Skip to main content

Physiological and molecular changes in plants grown at low temperatures

Abstract

Apart from water availability, low temperature is the most important environmental factor limiting the productivity and geographical distribution of plants across the world. To cope with cold stress, plant species have evolved several physiological and molecular adaptations to maximize cold tolerance by adjusting their metabolism. The regulation of some gene products represents an additional mechanism of cold tolerance. A consequence of these mechanisms is that plants are able to survive exposure to low temperature via a process known as cold acclimation. In this review, we briefly summarize recent progress in research and hypotheses on how sensitive plants perceive cold. We also explore how this perception is translated into changes within plants following exposure to low temperatures. Particular emphasis is placed on physiological parameters as well as transcriptional, post-transcriptional and post-translational regulation of cold-induced gene products that occur after exposure to low temperatures, leading to cold acclimation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

ABA:

Abscisic acid

CBF:

C-repeat binding factor

COR :

Cold-responsive genes

CRT:

C-repeat elements

DRE:

Dehydration-responsive elements

DREB:

Dehydration-responsive element binding

ICE :

Inducer of CBF expression

LT:

Low temperature

References

  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, Del Rio LA, Palma JM, Corpas FJ (2011) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295

    PubMed  Google Scholar 

  • Aït Barka E, Audran JC (1996) Réponse des vignes champenoises aux températures négatives: effet d’un refroidissement contrôlé sur les réserves glucidiques du complexe gemmaire avant et au cours du débourrement. Can J Bot 74:492–505

    Google Scholar 

  • Ait Barka E, Nowak J, Clement C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246–7252

    PubMed  Google Scholar 

  • Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    PubMed  CAS  Google Scholar 

  • Antikainen M, Griffith M, Zhang J, Hon WC, Yang D, Pihakaski-Maunsbach K (1996) Immunolocalization of antifreeze proteins in winter Rye leaves, crowns, and roots by tissue printing. Plant Physiol 110:845–857

    PubMed  CAS  Google Scholar 

  • Baena-Gonzalez E, Gray JC, Tyystjarvi E, Aro EM, Maenpaa P (2001) Abnormal regulation of photosynthetic electron transport in a chloroplast ycf9 inactivation mutant. J Biol Chem 276:20795–20802

    PubMed  CAS  Google Scholar 

  • Bergantino E, Dainese P, Cerovic Z, Sechi S, Bassi R (1995) A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress. J Biol Chem 270:8474–8481

    PubMed  CAS  Google Scholar 

  • Bies-Etheve N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M, Cooke R, Delseny M (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67:107–124

    PubMed  CAS  Google Scholar 

  • Bohnert HJ, Sheveleva E (1998) Plant stress adaptations—making metabolism move. Curr Opin Plant Biol 1:267–274

    PubMed  CAS  Google Scholar 

  • Bravo LA, Gallardo J, Navarrete A, Olave N, Martínez J, Alberdi M, Close TJ, Corcuera LJ (2003) Cryoprotective activity of a cold-induced dehydrin purified from barley. Physiol Plant 118:262–269

    CAS  Google Scholar 

  • Casacuberta JM, Puigdomenech P, San Segundo B (1991) A gene coding for a basic pathogenesis-related (PR-like) protein from Zea mays. Molecular cloning and induction by a fungus (Fusarium moniliforme) in germinating maize seeds. Plant Mol Biol 16:527–536

    PubMed  CAS  Google Scholar 

  • Catala R, Santos E, Alonso JM, Ecker JR, Martinez-Zapater JM, Salinas J (2003) Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940–2951

    PubMed  CAS  Google Scholar 

  • Chaikam V, Karlson DT (2010) Comparison of structure, function and regulation of plant cold shock domain proteins to bacterial and animal cold shock domain proteins. BMB Rep 43:1–8

    PubMed  CAS  Google Scholar 

  • Chen TH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505

    PubMed  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Develop 17:1043–1054

