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What happens in plant molecular responses to cold stress?

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Abstract

Low temperature is one of the major abiotic stresses limiting the productivity and the geographical distribution of many important crops. Many plants increase in freezing tolerance in response to low temperatures. This phenomenon needs a vast reprogramming of gene expression which results in the adjusted metabolic-structural alterations. However, the efficient adjustments are dependent on proper cold signal transduction. The first stage is cold stress signal perception which is carried out by different pathways. Transcriptional cascades are next players which operate through ABA-dependent and ABA-independent pathways to induce cold-regulated (COR) gene expression and the result is increasing in the levels of hundreds of metabolites, which some of them are known to have protective effects against the damaging effects of cold stress and some like soluble sugars, reactive oxygen species and photosynthetic metabolites are thought to act as signaling molecules and regulate special COR genes. The different aspects of these events are discussed in detail below.

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References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  Google Scholar 

  • Atici O, Nalbantoglu B (2003) Antifreeze proteins in higher plants. Phytochemistry 64:1187–1196

    CAS  PubMed  Google Scholar 

  • Badawi M, Reddy YV, Agharbaoui Z, Tominaga Y, Danyluk J, Sarhan F, Houde M (2008) Structure and functional analysis of wheat ICE (inducer of CBF expression) genes. Plant Cell Physiol 49:1237–1249

    CAS  PubMed  Google Scholar 

  • Beck EH, Heim R, Hansen J (2004) Plant resistance to cold stress: mechanisms and environmental signals triggering frost hardening and dehardening. J Biosci 29:449–459

    PubMed  Google Scholar 

  • Beck EH, Fettig S, Knake C, Hartig K, Bhattarai T (2007) Specific and unspecific responses of plants to cold and drought stress. J Biosci 32:501–510

    CAS  PubMed  Google Scholar 

  • Carpaneto A, Ivashikina N, Levchenko V, Krol E, Jeworutzki E, Zhu JK, Hedrich R (2007) Cold transiently activates calcium-permeable channels in Arabidopsis mesophyll cells. Plant Physiol 143:487–494

    CAS  PubMed  Google Scholar 

  • Charron JBF, Ouellet F, Pelletier M, Danyluk J, Chauve C, Sarhan F (2005) Identification, expression, and evolutionary analyses of plant lipocalins. Plant Physiol 139:2017–2028

    CAS  PubMed  Google Scholar 

  • Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye XG, Xia LQ, Ma YZ (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem Biophys Res Commun 353:299–305

    CAS  PubMed  Google Scholar 

  • Chen M, Xu Z, Xia L, Li L, Cheng X, Dong J, Wang Q, Ma Y (2009) Cold-induced modulation and functional analyses of the DRE-binding transcription factor gene, GmDREB3, in soybean (Glycine max L.). J Exp Bot 60:121–135

    CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu JK (2002) Molecular genetic analysis of cold-regulated gene transcription. Phil Trans R Soc Lond B 357:877–886

    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 Dev 17:1043–1054

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Choi HI, Hong JH, Ha JO, Kang JY, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730

    CAS  PubMed  Google Scholar 

  • Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803. doi:10.1111/j.1399-3054.1996.tb00546.x

    CAS  Google Scholar 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226

    CAS  PubMed  Google Scholar 

  • Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638

    CAS  PubMed  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    CAS  PubMed  Google Scholar 

  • Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856

    CAS  PubMed  Google Scholar 

  • Deryabin AN, Dubinina IM, Burakhanova EA, Astakhova NV, Sabel’nikova EP, Trunova TI (2005) Influence of yeast-derived invertase gene expression in potato plants on membrane lipid peroxidation at low temperature. J Therm Biol 30:73–77. doi:10.1016/j.jtherbio.2004.07.002

    CAS  Google Scholar 

  • Desikan R, Mackerness SAH, Hancock JT, Neill SJ (2001) Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol 127:159–172

    CAS  PubMed  Google Scholar 

  • Dhonukshe P, Laxalt AM, Goedhart J, Gadella TWJ, Munnik T (2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15:2666–2679

    CAS  PubMed  Google Scholar 

  • Ding JP, Pickard BG (1993) Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J 3:713–720

