The Omics of Cold Stress Responses in Plants

  • Somya Sinha
  • Bharti Kukreja
  • Priyanka Arora
  • Manisha Sharma
  • Girdhar K. Pandey
  • Manu Agarwal
  • Viswanathan Chinnusamy


Low temperature (LT) is a major threat that limits growth, development, and distribution leading to plant damage and crop losses. Plants respond to cold stress through a phenomenon known as cold acclimation, which is a complex process involving changes at multiple levels that include physiological and biochemical modifications, alterations in gene expression, and changes in concentrations of proteins and metabolites. Perception of cold stress by the cell membranes results in activation of cold-responsive genes and transcription factors that help in combating cold stress. Transcriptional responses to cold are guided by both ABA-dependent and -independent pathways that induce the expression of cold-regulated (COR) genes, thereby changing protein and metabolite homeostasis. Recent advances in the field of genomics, proteomics, and metabolomics has led to new discoveries, which has augmented our understanding of this intricate phenomenon. Here, we discuss the various aspects of cold stress responses in plants to develop a holistic understanding in the field of stress-mediated signaling.


Cold acclimation Low temperature stress C-repeat binding factor Signal transduction 



Research in MA lab is funded by the Department of Biotechnology and Delhi University.


  1. Abat JK, Deswal R (2009) Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9(18):4368–4380PubMedGoogle Scholar
  2. Abdrakhamanova A, Wang QY, Khokhlova L, Nick P (2003) Is microtubule disassembly a trigger for cold acclimation? Plant Cell Physiol 44:676–686PubMedGoogle Scholar
  3. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645PubMedGoogle Scholar
  4. Albrecht V, Weinl S, Balzevic D, D’Angelo C, Batistic O, Kolukisaouglu Ü, Bock R, Schulz B, Harter K, Kudla J (2003) The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J 36:457–470PubMedGoogle Scholar
  5. Alcazar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28(23):1867–1876PubMedGoogle Scholar
  6. Alcázar 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 231:1237–1249PubMedGoogle Scholar
  7. Allagulova CR, Gimalov FR, Shakirova FM, Vakhitov VA (2003) The plant dehydrins: structure and putative functions. Biochemistry 68:945–951PubMedGoogle Scholar
  8. Amme S, Matros A, Schlesier B, Mock HP (2006) Proteome analysis of cold stress response in Arabidopsis thaliana using DIGE-technology. J Exp Bot 57:1537–1546PubMedGoogle Scholar
  9. An D, Yang J, Zhang P (2012) Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genomics 13:64PubMedCentralPubMedGoogle Scholar
  10. Antikainen M, Griffith M (1997) Antifreeze protein accumulation in freezing tolerant cereals. Physiol Plant 99:423–432Google Scholar
  11. Atici O, Nalbantoglu B (2003) Antifreeze proteins in higher plants. Phytochemistry 64:1187–1196PubMedGoogle Scholar
  12. Bachmann M, Matile P, Keller F (1994) Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans 1. Plant Physiol 105:1335–1345PubMedCentralPubMedGoogle Scholar
  13. 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 49:1237–1249PubMedGoogle Scholar
  14. Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 36:652–663PubMedGoogle Scholar
  15. Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713PubMedGoogle Scholar
  16. Bauer H, Pamer R, Perathoner C, Loidolt-Nagele M (1996) Photosynthetic depression in leaves of frost-hardened ivy is not caused by feedback inhibition via assimilate accumulation. J Plant Physiol 149:51–56Google Scholar
  17. Behnam B, Kikuchi A, Celebi-Toprak F, Kasuga M, Yamaguchi-Shinozaki K, Watanabe KN (2007) Arabidopsis rd29A::DREB1A enhances freezing tolerance in transgenic potato. Plant Cell Rep 26:1275–1282PubMedGoogle Scholar
  18. 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 29:1259–1272PubMedGoogle Scholar
  19. Bouchereau A, Aziz A, Larher F, Martin-Tangui J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125Google Scholar
  20. Bray EA (1993) Molecular responses to water-deficit. Plant Physiol 103:1035–1040PubMedCentralPubMedGoogle Scholar
  21. Byun YJ, Kim HJ, Lee DH (2009) Long SAGE analysis of the early response to cold stress in Arabidopsis leaf. Planta 229:1181–1200PubMedGoogle Scholar
  22. Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292PubMedGoogle Scholar
  23. Canella D, Gilmour SJ, Kuhn LA, Thomashow MF (2010) DNA binding by the Arabidopsis CBF1 transcription factor requires the PKKP/RAGRxKFxETRHP signature sequence. Biochim Biophys Acta 1799:454–462PubMedGoogle Scholar
  24. Chen TH, Murata N (2008) Glycinbetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505PubMedGoogle Scholar
  25. Chen M, Thelen JJ (2013) ACYL-LIPID DESATURASE2 is required for chilling and freezing tolerance in Arabidopsis. Plant Cell 25:1430–1444PubMedCentralPubMedGoogle Scholar
  26. 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 60:121–135PubMedCentralPubMedGoogle Scholar
  27. Chen J, Tian L, Xu H, Tian D, Luo Y, Ren C, Yang L, Shi J (2012a) Cold-induced changes of protein and phosphoprotein expression patterns from rice roots as revealed by multiplex proteomic analysis. Plant Omics J 5:194–199Google Scholar