    PubMed  CAS  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55

    PubMed  CAS  Google Scholar 

  • Clarke SM, Mur LA, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J 38:432–447

    PubMed  CAS  Google Scholar 

  • Couee I, Sulmon C, Gouesbet G, El Amrani A (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. J Exp Bot 57:449–459

    PubMed  CAS  Google Scholar 

  • Crifo T, Puglisi I, Petrone G, Recupero GR, Lo Piero AR (2011) Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 478:1–9

    Google Scholar 

  • Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148:1094–1105

    PubMed  CAS  Google Scholar 

  • Ding S, Huang CL, Sheng HM, Song CL, Li YB, An LZ (2011) Effect of inoculation with the endophyte Clavibacter sp. strain Enf12 on chilling tolerance in Chorispora bungeana. Physiol Plant 141:141–151

    PubMed  CAS  Google Scholar 

  • Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984

    PubMed  CAS  Google Scholar 

  • Du L, Poovaiah BW (2005) Ca2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437:741–745

    PubMed  CAS  Google Scholar 

  • Eriksson SK, Kutzer M, Procek J, Grobner G, Harryson P (2011) Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. Plant Cell 23:2391–2404

    PubMed  CAS  Google Scholar 

  • Fernandez O, Bethencourt L, Quero A, Sangwan RS, Clement C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417

    PubMed  CAS  Google Scholar 

  • Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, Clément C, Fontaine F, Ait Barka E (2012) Burkholderia phytofirmans strain PsJN acclimates grapevine to cold by modulating carbohydrates metabolism. Mol Plant Microbe Interact 25:496–504

    PubMed  CAS  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    PubMed  CAS  Google Scholar 

  • Fursova OV, Pogorelko GV, Tarasov VA (2009) Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 429:98–103

    PubMed  CAS  Google Scholar 

  • Gechev T, Willekens H, Van Montagu M, Inze D, Van Camp W, Toneva V, Minkov I (2003) Different responses of tobacco antioxidant enzymes to light and chilling stress. J Plant Physiol 160:509–515

    PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33

    PubMed  CAS  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    PubMed  CAS  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    PubMed  CAS  Google Scholar 

  • Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781

    PubMed  CAS  Google Scholar 

  • Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardestrom P, Schroder W, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J 47:720–734

    PubMed  CAS  Google Scholar 

  • Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    PubMed  CAS  Google Scholar 

  • Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138:330–340

    PubMed  CAS  Google Scholar 

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    PubMed  CAS  Google Scholar 

  • Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648

    PubMed  CAS  Google Scholar 

  • Han H, Gao S, Li B, Dong XC, Feng HL, Meng QW (2010) Overexpression of violaxanthin de-epoxidase gene alleviates photoinhibition of PSII and PSI in tomato during high light and chilling stress. J Plant Physiol 167:176–183

    PubMed  CAS  Google Scholar 

  • Hekneby M, Antolín MC, Sánchez-Díaz M (2006) Frost resistance and biochemical changes during cold acclimation in different annual legumes. Environ Exp Bot 55:305–314

    CAS  Google Scholar 

  • Hincha DK (2002) Cryoprotectin: a plant lipid-transfer protein homologue that stabilizes membranes during freezing. Philos Trans R Soc Lond B Biol Sci 357:909–916

    PubMed  CAS  Google Scholar 

  • Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2004) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. (vol 129, pg 1086, 2002). Plant Physiol 135:1145–1155

    CAS  Google Scholar 

  • Huang T, Duman JG (2002) Cloning and characterization of a thermal hysteresis (antifreeze) protein with DNA-binding activity from winter bittersweet nightshade, Solanum dulcamara. Plant Mol Biol 48:339–350

    PubMed  CAS  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    PubMed  CAS  Google Scholar 

  • Ivanov AG, Sane PV, Krol M, Gray GR, Balseris A, Savitch LV, Oquist G, Huner NP (2006) Acclimation to temperature and irradiance modulates PSII charge recombination. FEBS Lett 580:2797–2802

    PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    PubMed  CAS  Google Scholar 

  • Jouve L, Hoffmann L, Hausman JF (2004) Polyamine, carbohydrate, and proline content changes during salt stress exposure of aspen (Populus tremula L.): involvement of oxidation and osmoregulation metabolism. Plant Biol 6:74–80

    PubMed  CAS  Google Scholar 

  • Kaur G, Kumar S, Thakur P, Malik JA, Bhandhari K, Sharma KD, Nayyar H (2011) Involvement of proline in response of chickpea (Cicer arietinum L.) to chilling stress at reproductive stage. Sci Hortic 128:174–181

    CAS  Google Scholar 

  • Kim MH, Sasaki K, Imai R (2009) Cold shock domain protein 3 regulates freezing tolerance in Arabidopsis thaliana. J Biol Chem 284:23454–23460

    PubMed  CAS  Google Scholar 

  • King AI, Joyce DC, Reid MS (1988) Role of carbohydrates in diurnal chilling sensitivity of tomato seedlings. Plant Physiol 86:764–768

    PubMed  CAS  Google Scholar 

  • Kishor PBK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao K, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    CAS  Google Scholar 

  • Knight H, Brandt S, Knight MR (1998) A history of stress alters drought calcium signalling pathways in Arabidopsis. Plant J 16:681–687

    PubMed  CAS  Google Scholar 

  • Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135:1710–1717

    PubMed  CAS  Google Scholar 

  • Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    PubMed  CAS  Google Scholar 

  • Krol M, Ivanov AG, Jansson S, Kloppstech K, Huner NP (1999) Greening under high light or cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the Chlorina f2 mutant. Plant Physiol 120:193–204

    PubMed  CAS  Google Scholar 

  • Kushad MM, Yelenosky G (1987) Evaluation of polyamine and proline levels during low temperature acclimation of citrus. Plant Physiol 84:692–695

    PubMed  CAS  Google Scholar 

  • Lang V, Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20:951–962

    PubMed  CAS  Google Scholar 

  • Laugier E, Tarrago L, Vieira Dos Santos C, Eymery F, Havaux M, Rey P (2010) Arabidopsis thaliana plastidial methionine sulfoxide reductases B, MSRBs, account for most leaf peptide MSR activity and are essential for growth under environmental constraints through a role in the preservation of photosystem antennae. Plant J 61:271–282

    PubMed  CAS  Google Scholar 

  • Lindow SE, Leveau JHJ (2002) Phyllosphere microbiology. Curr Opin Biotech 13:238–243

    PubMed  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    PubMed  CAS  Google Scholar 

  • Liu Y, Jiang H, Zhao Z, An L (2011) Abscisic acid is involved in brassinosteroids-induced chilling tolerance in the suspension cultured cells from Chorispora bungeana. J Plant Physiol 168:853–862

    PubMed  CAS  Google Scholar 

  • Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol Plant Mol Biol 24:445–466

    CAS  Google Scholar 

  • MacKay VL, Li X, Flory MR, Turcott E, Law GL, Serikawa KA, Xu XL, Lee H, Goodlett DR, Aebersold R, Zhao LP, Morris DR (2004) Gene expression analyzed by high-resolution state array analysis and quantitative proteomics: response of yeast to mating pheromone. Mol Cell Proteomics 3:478–489

    PubMed  CAS  Google Scholar 

  • Mantyla E, Lang V, Palva ET (1995) Role of abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LT178 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol 107:141–148

    PubMed  Google Scholar 

  • Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993

    PubMed  CAS  Google Scholar 

  • Matsuda O, Sakamoto H, Hashimoto T, Iba K (2005) A temperature-sensitive mechanism that regulates post-translational stability of a plastidial omega-3 fatty acid desaturase (FAD8) in Arabidopsis leaf tissues. J Biol Chem 280:3597–3604