    CAS  PubMed  Google Scholar 

  • Dodd AN, Jakobsen MK, Baker AJ, Telzerow A, Hou SW, Laplaze L, Barrot L, Poethig RS, Haseloff J, Webb AAR (2006) Time of day modulates low-temperature Ca2+ signals in Arabidopsis. Plant J 48:962–973

    CAS  PubMed  Google Scholar 

  • Drøbak BK, Franklin-Tong VE, Staiger CJ (2004) The role of the actin cytoskeleton in plant cell signaling. New Phytol 163:13–30. doi:10.1111/j.1469-8137.2004.01076.x

    Google Scholar 

  • Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44. doi:10.1111/j.1399-3054.2005.00627.x

    CAS  Google Scholar 

  • Ganeshan S, Vitamvas P, Fowler DB, Chibbar RN (2008) Quantitative expression analysis of selected COR genes reveals their differential expression in leaf and crown tissues of wheat (Triticum aestivum L.) during an extended low temperature acclimation regimen. J Exp Bot 59:2393–2402

    CAS  PubMed  Google Scholar 

  • Gardiner JC, Harper JDI, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158

    CAS  PubMed  Google Scholar 

  • Gardiner J, Collings DA, Harper JDI, Marc J (2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant Cell Physiol 44:687–696

    CAS  PubMed  Google Scholar 

  • George L, Romanowsky SM, Harper JF, Sharrock RA (2008) The ACA10 Ca2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146:716–728

    CAS  PubMed  Google Scholar 

  • Griffith M, Antikainen M, Hon WC, Pihakaski-Maunsbach K, Yu XM, Chun JU, Yang DSC (1997) Antifreeze proteins in winter rye. Physiol Plant 100:327–332. doi:10.1111/j.1399-3054.1997.tb04790.x

    CAS  Google Scholar 

  • Guy C (1999) Molecular responses of plants to cold shock and cold acclimation. J Mol Microbiol Biotechnol 1:231–242

    CAS  PubMed  Google Scholar 

  • Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235

    CAS  PubMed  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2005) Metal binding by Citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695–2703

    CAS  PubMed  Google Scholar 

  • Heath RJ, Rock CO (1996) Regulation of fatty acid elongation and initiation by acyl-acyl carrier protein in Escherichia coli. J Biol Chem 271:1833–1836

    CAS  PubMed  Google Scholar 

  • Hon WC, Griffith M, Mlynarz A, Kwok YC, Yang DSC (1995) Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Plant Physiol 109:879–889

    CAS  PubMed  Google Scholar 

  • Hong Y, Zheng S, Wang X (2008) Dual functions of phospholipase Dα1 in plant response to drought. Mol Plant 1:262–269. doi:10.1093/mp/ssm025

    CAS  PubMed  Google Scholar 

  • Houde M, Belcaid M, Ouellet F, Danyluk J, Monroy AF, Dryanova A, Gulick P, Bergeron A, Laroche A, Links MG, MacCarthy L, Crosby WL, Sarhan F (2006) Wheat EST resources for functional genomics of abiotic stress. BMC Genomics 7:149. doi:10.1186/1471-2164-7-149

    PubMed  Google Scholar 

  • Humphrey TV, Bonetta DT, Goring DR (2007) Sentinels at the wall: cell wall receptors and sensors. New Phytol 176:7–21

    CAS  PubMed  Google Scholar 

  • Hung SH, Yu CW, Lin CH (2005) Hydrogen peroxide functions as a stress signal in plants. Bot Stud 46:1–10

    CAS  Google Scholar 

  • Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMK4 and ATMK6. Plant J 24:655–665

    CAS  PubMed  Google Scholar 

  • Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreis M, Zhang S, Hirt H, Wilson C, Heberle-Bors E, Ellis BE, Morris PC, Innes RW, Ecker JR, Scheel D, Klessig DF, Machida Y, Mundy J, Ohashi Y, Walker JC (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    CAS  Google Scholar 

  • Ishizaki-Nishizawa O, Fujii T, Azuma M, Sekiguchi K, Murata N, Ohtani T, Toguri T (1996) Low-temperature resistance of higher plants is significantly enhanced by a nonspecific cyanobacterial desaturase. Nat Biotechnol 14:1003–1006