  28. Chen L, Chen Y, Jiang J, Chen S, Chen F, Guan Z, Fang W (2012b) The constitutive expression of Chrysanthemum dichrum ICE1 in Chrysanthemum grandiflorum improves the level of low temperature, salinity and drought tolerance. Plant Cell Rep 31:1747–1758PubMedGoogle Scholar
  29. Chen Y, Jiang J, Song A, Chen S, Shan H, Luo H, Gu C, Sun J, Zhu L, Fang W, Chen F (2013) Ambient temperature enhanced freezing tolerance of Chrysanthemum dichrum CdICE1 Arabidopsis via miR398. BMC Biol 11:121PubMedCentralPubMedGoogle Scholar
  30. Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485PubMedCentralPubMedGoogle Scholar
  31. Cheng L, Gao X, Li S, Shi M, Javeed H, Jing X, Yang G, He G (2010) Proteomic analysis of soybean [Glycine max (L.) Meer.] seeds during imbibition at chilling temperature. Mol Breeding 26:1–17Google Scholar
  32. Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845PubMedCentralPubMedGoogle Scholar
  33. 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 17:1043–1054PubMedCentralPubMedGoogle Scholar
  34. Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236PubMedGoogle Scholar
  35. Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61Google Scholar
  36. Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451PubMedGoogle Scholar
  37. Chinnusamy V, Zhu JK, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55PubMedCentralPubMedGoogle Scholar
  38. Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226PubMedGoogle Scholar
  39. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci U S A 101:15243–15248PubMedCentralPubMedGoogle Scholar
  40. Cox SE, Stushnoff C (2001) Temperature-related shifts in soluble carbohydrate content during dormancy and cold acclimation in Populus tremuloides. Can J For Res 31:730–737Google Scholar
  41. Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11:163PubMedCentralPubMedGoogle Scholar
  42. Cuevas JC, López-Cobollo R, Alcázar 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 148:1094–1105PubMedCentralPubMedGoogle Scholar
  43. Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172PubMedGoogle Scholar
  44. Danyluk J, Carpentier E, Sarhan F (1996) Identification and characterization of a low temperature regulated gene encoding an actin-binding protein from wheat. FEBS Lett 389:324–327PubMedGoogle Scholar
  45. Das R, Pandey GK (2010) Expressional analysis and role of calcium regulated kinases in abiotic stress signaling. Curr Genomics 11(1):2–13PubMedCentralPubMedGoogle Scholar
  46. Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795PubMedGoogle Scholar
  47. 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 139:847–856PubMedCentralPubMedGoogle Scholar
  48. Debnath M, Pandey M, Bisen PS (2011) An omics approach to understand the plant abiotic stress. Omics J 15:739–762Google Scholar
  49. Degand H, Faber AM, Dauchot N, Mingeot D, Watillon B, Cutsem PV, Morsomme P, Boutry M (2009) Proteomic analysis of chicory root identifies proteins typically involved in cold acclimation. Proteomics 9:2903–2907PubMedGoogle Scholar
  50. Desimone M, Henke A, Wagner E (1996) Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol 111:789–796PubMedCentralPubMedGoogle Scholar
  51. Dinari A, Niazi A, Afsharifar AR, Ramezani A (2013) Identification of upregulated genes under cold stress in cold-tolerant chickpea using the cDNA-AFLP approach. PLoS One 8:e52757PubMedCentralPubMedGoogle Scholar
  52. Doczi R, Brader G, Pettko-Szandtner A, Rajh I, Djamei A, Pitzschke A, Teige M, Hirt H (2007) The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19:3266–3279PubMedCentralPubMedGoogle Scholar
  53. 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 21:972–984PubMedCentralPubMedGoogle Scholar
  54. Dong CH, Hu X, Tang W, Zheng X, Kim YS, Lee BH, Zhu JK (2006) A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol Cell Biol 26:9533–9543PubMedCentralPubMedGoogle Scholar
  55. Dong C, Zhang Z, Ren J, Qin Y, Huang J, Wang Y, Cai B, Wang B, Tao J (2013) Stress-responsive gene ICE1 from Vitis amurensis increases cold tolerance in tobacco. Plant Physiol Biochem 71:212–217PubMedGoogle Scholar
  56. dos Santos R, Vergauwen R, Pacolet P, Lescrinier E, Van den Ende W (2012) Manninotriose is a major carbohydrate in red deadnettle (Lamium purpureum, Lamiaceae). Ann Bot 111(3):385–393PubMedCentralPubMedGoogle Scholar
  57. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763PubMedGoogle Scholar
  58. Dumont E, Bahrman N, Goulas E, Valot B, Sellier H, Hilbert JL, Vuylsteker C, Lejeune-Henaut I, Delbreil B (2011) A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci 180:86–98PubMedGoogle Scholar
  59. Egert A, Keller F, Peters S (2013) Abiotic stress-induced accumulation of raffinose in Arabidopsis leaves is mediated by a single raffinose synthase (RS5, At5g40390). BMC Plant Biol 13:218. doi: 10.1186/1471-2229-13-218 PubMedCentralPubMedGoogle Scholar
  60. Espartero J, Sanchez-Aguayo I, Pardo JM (1995) Molecular characterization of glyoxalase-I from a higher plant; upregulation by stress. Plant Mol Biol 29:1223–1233PubMedGoogle Scholar
  61. Feng XM, Zhao Q, Zhao LL, Qiao Y, Xie XB, Li HF, Yao YX, You CX, Hao YJ (2012) The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biol 12:22PubMedCentralPubMedGoogle Scholar
