar 

  • Wisniewski M (1995) Deep supercooling in woody plants and the role of cell wall structure. In: Lee RE, Warren GJ, Gusta LV (eds) Biological ice nucleation and its applications. APS Press, Minneapolis, pp 163–181

    Google Scholar 

  • Wisniewski M, Davis G (1989) Evidence for the involvement of a specific cell wall layer in regulation of deep supercooling of xylem parenchyma. Plant Physiol 91:151–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wisniewski M, Davis G (1995) Immunogold localization of pectins and glycoproteins in tissues of peach with reference to deep supercooling. Trees 9:253–260

    Article  Google Scholar 

  • Wisniewski M, Webb R, Balsamo R, Close TJ, Yu X-M, Griffith M (1999) Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol Plant 105:600–608

    Article  CAS  Google Scholar 

  • Wisniewski M, Norelli J, Bassett C, Artlip T, Macarisin D (2011) Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus x domestica) results in short-day induced dormancy and increased cold hardiness. Planta 233:971–983

    Article  CAS  PubMed  Google Scholar 

  • Wisniewski M, Gusta L, Neuner G (2014) Adaptive mechanisms of freeze avoidance in plants: a brief update. Environ Exp Bot 99:133–140

    Article  CAS  Google Scholar 

  • Zhang G, Ryyppö A, Vapaavuori E, Repo T (2003) Quantification of additive response and stationarity of frost hardiness by photoperiod and temperature in Scots pine. Can J For Res 33:1772–1784

    Article  Google Scholar 

  • Zhou B-L, Arakawa K, Fujikawa S, Yoshida S (1994) Cold-induced alterations in plasma membrane proteins that are specifically related to the development of freezing tolerance in cold-hardy winter wheat. Plant Cell Physiol 35:175–182

    CAS  Google Scholar 

Download references

Acknowledgments

Some studies cited in this chapter were partially supported by the Japan Society for the Promotion of Science under a Grant-in-Aid for Scientific Research (KAKENHI) [grant numbers: 15H04615, 23580453, 20580360 (KA)].

Author information

Authors and Affiliations

  1. Research Faculty and Graduate School of Agriculture, Hokkaido University, Sapporo, Japan

    Keita Arakawa

  2. Research Center for Global Agromedicine, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Japan

    Jun Kasuga

  3. Forest Research and Management Organization, Forestry and Forest Products Research Institute, Forest Bio-Research Center, Hitachi, Japan

    Naoki Takata

Authors
  1. Keita Arakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jun Kasuga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naoki Takata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keita Arakawa .

Editor information

Editors and Affiliations

  1. Faculty of Agriculture, Kyushu University, Fukuoka, Japan

    Mari Iwaya-Inoue

  2. Center for Biological Resources and Informatics, Tokyo Institute of Technology, Yokohama, Japan

    Minoru Sakurai

  3. United Graduate School of Agricultural Sciences and Department of Plant-biosciences, Faculty of Agriculture, Iwate University, Morioka, Japan

    Matsuo Uemura

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Arakawa, K., Kasuga, J., Takata, N. (2018). Mechanism of Overwintering in Trees. In: Iwaya-Inoue, M., Sakurai, M., Uemura, M. (eds) Survival Strategies in Extreme Cold and Desiccation. Advances in Experimental Medicine and Biology, vol 1081. Springer, Singapore. https://doi.org/10.1007/978-981-13-1244-1_8

Download citation

Publish with us

Policies and ethics

Search

Navigation