    CAS  PubMed  Google Scholar 

  • Jin UH, Lee JW, Chung YS, Lee JH, Yi YB, Kim YK, Hyung NI, Pyee JH, Chung CH (2001) Characterization and temporal expression of a ω-6 fatty acid desaturase cDNA from sesame (Sesamum indicum L.) seeds. Plant Sci 161:935–941

    CAS  Google Scholar 

  • Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H (1996) Stress signalling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274–11279

    CAS  PubMed  Google Scholar 

  • Kaplan F, Guy CL (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135:1674–1684

    CAS  PubMed  Google Scholar 

  • Kim MC, Chung WS, Yun DJ, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21. doi:10.1093/mp/ssn091

    CAS  PubMed  Google Scholar 

  • Klimecka M, Muszyńska G (2007) Structure and functions of plant calcium-dependent protein kinases. Acta Biochim Pol 54:219–233

    CAS  PubMed  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    CAS  PubMed  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after cold acclimation. Plant Cell 8:489–503

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Koo BC, Bushman BS, Mott IW (2008) Transcripts associated with non-acclimated freezing response in two barley cultivars. Plant Genome 1:21–32. doi:10.3835/plantgenome2008.06.0344

    CAS  Google Scholar 

  • Kosova K, Vitamvas P, Prasil IT (2007) The role of dehydrins in plant response to cold. Biologia Plantarum 51:601–617. doi:10.1007/s10535-007-0133-6

    CAS  Google Scholar 

  • Kosova K, Holkova L, Prasil IT, Prasilova P, Bradacova M, Vitamvas P, Capkova V (2008) Expression of dehydrin 5 during the development of frost tolerance in barley (Hordeum vulgare). J Plant Physiol 165:1142–1151

    CAS  PubMed  Google Scholar 

  • Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381–390

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Last RL, Jones AD, Shachar-Hill Y (2007) Towards the plant metabolome and beyond. Nat Rev Mol Cell Biol 8:167–174

    CAS  PubMed  Google Scholar 

  • Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14:1235–1251

    CAS  PubMed  Google Scholar 

  • Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane-bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–433

    PubMed  Google Scholar 

  • Liu HT, Li GL, Chang H, Sun DY, Zhou RG, Li B (2007) Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant Cell Environ 30:156–164

    CAS  PubMed  Google Scholar 

  • Liu HT, Gao F, Li GL, Han JL, Liu DL, Sun DY, Zhou RG (2008) The calmodulin-binding protein kinase 3 is part of heat shock signal transduction in Arabidopsis thaliana. Plant J 55:760–773

    CAS  PubMed  Google Scholar 

  • Maali R, Schimschilaschvili HR, Pchelkin VP, Tsydendambaev VD, Nosov AM, Los DA, Goldenkova-Pavlova IV (2007) Comparative expression in Escherichia coli of the native and hybrid genes for acyl-lipid ∆9-desaturase. Russian J Genet 43:121–126. doi:10.1134/S1022795407020044

    CAS  Google Scholar 

  • Maali-Amiri R, Goldenkova-Pavlova IV, Yur’eva NO, Pchelkin VP, Tsydendambaev VD, Vereshchagin AG, Deryabin AN, Trunova TI, Los DA, Nosov AM (2007) Lipid fatty acid composition of potato plants transformed with the ∆12-desaturase gene from cyanobacterium. Russian J Plant Physiol 54:600–606. doi:10.1134/S1021443707050056

    CAS  Google Scholar 

  • Maeda H, Song W, Sage TL, DellaPenna D (2006) Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis. Plant Cell 18:2710–2732

    CAS  PubMed  Google Scholar 

  • Matos AR, Hourton-Cabassa C, Cicek D, Reze N, Arrabaca JD, Zachowski A, Moreau F (2007) Alternative oxidase involvement in cold stress response of Arabidopsis thaliana fad2 and FAD3+ cell suspensions altered in membrane lipid composition. Plant Cell Physiol 48:856–865

    CAS  PubMed  Google Scholar 

  • McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294

    CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    CAS  PubMed  Google Scholar 

  • Monroy AF, Dhindsa RS (1995) Low temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25°C. Plant Cell 7:321–331