  62. Feng HL, Ma NN, Meng S, Zhang S, Wang JR, Chai S, Meng QW (2013) A novel tomato MYC-type ICE1-like transcription factor, SlICE1a, confers cold, osmotic and salt tolerance in transgenic tobacco. Plant Physiol Biochem 73:309–320PubMedGoogle Scholar
  63. Fernandez P, Di Rienzo J, Fernandez L, Hopp HE, Paniego N, Heinz RA (2008) Transcriptomic identification of candidate genes involved in sunflower responses to chilling and salt stresses based on cDNA microarray analysis. BMC Plant Biol 8:11PubMedCentralPubMedGoogle Scholar
  64. Fournier ML, Gilmore JM, Martin-Brown SA, Washburn MP (2007) Multidimensional separations-based shotgun proteomics. Chem Rev 107:3654–3686PubMedGoogle Scholar
  65. 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 14:1675–1690PubMedCentralPubMedGoogle Scholar
  66. French AD, Waterhouse AL (1993) Chemical structure and characherisitc. In: Suzuki M, Chatterton NJ (eds) Science and technology of fructans. CRC Press, Florida, pp 41–81Google Scholar
  67. Fursova OV, Pogorelko GV, Tarasov VA (2009) Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 429:98–103PubMedGoogle Scholar
  68. 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 59:2393–2402PubMedCentralPubMedGoogle Scholar
  69. Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49(5):459–471PubMedGoogle Scholar
  70. Gao F, Zhou Y, Zhu W, Li X, Fan L, Zhang G (2009) Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230:1033–1046PubMedGoogle Scholar
  71. Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371PubMedGoogle Scholar
  72. Ghangal R, Raghuvanshi S, Sharma PC (2012) Expressed sequence tag based identification and expression analysis of some cold inducible elements in seabuckthorn (Hippophae rhamnoides L.). Plant Physiol Biochem 51:123–128PubMedGoogle Scholar
  73. 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 16:433–442PubMedGoogle Scholar
  74. 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 124:1854–1865PubMedCentralPubMedGoogle Scholar
  75. Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781PubMedGoogle Scholar
  76. Gong Z, Lee H, Xiong L, Jagendorf A, Stevenson B, Zhu JK (2002) RNA helicase-like protein as an early regulator of transcription factors for plant chilling and freezing tolerance. Proc Natl Acad Sci U S A 99:11507–11512PubMedCentralPubMedGoogle Scholar
  77. Gong Z, Dong CH, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu JK (2005) A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17:256–267PubMedCentralPubMedGoogle Scholar
  78. Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder 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 47:720–734PubMedGoogle Scholar
  79. Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405PubMedGoogle Scholar
  80. Griffith M, Antikainen M, Hon WC, Pihakaski-Maunsbach K, Yu XM, Chun JU, Yang DSC (1997) Antifreeze proteins in winter rye. Physiol Plant 100:327–332Google Scholar
  81. Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138:330–340PubMedCentralPubMedGoogle Scholar
  82. Gu X, Gao Z, Zhuang W, Qiao Y, Wang X, Mi L, Zhang Z, Lin Z (2013) Comparative proteomic analysis of rd29A:RdreB1BI transgenic and non-transgenic strawberries exposed to low temperature. J Plant Physiol 170:696–706PubMedGoogle Scholar
  83. Guan Q, Wu J, Zhang Y, Jiang C, Liu R, Chai C, Zhu J (2013) A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25(1):342–356PubMedCentralPubMedGoogle Scholar
  84. Guerra D, Mastrangelo AM, Lopez-Torrejon G, Marzin S, Schweizer P, Stanca AM, del Pozo JC, Cattivelli L, Mazzucotelli E (2012) Identification of a protein network interacting with TdRF1, a wheat RING ubiquitin ligase with a protective role against cellular dehydration. Plant Physiol 158:777–789PubMedCentralPubMedGoogle Scholar
  85. Gulick PJ, Drouin S, Yu Z, Danyluk J, Poisson G, Monroy AF, Sarhan F (2005) Transcriptome comparison of winter and spring wheat responding to low temperature. Genome 48:913–923PubMedGoogle Scholar
  86. Gusta LV, Wisniewski M, Nesbitt NT, Gusta ML (2004) The effect of water, sugars, and proteins on the pattern of ice nucleation and propagation in acclimated and nonacclimated canola leaves. Plant Physiol 135:1642–1653PubMedCentralPubMedGoogle Scholar
  87. Gutha LR, Reddy AR (2008) Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol Biol 68:533–555PubMedGoogle Scholar
  88. Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150PubMedGoogle Scholar
  89. Hansen J, Vogg G, Beck E (1996) Assimilation, allocation and utilization of carbon by 3-year-old Scots pine (Pinus sylvestris L.) tree during winter and early spring. Trees 11:83–90Google Scholar
  90. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553Google Scholar
  91. Hashimoto M, Komatsu S (2007) Proteomic analysis of rice seedlings during cold stress. Proteomics 7:1293–1302PubMedGoogle Scholar
  92. Hashimoto M, Toorchi M, Matsushita K, Iwasaki Y, Komatsu S (2009) Proteome analysis of rice root plasma membrane and detection of cold stress responsive proteins. Protein Peptide Lett 16:685–697Google Scholar
  93. Hausman JF, Evers D, Thiellement H, Jouve L (2000) Compared responses of poplar cuttings and in vitro raised shoots to short-term chilling treatments. Plant Cell Rep 19:954–960Google Scholar
  94. Heidarvand L, Maali Amiri R (2010) What happens in plant molecular responses to cold stress? Acta Physiol Plant 32:419–431Google Scholar