    PubMed  CAS  Google Scholar 

  • Matteucci M, D’Angeli S, Errico S, Lamanna R, Perrotta G, Altamura MM (2011) Cold affects the transcription of fatty acid desaturases and oil quality in the fruit of Olea europaea L. genotypes with different cold hardiness. J Exp Bot 62:3403–3420

    PubMed  CAS  Google Scholar 

  • Miranda JA, Avonce N, Suarez R, Thevelein JM, Van Dijck P, Iturriaga G (2007) A bifunctional TPS-TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226:1411–1421

    PubMed  CAS  Google Scholar 

  • Miura K, Ohta M, Nakazawa M, Ono M, Hasegawa PM (2011) ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J 67:269–279

    PubMed  CAS  Google Scholar 

  • Nair S, Singh Z (2004) Chilling injury in mango fruit in relation to biosynthesis of free polyamines. Headley, Ashford

    Google Scholar 

  • Nakaminami K, Karlson DT, Imai R (2006) Functional conservation of cold shock domains in bacteria and higher plants. Proc Nat Acad Sci USA 103:10122–10127

    PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    PubMed  CAS  Google Scholar 

  • Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104:21002–21007

    PubMed  CAS  Google Scholar 

  • Orvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23:785–794

    PubMed  CAS  Google Scholar 

  • Park MR, Yun KY, Mohanty B, Herath V, Xu F, Wijaya E, Bajic VB, Yun SJ, De Los Reyes BG (2010) Supra-optimal expression of the cold-regulated OsMyb4 transcription factor in transgenic rice changes the complexity of transcriptional network with major effects on stress tolerance and panicle development. Plant Cell Environ 33:2209–2230

    PubMed  CAS  Google Scholar 

  • Passarini F, Wientjes E, Hienerwadel R, Croce R (2009) Molecular basis of light harvesting and photoprotection in CP24: unique features of the most recent antenna complex. J Biol Chem 284:29536–29546

    PubMed  CAS  Google Scholar 

  • Patton AJ, Cunningham SM, Volenec JJ, Reicher ZJ (2007) Differences in freeze tolerance of zoysiagrasses: II. Carbohydrates and proline accumulation. Crop Science Society of America, Madison

    Google Scholar 

  • Penna S (2003) Building stress tolerance through over-producing trehalose in transgenic plants. Trends Plant Sci 8:355–357

    PubMed  CAS  Google Scholar 

  • Pollock CJ, Lloyd EJ (1987) The effect of low temperature upon starch, sucrose and fructan synthesis in leaves. Ann Bot 60:231–235

    CAS  Google Scholar 

  • Pradet-Balade B, Boulme F, Beug H, Mullner EW, Garcia-Sanz JA (2001) Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci 26:225–229

    PubMed  CAS  Google Scholar 

  • Provart NJ, Gil P, Chen W, Han B, Chang HS, Wang X, Zhu T (2003) Gene expression phenotypes of Arabidopsis associated with sensitivity to low temperatures. Plant Physiol 132:893–906

    PubMed  CAS  Google Scholar 

  • Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753

    PubMed  CAS  Google Scholar 

  • Raison JK, Lyons JM (1986) Chilling injury—a plea for uniform terminology. Plant Cell Environ 9:685–686

    Google Scholar 

  • Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232

    Google Scholar 

  • Ruelland E, Vaultier M-N, Zachowski A, Hurry V, Kader J-C, Delseny M (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150

    CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401–S417

    PubMed  CAS  Google Scholar 

  • Sangwan V, Foulds I, Singh J, Dhindsa RS (2001) Cold-activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. Plant J 27:1–12

    PubMed  CAS  Google Scholar 

  • Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31:629–638

    PubMed  CAS  Google Scholar 

  • Sasaki H, Ichimura K, Oda M (1996) Changes in sugar content during cold acclimation and deacclimation of cabbage seedlings. Ann Bot 78:365–369

    CAS  Google Scholar 

  • Sasaki K, Kim MH, Imai R (2007) Arabidopsis cold shock domain protein2 is a RNA chaperone that is regulated by cold and developmental signals. Biochem Biophys Res Commun 364:633–638