    CAS  PubMed  Google Scholar 

  • Monroy AF, Sangwan V, Dhindsa RS (1998) Low temperature signal transduction during cold acclimation: protein phosphatase 2A as an early target for cold-inactivation. Plant J 13:653–660

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Murata N, Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of Cyanobacteria. Biochem J 308:1–8

    CAS  PubMed  Google Scholar 

  • Nakaminami K, Hill K, Perry SE, Sentoku N, Long JA, Karlson DT (2009) Arabidopsis cold shock domain proteins: relationships to floral and silique development. J Exp Bot 60:1047–1062

    CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Plant Physiol 126:62–71. doi:10.1111/j.1399-3054.2005.00592.x

    CAS  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95

    CAS  PubMed  Google Scholar 

  • Nguema-Ona E, Bannigan A, Chevalier L, Baskin TI, Driouich A (2007) Disruption of arabinogalactan proteins disorganizes cortical microtubules in the root of Arabidopsis thaliana. Plant J 52:240–251

    CAS  PubMed  Google Scholar 

  • Nover L, Scharf KD (1997) Heat stress proteins and transcription factors. Cell Mol Life Sci 53:80–103

    CAS  PubMed  Google Scholar 

  • Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101:3985–3990. doi:10.1073/pnas.0303029101

    CAS  PubMed  Google Scholar 

  • Orlova IV, Serebriiskaya TS, Popov V, Merkulova N, Nosov AM, Trunova TI, Tsydendambaev VD, Los DA (2003) Transformation of tobacco with a gene for the thermophilic acyl-lipid desaturase enhances the chilling tolerance of plants. Plant Cell Physiol 44:447–450

    CAS  PubMed  Google Scholar 

  • Örvar 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  Google Scholar 

  • Ouellet F (2007) Cold acclimation and freezing tolerance in plants. Encycl Life Sci. doi:10.1002/9780470015902.a0020093

  • Park SJ, Kwak KJ, Oh TR, Kim YO, Kang H (2009) Cold shock domain proteins affect seed germination and growth of Arabidopsis thaliana under abiotic stress conditions. Plant Cell Physiol 50:869–878

    CAS  PubMed  Google Scholar 

  • Plieth C, Hansen UP, Knight H, Knight MR (1999) Temperature sensing by plants: the primary characteristics of signal perception and calcium response. Plant J 18:491–497

    CAS  PubMed  Google Scholar 

  • Pourtau N, Jennings R, Pelzer E, Pallas J, Wingler A (2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224:556–568

    CAS  PubMed  Google Scholar 

  • Rapacz M, Wolanin B, Hura K, Tyrka M (2008) The effects of cold acclimation on photosynthetic apparatus and the expression of COR14b in four genotypes of barley (Hordeum vulgare) contrasting in their tolerance to freezing and high-light treatment in cold conditions. Ann Bot 101:689–699

    CAS  PubMed  Google Scholar 

  • Rekarte-Cowie I, Ebshish OS, Mohamed KS, Pearce RS (2008) Sucrose helps regulate cold acclimation of Arabidopsis thaliana. J Exp Bot 59:4205–4217

    CAS  PubMed  Google Scholar 

  • Renaut J, Hausman JF, Bassett C, Artlip T, Cauchie HM, 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. doi:10.1007/s11295-008-0134-4

    Google Scholar 

  • Rorat T (2006) Plant dehydrins—tissue location, structure and function. Cell Mol Biol Lett 11:536–556

    CAS  PubMed  Google Scholar 

  • Russel NJ (1984) Mechanism of thermal adaptation in bacteria: blueprints for survival. Trends Biochem Sci 9:108–112

    Google Scholar 

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

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Sangwan V, Örvar 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

    CAS  PubMed  Google Scholar 

  • Seo PJ, Lee AK, Xiang F, Park CM (2008) Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol 49:334–344

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    CAS  PubMed  Google Scholar 

  • Somerville J (1999) Activities of cold-shock domain proteins in translation control. BioEssays 21:319–325

    Google Scholar 

  • Somerville C, Browse J (1991) Plant lipids: metabolism, mutants, and membranes. Science 252:80–87

    CAS  PubMed  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    CAS  PubMed  Google Scholar 

  • Sugie A, Naydenov N, Mizuno N, Nakamura C, Takumi S (2006) Overexpression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet Syst 81:349–354