  95. Heidarvand L, Maali-Amiri R (2013) Physio-biochemical and proteome analysis of chickpea in early phases of cold stress. J Plant Physiol 170:459–469PubMedGoogle Scholar
  96. Henriksson NK, Trewavas AJ (2003) The effect of short-term low-temperature treatments on gene expression in Arabidopsis correlates with changes in intracellular Ca2+ levels. Plant Cell Environ 26:485–496Google Scholar
  97. Hoffmann-Sommergruber K (2000) Plant allergens and pathogenesis-related proteins. What do they have in common? Int Arch Allergy Immunol 122:155–166PubMedGoogle Scholar
  98. Hong Z, Lakkineni K, Zhang Z, Verma DP (2000) Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136PubMedCentralPubMedGoogle Scholar
  99. Houde M, Dallaire S, N’Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2:381–387PubMedGoogle Scholar
  100. Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) 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. Plant Physiol 129:1086–1094PubMedCentralPubMedGoogle Scholar
  101. Hu Y, Zhang L, Zhao L, Li J, He S (2011) Trichostatin a selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS One 6(7):e22132PubMedCentralPubMedGoogle Scholar
  102. Huang C, Ding S, Zhang H, Du H, An L (2011) CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Sci 181:57–64PubMedGoogle Scholar
  103. Huang XS, Wang W, Zhang Q, Liu JH (2013) A basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiol 162:1178–1194PubMedCentralPubMedGoogle Scholar
  104. Hugly S, Somerville C (1992) A role for membrane lipid polyunsaturation in chloroplast biogenesis at low temperature. Plant Physiol 99:197–202PubMedCentralPubMedGoogle Scholar
  105. Hung SH, Yu CW, Lin CH (2005) Hydrogen peroxide functions as a stress signal in plants. Bot Bull Acad Sin 46:1–10Google Scholar
  106. Hurry V, Strand A, Furbank R, Stitt M (2000) The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana. Plant J 24:383–396PubMedGoogle Scholar
  107. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24:655–665PubMedGoogle Scholar
  108. Imin N, Kerim T, Rolfe BG, Weinman JJ (2004) Effect of early cold stress on the maturation of rice anthers. Proteomics 4:1873–1882PubMedGoogle Scholar
  109. Ishikawa M, Yoshida S (1985) Seasonal changes in plasma membranes and mitochondria isolated from jerusalem artichoke tubers. Possible relationship to cold hardiness. Plant Cell Physiol 26:1331–1344Google Scholar
  110. Ishitani M, Xiong L, Lee H, Stevenson B, Zhu JK (1998) HOS1, a genetic locus involved in cold-responsive gene expression in arabidopsis. Plant Cell 10:1151–1161PubMedCentralPubMedGoogle Scholar
  111. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153PubMedGoogle Scholar
  112. Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917PubMedCentralPubMedGoogle Scholar
  113. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106PubMedGoogle Scholar
  114. Janmohammadi M (2012) Metabolomic analysis of low temperature responses in plants. Curr Opin Agric 1:1–6Google Scholar
  115. Janska A, Marsik P, Zelenkova S, Ovesna J (2010) Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol 12:395–405PubMedGoogle Scholar
  116. Jiang C, Iu B, Singh J (1996) Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol Biol 30:679–684PubMedGoogle Scholar
  117. Jiang QW, Kiyoharu O, Ryozo I (2002) Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol 129:1880–1891Google Scholar
  118. Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H (1996) Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci U S A 93:11274–11279PubMedCentralPubMedGoogle Scholar
  119. Jouve L, Hoffmann L, Hausman J-F (2004) Polyamine, carbohydrate, and proline content changes during salt stress exposure of aspen (Populus tremula L.): involvement of oxidation and osmoregulation metabolism. Plant Biol (Stuttg) 6:74–80Google Scholar
  120. Jung SH, Lee JY, Lee DH (2003) Use of SAGE technology to reveal changes in gene expression in Arabidopsis leaves undergoing cold stress. Plant Mol Biol 52:553–567PubMedGoogle Scholar
  121. Jung JH, Seo PJ, Park CM (2012) The E3 ubiquitin ligase HOS1 regulates Arabidopsis flowering by mediating CONSTANS degradation under cold stress. J Biol Chem 287:43277–43287PubMedCentralPubMedGoogle Scholar
  122. Jung JH, Park JH, Lee S, To TK, Kim JM, Seki M, Park CM (2013) The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25:4378–4390PubMedCentralPubMedGoogle Scholar
  123. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome. Plant Physiol 136:4159–4168PubMedCentralPubMedGoogle Scholar
  124. Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981PubMedGoogle Scholar
  125. Kasamo K (1988) Inhibition of tonoplast and plasma membrane H+-ATPase activity in rice (Oryza sativa L.) culture cells by local anesthetics. Plant Cell Physiol 29:215–221Google Scholar
  126. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17(3):287–291PubMedGoogle Scholar
  127. Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350PubMedGoogle Scholar
  128. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722PubMedGoogle Scholar
  129. Kaul S, Sharma SS, Mehta IK (2008) Free radical scavenging potential of L-proline: evidence from in vitro assays. Amino Acids 34:315–320PubMedGoogle Scholar