    PubMed  CAS  Google Scholar 

  • Scott IM, Clarke SM, Wood JE, Mur LA (2004) Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 135:1040–1049

    PubMed  CAS  Google Scholar 

  • Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661–671

    PubMed  CAS  Google Scholar 

  • Sharma N, Cram D, Huebert T, Zhou N, Parkin IA (2007) Exploiting the wild crucifer Thlaspi arvense to identify conserved and novel genes expressed during a plant’s response to cold stress. Plant Mol Biol 63:171–184

    PubMed  CAS  Google Scholar 

  • Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439

    PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 250:161–170

    PubMed  CAS  Google Scholar 

  • Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551

    PubMed  CAS  Google Scholar 

  • Skirvin RM, Kohler E, Steiner H, Ayers D, Laughnan A, Norton MA, Warmund M (2000) The use of genetically engineered bacteria to control frost on strawberries and potatoes. Whatever happened to all of that research? Sci Hortic 84:179–189

    Google Scholar 

  • Smallwood M, Bowles DJ (2002) Plants in a cold climate. Philos Trans R Soc Lond B Biol Sci 357:831–846

    PubMed  CAS  Google Scholar 

  • Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206

    PubMed  CAS  Google Scholar 

  • Su CF, Wang YC, Hsieh TH, Lu CA, Tseng TH, Yu SM (2010) A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol 153:145–158

    PubMed  CAS  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2011) ROS and redox signaling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    PubMed  Google Scholar 

  • Svensson JT, Crosatti C, Campoli C, Bassi R, Stanca AM, Close TJ, Cattivelli L (2006) Transcriptome analysis of cold acclimation in barley albina and xantha mutants. Plant Physiol 141:257–270

    PubMed  CAS  Google Scholar 

  • Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    PubMed  CAS  Google Scholar 

  • Tabaei-Aghdaei SR, Pearce RS, Harrison P (2003) Sugars regulate cold-induced gene expression and freezing-tolerance in barley cell cultures. J Exp Bot 54:1565–1575

    PubMed  CAS  Google Scholar 

  • Takuhara Y, Kobayashi M, Suzuki S (2011) Low-temperature-induced transcription factors in grapevine enhance cold tolerance in transgenic Arabidopsis plants. J Plant Physiol 168:967–975

    Google Scholar 

  • Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, Baillieul F, Clément C, Ait Barka E (2011) Burkholderia phytofirmans strain PsJN primes Vitis vinifera L. and confers a better tolerance to low non-freezing temperatures. Mol Plant Microbe Interact 25:241–249

    Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577

    PubMed  CAS  Google Scholar 

  • Tian Q, Stepaniants SB, Mao M, Weng L, Feetham MC, Doyle MJ, Yi EC, Dai H, Thorsson V, Eng J, Goodlett D, Berger JP, Gunter B, Linseley PS, Stoughton RB, Aebersold R, Collins SJ, Hanlon WA, Hood LE (2004) Integrated genomic and proteomic analyses of gene expression in mammalian cells. Mol Cell Proteomics 3:960–969

    PubMed  CAS  Google Scholar 

  • Uemura M, Steponkus PL (1999) Cold acclimation in plants: relationship between the lipid composition and the cryostability of the plasma membrane. J Plant Res 112:245–254

    Google Scholar 

  • Uemura M, Warren G, Steponkus PL (2003) Freezing sensitivity in the sfr4 mutant of Arabidopsis is due to low sugar content and is manifested by loss of osmotic responsiveness. Plant Physiol 131:1800–1807

    PubMed  CAS  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Google Scholar 

  • Venketesh S, Dayananda C (2008) Properties, potentials, and prospects of antifreeze proteins. Crit Rev Biotechnol 28:57–82