    CAS  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

    CAS  PubMed  Google Scholar 

  • Tähtiharju S, Palva T (2001) Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J 26:461–470

    PubMed  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152

    CAS  PubMed  Google Scholar 

  • Thion L, Mazars C, Thuleau P, Graziana A, Rossignol M, Moreau M, Ranjeva R (1996) Activation of plasma membrane voltage-dependent calcium-permeable channels by disruption of microtubules in carrot cells. FEBS Lett 393:13–18

    CAS  PubMed  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? lots!. Plant Physiol 125:89–93

    CAS  PubMed  Google Scholar 

  • Thomson GAJR (1989) Membrane acclimation by unicellular organisms in response to temperature change. J Bioenerg Biomembr 21:43–60

    Google Scholar 

  • Townley HE, Knight MR (2002) Calmodulin as a negative regulator of Arabidopsis COR gene expression. Plant Physiol 128:1169–1172

    CAS  PubMed  Google Scholar 

  • Uemura M, Steponkus PL (2003) Modification of the intracellular sugar content alters the incidence of freeze-induced membrane lesions of protoplasts isolated from Arabidopsis thaliana leaves. Plant Cell Environ 26:1083–1096. doi:10.1046/j.1365-3040.2003.01033.x

    CAS  Google Scholar 

  • Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-lnduced lesions). Plant Physiol 109:15–30

    CAS  PubMed  Google Scholar 

  • Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89. doi:10.1111/j.1399-3054.2005.00594.x

    CAS  Google Scholar 

  • Ukaji N, Kuwabara C, Takezawa D, Arakawa K, Yoshida S, Fujikawa S (1999) Accumulation of small heat-shock protein homologs in the endoplasmic reticulum of cortical parenchyma cells in mulberry in association with seasonal cold acclimation. Plant Physiol 120:481–489

    CAS  PubMed  Google Scholar 

  • Vaultier MN, Cantrel C, Vergnolle C, Justin AM, Demandre C, Benhassaine-Kesri G, Cicek D, Zachowski A, Ruelland E (2006) Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells. FEBS Lett 580:4218–4223

    CAS  PubMed  Google Scholar 

  • Vergnolle C, Vaultier MN, Taconnat L, Renou JP, Kader JC, Zachowski A, Ruelland E (2005) The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions. Plant Physiol 139:1217–1233

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Wada H, Gombos Z, Murata N (1994) Contribution of membrane lipids to the ability of the photosynthetic machinery to tolerate temperature stress. Proc Natl Acad Sci USA 91:4273–4277

    CAS  PubMed  Google Scholar 

  • Webb MS, Steponkus PL (1993) Freeze-lnduced membrane ultrastructural alterations in rye (Sede cereale) leaves. Plant Physiol 101:955–963

    CAS  PubMed  Google Scholar 

  • Webb MS, Gilmour SJ, Thomashow MF, Steponkus PL (1996) Effects of COR6.6 and COR15am polypeptides encoded by COR (cold-regulated) genes of Arabidopsis thaliana on dehydration-lnduced phase transitions of phospholipid membranes. Plant Physiol 111:301–312

    CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    CAS  PubMed  Google Scholar 

  • Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 5:484–496

    CAS  PubMed  Google Scholar 

  • Yano R, Nakamura M, Yoneyama T, Nishida I (2005) Starch-related α-glucan/water dikinase is involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol 138:837–846

    CAS  PubMed  Google Scholar 

  • Yoshida K, Terashima I, Noguchi K (2007) Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol 48:606–614

    CAS  PubMed  Google Scholar 

  • Zhu J, 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

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Agronomy and Plant Breeding, University College of Agriculture and Natural Resources, University of Tehran, 31587-77871, Karaj, Iran

    Leila Heidarvand & Reza Maali Amiri

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  1. Leila Heidarvand
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  2. Reza Maali Amiri
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Correspondence to Reza Maali Amiri.

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Communicated by A. Kononowicz.

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Heidarvand, L., Maali Amiri, R. What happens in plant molecular responses to cold stress?. Acta Physiol Plant 32, 419–431 (2010). https://doi.org/10.1007/s11738-009-0451-8

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  • DOI: https://doi.org/10.1007/s11738-009-0451-8

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