  130. 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 (Amsterdam) 128:174–181Google Scholar
  131. Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36:141–154PubMedGoogle Scholar
  132. Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO, Cho MJ (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 25(3):247–259PubMedGoogle Scholar
  133. Kim TE, Kim S-K, Han TJ, Lee JS, Chang SC (2002) ABA and polyamines act independently in primary leaves of cold-stressed tomato (Lycopersicon esculentum). Physiol Plant 115:370–376PubMedGoogle Scholar
  134. Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423PubMedCentralPubMedGoogle Scholar
  135. Kim MC, Chung WS, Yun DJ, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21PubMedCentralPubMedGoogle Scholar
  136. Kitashiba H, Ishizaka T, Isuzugawa K, Nishimura K, Suzuki T (2004) Expression of a sweet cherry DREB1/CBF ortholog in Arabidopsis confers salt and freezing tolerance. J Plant Physiol 161:1171–1176PubMedGoogle Scholar
  137. Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267PubMedGoogle Scholar
  138. Knight MR, Campbell AK, Smith SM, Trewavas AJ (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352:524–526PubMedGoogle Scholar
  139. Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489–503PubMedCentralPubMedGoogle Scholar
  140. Knight H, Veale EL, Warren GJ, Knight MR (1999) The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell 11:875–886PubMedCentralPubMedGoogle Scholar
  141. Kodama H, Hamada T, Horiguchi G, Nishimura M, Iba K (1994) Genetic enhancement of cold tolerance by expression of a gene for chloroplast v-3 fatty acid desaturase in transgenic tobacco. Plant Physiol 105:601–605PubMedCentralPubMedGoogle Scholar
  142. Koiwa H, Hausmann S, Bang WY, Ueda A, Kondo N, Hiraguri A, Fukuhara T, Bahk JD, Yun DJ, Bressan RA, Hasegawa PM, Shuman S (2004) Arabidopsis C-terminal domain phosphatase-like 1 and 2 are essential Ser-5-specific C-terminal domain phosphatases. Proc Natl Acad Sci U S A 101:14539–14544PubMedCentralPubMedGoogle Scholar
  143. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Gelgenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci U S A 102:11118–11123PubMedCentralPubMedGoogle Scholar
  144. Komatsu S, Yang G, Khan M, Onodera H, Toki S, Yamaguchi M (2007) Over-expression of calcium dependent protein kinase 13 and calreticulin interacting protein 1 confers cold tolerance on rice plants. Mol Genet Genomics 277:713–723PubMedGoogle Scholar
  145. Korn M, Peterek S, Mock HP, Heyer AG, Hincha DK (2008) Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ 31(6):813–827PubMedCentralPubMedGoogle Scholar
  146. Korn M, Gartner T, Erban A, Kopka J, Selbig J, Hincha DK (2010) Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant 3(1):224–235PubMedCentralPubMedGoogle Scholar
  147. Kosová K, Vítámvás P, Prášil IT (2007) The role of dehydrins in plant response to cold. Biol Plant 51:601–617Google Scholar
  148. Kosova K, Vitamvas P, Prasil IT, Renaut J (2011) Plant proteome changes under abiotic stress–contribution of proteomics studies to understanding plant stress response. J Proteomics 74:1301–1322PubMedGoogle Scholar
  149. Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381–390PubMedCentralPubMedGoogle Scholar
  150. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97:2940–2945PubMedCentralPubMedGoogle Scholar
  151. Krause E, Dathe M, Wieprecht T, Bienert M (1999) Noncovalent immobilized artificial membrane chromatography, an improved method for describing peptide-lipid bilayer interactions. J Chromatogr A 849:125–133PubMedGoogle Scholar
  152. Kubis J (2003) Polyamines and “scavenging system”: influence of exogenous spermidine on catalase and guaiacol peroxidase activities, and free polyamine level in barley leaves under water deficit. Acta Physiol Plant 25:337–343Google Scholar
  153. Kudla J, Xu Q, Harter K, Gruissem W, Luan S (1999) Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proc Natl Acad Sci U S A 96:4718–4723PubMedCentralPubMedGoogle Scholar
  154. Laudencia-Chingcuanco D, Ganeshan S, You F, Fowler B, Chibbar R, Anderson O (2011) Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L.). BMC Genomics 12:299PubMedCentralPubMedGoogle Scholar
  155. Lazaro A, Valverde F, Pineiro M, Jarillo JA (2012) The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. Plant Cell 24:982–999PubMedCentralPubMedGoogle Scholar
  156. Lee JY, Lee DH (2003) Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress. Plant Physiol 132:517–529PubMedCentralPubMedGoogle Scholar
  157. Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo–cytoplasmic partitioning. Genes Dev 15:912–924PubMedCentralPubMedGoogle Scholar
  158. Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002a) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21:2692–2702PubMedCentralPubMedGoogle Scholar
  159. Lee BH, Lee H, Xiong L, Zhu JK (2002b) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14:1235–1251PubMedCentralPubMedGoogle Scholar
  160. Lee SC, Lee MY, Kim SJ, Jun SH, An G, Kim SR (2005a) Characterization of an abiotic stress-inducible dehydrin gene, OsDhn1, in rice (Oryza sativa L.). Mol Cells 19:212–218PubMedGoogle Scholar
  161. Lee BH, Henderson DA, Zhu JK (2005b) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175PubMedCentralPubMedGoogle Scholar