    PubMed  CAS  Google Scholar 

  • Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35:753–759

    PubMed  CAS  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Google Scholar 

  • Vogg G, Heim R, Gotschy B, Beck E, Hansen J (1998) Frost hardening and photosynthetic performance of Scots pine (Pinus sylvestris L.). II. Seasonal changes in the fluidity of thylakoid membranes. Planta 204:201–206

    CAS  Google Scholar 

  • Wang R, Li R, Sun Z, Ren Y, Yue W (2006) Anti-freezing proteins and plant responses to low temperature stress. Ying Yong Sheng Tai Xue Bao 17:551–556

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    PubMed  CAS  Google Scholar 

  • Xiao H, Siddiqua M, Braybrook S, Nassuth A (2006) Three grape CBF/DREB1 genes respond to low temperature, drought and abscisic acid. Plant Cell Environ 29:1410–1421

    PubMed  CAS  Google Scholar 

  • Xiao H, Tattersall EA, Siddiqua MK, Cramer GR, Nassuth A (2008) CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant Cell Environ 31:1–10

    PubMed  CAS  Google Scholar 

  • Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902

    Google Scholar 

  • Xin Z, Li PH (1993) Relationship between proline and abscisic acid in the induction of chilling tolerance in maize suspension-cultured cells. Plant Physiol 103:607–613

    PubMed  CAS  Google Scholar 

  • Yaish MW, Doxey AC, McConkey BJ, Moffatt BA, Griffith M (2006) Cold-active winter rye glucanases with ice-binding capacity. Plant Physiol 141:1459–1472

    PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    PubMed  CAS  Google Scholar 

  • Yang T, Chaudhuri S, Yang L, Du L, Poovaiah BW (2010) A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J Biol Chem 285:7119–7126

    PubMed  CAS  Google Scholar 

  • Yeh S, Moffatt BA, Griffith M, Xiong F, Yang DS, Wiseman SB, Sarhan F, Danyluk J, Xue YQ, Hew CL, Doherty-Kirby A, Lajoie G (2000) Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiol 124:1251–1264

    PubMed  CAS  Google Scholar 

  • Zeng Y, Yu J, Cang J, Liu L, Mu Y, Wang J, Zhang D (2011) Detection of sugar accumulation and expression levels of correlative key enzymes in winter wheat (Triticum aestivum) at low temperatures. Biosci Biotechnol Biochem 75:681–687

    PubMed  CAS  Google Scholar 

  • Zhai H, Bai X, Zhu Y, Li Y, Cai H, Ji W, Ji Z, Liu X, Li J (2010) A single-repeat R3-MYB transcription factor MYBC1 negatively regulates freezing tolerance in Arabidopsis. Biochem Biophys Res Commun 394:1018–1023

    PubMed  CAS  Google Scholar 

  • Zhang S, Jiang H, Peng S, Korpelainen H, Li C (2011) Sex-related differences in morphological, physiological, and ultrastructural responses of Populus cathayana to chilling. J Exp Bot 62:675–686

    PubMed  CAS  Google Scholar 

  • Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779:780–788

    PubMed  CAS  Google Scholar 

  • Zhou MQ, Shen C, Wu LH, Tang KX, Lin J (2011) CBF-dependent signaling pathway: a key responder to low temperature stress in plants. Crit Rev Biotechnol 31:186–192

    PubMed  CAS  Google Scholar 

  • Zhu JH, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295

    PubMed  CAS  Google Scholar 

  • Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu JK, Hasegawa PM, Bohnert HJ, Shi H, Yun DJ, Bressan RA (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 105:4945–4950

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The first author (A.T.) was supported by a Grant from the Greek State Scholarship Foundation (I.K.Y.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Essaïd Ait Barka.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Theocharis, A., Clément, C. & Barka, E.A. Physiological and molecular changes in plants grown at low temperatures. Planta 235, 1091–1105 (2012). https://doi.org/10.1007/s00425-012-1641-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1641-y

Keywords

  • C-repeat binding factor
  • Low temperatures
  • Plant acclimation
  • Signal perception