  162. Lee D-G, Ahsan N, Lee S-H, Lee J, Bahk JD, Kang KY, Lee BH (2009) Chilling stress-induced proteomic changes in rice roots. J Plant Physiol 166:1–11PubMedGoogle Scholar
  163. Lee YP, Babakov A, de Boer B, Zuther E, Hincha DK (2012a) Comparison of freezing tolerance, compatible solutes and polyamines in geographically diverse collections of Thellungiella sp. and Arabidopsis thaliana accessions. BMC Plant Biol 12:131PubMedCentralPubMedGoogle Scholar
  164. Lee JH, Kim JJ, Kim SH, Cho HJ, Kim J, Ahn JH (2012b) The E3 ubiquitin ligase HOS1 regulates low ambient temperature-responsive flowering in Arabidopsis thaliana. Plant Cell Physiol 53:1802–1814PubMedGoogle Scholar
  165. Lee JH, Kim SH, Kim JJ, Ahn JH (2012c) Alternative splicing and expression analysis of High expression of osmotically responsive genes1 (HOS1) in Arabidopsis. BMB Rep 45:515–520PubMedGoogle Scholar
  166. Levitt J (1980) Responses of plants to environmental stress, vol 1, 2nd edn. Academic, New York, pp 166–222Google Scholar
  167. Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane-bound phospholipase Ddelta enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–433PubMedGoogle Scholar
  168. Li J, Wang L, Zhu W, Wang N, Xin H, Li S (2014) Characterization of two VvICE1 genes isolated from ‘Muscat Hamburg’ grapevine and their effect on the tolerance to abiotic stresses. Sci Hortic 165:266–273Google Scholar
  169. Lin Y, Zheng H, Zhang Q, Liu C, Zhang Z (2014) Functional profiling of EcaICE1 transcription factor gene from Eucalyptus camaldulensis involved in cold response in tobacco plants. J Plant Biochem Biotechnol 23:141–150Google Scholar
  170. Lister R, Gregory BD, Ecker JR (2009) Next is now: new technologies for sequencing of genomes, transcriptomes, and beyond. Curr Opin Plant Biol 12:107–118PubMedCentralPubMedGoogle Scholar
  171. 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 in Arabidopsis. Plant Cell 10:1391–1406PubMedCentralPubMedGoogle Scholar
  172. Liu JJ, Ekramoddoullah AKM, Yu X (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant 119:544–553Google Scholar
  173. Liu L, Duan L, Zhang J, Zhang Z, Mi G, Ren H (2010) Cucumber (Cucumis sativus L.) over-expressing cold-induced transcriptome regulator ICE1 exhibits changed morphological characters and enhances chilling tolerance. Sci Hortic 124:29–33Google Scholar
  174. Liu MQ, Shi J, Lu CF (2013) Identification of stress-responsive genes in Ammopiptanthus mongolicus using ESTs generated from cold- and drought-stressed seedlings. BMC Plant Biol 13Google Scholar
  175. Livingston DP, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cell Mol Life Sci 66:2007–2023PubMedCentralPubMedGoogle Scholar
  176. Lopez-Matas MA, Nunez P, Soto A, Allona I, Casado R, Collada C, Guevara MA, Aragoncillo C, Gomez L (2004) Protein cryoprotective activity of a cytosolic small heat shock protein that accumulates constitutively in chestnut stems and is up-regulated by low and high temperatures. Plant Physiol 134:1708–1717PubMedCentralPubMedGoogle Scholar
  177. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14(Suppl):S389–S400PubMedCentralPubMedGoogle Scholar
  178. MacGregor DR, Gould P, Foreman J, Griffiths J, Bird S, Page R, Stewart K, Steel G, Young J, Paszkiewicz K, Millar AJ, Halliday KJ, Hall AJ, Penfield S (2013) High expression of osmotically responsive genes1 is required for circadian periodicity through the promotion of nucleo-cytoplasmic mRNA export in Arabidopsis. Plant Cell 25:4391–4404PubMedCentralPubMedGoogle Scholar
  179. 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 38:982–993PubMedGoogle Scholar
  180. Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Fujita M, Yoshiwara K, Matsukura S, Morishita Y et al (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150(4):1972–1980PubMedCentralPubMedGoogle Scholar
  181. Maul P, McCollum GT, Popp M, Guy CL, Porat R (2008) Transcriptome profiling of grapefruit flavedo following exposure to low temperature and conditioning treatments uncovers principal molecular components involved in chilling tolerance and susceptibility. Plant Cell Environ 31:752–768PubMedGoogle Scholar
  182. Mauro S, Dainese P, Lannoye R, Bassi R (1997) Cold-resistant and cold-sensitive maize lines differ in the phosphorylation of the photosystem II subunit, CP29. Plant Physiol 115:171–180PubMedCentralPubMedGoogle Scholar
  183. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294PubMedGoogle Scholar
  184. Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–470PubMedCentralPubMedGoogle Scholar
  185. Miquel M, James D, Dooner H, Browse J (1993) Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proc Natl Acad Sci U S A 90:6208–6212PubMedCentralPubMedGoogle Scholar
  186. Mittal D, Madhyastha DA, Grover A (2012) Genome-wide transcriptional profiles during temperature and oxidative stress reveals coordinated expression patterns and overlapping regulons in rice. PLoS One 7:e40899PubMedCentralPubMedGoogle Scholar
  187. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedGoogle Scholar
  188. Miura K, Jin JB, Hasegawa PM (2007) Sumoylation, a post-translational regulatory process in plants. Curr Opin Plant Biol 10:495–502PubMedGoogle Scholar
  189. 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 67:269–279PubMedGoogle Scholar
  190. Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2012) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J doi: 10.1111/tpj.12014Google Scholar
  191. Monroy AF, Dhindsa RS (1995) Low temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 °C. Plant Cell 7:321–331PubMedCentralPubMedGoogle Scholar
  192. Monroy AF, Sarhan F, Dhindsa RS (1993) Cold-induced changes in freezing tolerance, protein phosphorylation, and gene expression (evidence for a role of calcium). Plant Physiol 102:1227–1235PubMedCentralPubMedGoogle Scholar
  193. 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 13:653–660Google Scholar
  194. Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Langridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9(2):230–249PubMedGoogle Scholar
  195. Morsy MR, Jouve L, Hausman J-F, Hoffmann L, Stewart JM (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164:157–167PubMedGoogle Scholar
  196. Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713Google Scholar
  197. Murchie EH, Sarrobert C, Contard P, Betsche T, Foyer CH, Galtier N (1999) Overexpresion of sucrose-phosphate synthase in tomato plants grown with Co2 enrichment leads to decreased foliar carbohydrate accumulation relative to transfromed controls. Plant Physiol Biochem 37(4):251–260Google Scholar
  198. Nadimpalli R, Yalpani N, Johal GS, Simmons CR (2000) Prohibitins, stomatins, and plant disease response genes compose a protein superfamily that controls cell proliferation, ion channel regulation, and death. J Biol Chem 275:29579–29586PubMedGoogle Scholar
  199. Nakagami H, Soukupova H, Schikora A, Zarsky V, Hirt H (2006) A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem 281:38697–38704PubMedGoogle Scholar
  200. Nakamura J, Yuasa T, Thi HT, Harano K, Tanaka S, Iwata T, Phan T, Mari II (2011) Rice homologs of inducer of CBF expression (OsICE) are involved in cold acclimation. Plant Biotechnol 28:303–309Google Scholar
  201. Nakayama K, Okawa K, Kakizaki T, Inaba T (2008) Evaluation of the protective activities of a late embryogenesis abundant (LEA) related protein, Cor15am, during various stresses in vitro. Biosci Biotechnol Biochem 72:1642–1645PubMedGoogle Scholar
  202. 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(372):1237–1247PubMedGoogle Scholar
  203. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Riberiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176PubMedGoogle Scholar
  204. Neilson KA, Mariani M, Haynes PA (2011) Quantitative proteomic analysis of cold-responsive proteins in rice. Proteomics 11:1696–1706PubMedGoogle Scholar
  205. Nick P (2000) Control of the response to low temperatures. In: Nick P (ed) Plant microtubules: potential for biotechnology. Springer, Berlin, pp 121–135Google Scholar
  206. 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 U S A 101:3985–3990PubMedCentralPubMedGoogle Scholar
  207. 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 U S A 104:21002–21007PubMedCentralPubMedGoogle Scholar
  208. Nylander M, Svensson J, Palva ET, Welin BV (2001) Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol 45:263–279PubMedGoogle Scholar
  209. O’Kane D, Gill V, Boyd P, Burdon R (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198:371–377PubMedGoogle Scholar
  210. Oakenfull RJ, Baxter R, Knight MR (2013) A C-repeat binding factor transcriptional activator (CBF/DREB1) from European bilberry (Vaccinium myrtillus) induces freezing tolerance when expressed in Arabidopsis thaliana. PLoS One 8:e54119PubMedCentralPubMedGoogle Scholar
  211. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351PubMedCentralPubMedGoogle Scholar
  212. Oh SJ, Kwon CW, Choi DW, Song SI, Kim JK (2007) Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol J 5:646–656PubMedGoogle Scholar
  213. Ohno R, Takumi S, Nakamura C (2003) Kinetics of transcript and protein accumulation of a low-molecular-weight wheat LEA D-11 dehydrin in response to low temperature. J Plant Physiol 160:193–200PubMedGoogle Scholar
  214. Oliveira G, Peñuelas J (2004) Effects of winter cold stress on photosynthesis and photochemical efficiency of PSII of the Mediterranean Cistus albidus L. and Quercus ilex L. Plant Eco 175:179–191Google Scholar
  215. Ortiz-Masia D, Perez-Amador MA, Carbonell J, Marcote MJ (2007) Diverse stress signals activate the C1 subgroup MAP kinases of Arabidopsis. FEBS Lett 581:1834–1840PubMedGoogle Scholar
  216. 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 23:785–794PubMedGoogle Scholar
  217. Ouellet F (2007) Cold acclimation and freezing tolerance in plants. Encyclopaedia of Life Sciences. 1–6Google Scholar
  218. Ouellet F, Vazquez-Tello A, Sarhan F (1998) The wheat wcs120 promoter is cold-inducible in both monocotyledonous and dicotyledonous species. FEBS Lett 423:324–328PubMedGoogle Scholar
  219. Owens CL, Thomashow MF, Hancock JF, Iezzoni AF (2002) CBF1 orthologs in sour cherry and strawberry and the heterologous expression of CBF1 in strawberry. J Am Soc Hortic Sci 127:489–494Google Scholar
  220. Pandey GK (2008) Emergence of a novel calcium signaling pathway in plants: CBL-CIPK signaling network. Physiol Mol Biol Plants 14:51–68PubMedCentralPubMedGoogle Scholar
  221. Pang T, Ye CY, Xia XL, Yin WL (2013) De novo sequencing and transcriptome analysis of the desert shrub, Ammopiptanthus mongolicus, during cold acclimation using Illumina/Solexa. BMC Genomics 14:488PubMedCentralPubMedGoogle Scholar
  222. Pasquali G, Biricolti S, Locatelli F, Baldoni E, Mattana M (2008) Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep 27:1677–1686PubMedGoogle Scholar
  223. Paul MJ (2008) Trehalose 6-phosphate: a signal of sucrose status. Biochem J 412:e1–e2PubMedGoogle Scholar
  224. Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47:493–500PubMedGoogle Scholar
  225. Peng T, Zhu XF, Fan QJ, Sun PP, Liu JH (2012) Identification and characterization of low temperature stress responsive genes in Poncirus trifoliata by suppression subtractive hybridization. Gene 492:220–228PubMedGoogle Scholar
  226. Peng PH, Lin CH, Tsai HW, Lin TY (2014) Cold response in phalaenopsis aphrodite and characterization of PaCBF1 and PaICE1. Plant Cell Physiol pii: pcu093. [Epub ahead of print]Google Scholar
  227. Pennycooke JC, Cheng H, Roberts SM, Yang Q, Rhee SY, Stockinger EJ (2008a) The low temperature-responsive, Solanum CBF1 genes maintain high identity in their upstream regions in a genomic environment undergoing gene duplications, deletions, and rearrangements. Plant Mol Biol 67:483–497PubMedGoogle Scholar
  228. Pennycooke JC, Cheng H, Stockinger EJ (2008b) Comparative genomic sequence and expression analyses of Medicago truncatula and alfalfa subspecies falcata COLD-ACCLIMATION-SPECIFIC genes. Plant Physiol 146:1242–1254PubMedCentralPubMedGoogle Scholar
  229. Porat R, Pasentsis K, Rozentzvieg D, Gerasopoulos D, Falara V, Samach A, Lurie S, Kanellis AK (2004) Isolation of a dehydrin cDNA from orange and grapefruit citrus fruit that is specifically induced by the combination of heat followed by chilling temperatures. Physiol Plant 120:256–264PubMedGoogle Scholar
  230. Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in Maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74PubMedCentralPubMedGoogle Scholar
  231. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052PubMedGoogle Scholar
  232. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767PubMedCentralPubMedGoogle Scholar
  233. Ray S, Agarwal P, Arora R, Kapoor S, Tyagi AK (2007) Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in rice (Oryza sativa L. ssp. indica). Mol Genet Genomics 278(5):493–505PubMedGoogle Scholar
  234. Reddy VS, Reddy AS (2004) Proteomics of calcium signaling components in plants. Phytochemistry 65:1745–1776PubMedGoogle Scholar
  235. Rekarte-Cowie I, Ebshish OS, Mohamed KS, Pearce RS (2008) Sucrose helps regulate cold acclimation of Arabidopsis thaliana. J Exp Bot 59:4205–4217PubMedCentralPubMedGoogle Scholar
  236. Renaut J, Lutts S, Hoffmann L, Hausman JF (2004) Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biol 6:81–90PubMedGoogle Scholar
  237. Renaut J, Hausman J-F, Wisniewski ME (2006) Proteomics and low-temperature studies: bridging the gap between gene expression and metabolism. Physiol Plant 126:97–109Google Scholar
  238. 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 4:589–600Google Scholar
  239. Rinalducci S, Egidi MG, Karimzadeh G, Jazii FR, Zolla L (2011) Proteomic analysis of a spring wheat cultivar in response to prolonged cold stress. Electrophoresis 32:1807–1818PubMedGoogle Scholar
  240. Robinson SJ, Parkin IA (2008) Differential SAGE analysis in Arabidopsis uncovers increased transcriptome complexity in response to low temperature. BMC Genomics 9:434PubMedCentralPubMedGoogle Scholar
  241. Rontein D, Basset G, Hanson AD (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4:49–56PubMedGoogle Scholar
  242. Rorat T (2006) Plant dehydrins–tissue location, structure and function. Cell Mol Biol Lett 11:536–556PubMedGoogle Scholar
  243. Ruiz JM, Sánchez E, García PC, Lefebre LRL, Rivero RM, Romero L (2002) Proline metabolism and NAD kinase activity in greenbean plants subjected to cold-shock. Phytochemistry 59:473–478PubMedGoogle Scholar
  244. Sabehat A, Lurie S, Weiss D (1998) Expression of small heat-shock proteins at low temperatures. A possible role in protecting against chilling injuries. Plant Physiol 117:651–658PubMedCentralPubMedGoogle Scholar
  245. Sage RF, Kubien DS (2007) The temperature response of C(3) and C(4) photosynthesis. Plant Cell Environ 30:1086–1106PubMedGoogle Scholar
  246. Saijo Y, Kinoshita N, Ishiyama K, Hata S, Kyozuka J, Hayakawa T, Nakamura T, Shimamoto K, Yamaya T, Izui K (2001) A Ca2+ dependent protein kinase that endows rice plants with cold- and salt-stress tolerance functions in vascular bundles. Plant Cell Physiol 42:1228–1233PubMedGoogle Scholar
  247. Salinas J (2002) Molecular mechanisms of signal transduction in cold acclimation. In: Scheel D, Wasternack C (eds) Plant signal transduction. Oxford University Press, Oxford, pp 116–139Google Scholar
  248. 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 27:1–12PubMedGoogle Scholar
  249. 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 31:629–638PubMedGoogle Scholar
  250. Sathyanarayanan PV, Poovaiah BW (2004) Decoding Ca2+ signals in plants. Crit Rev Plant Sci 23:1–11PubMedGoogle Scholar
  251. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72PubMedCentralPubMedGoogle Scholar
  252. Seki M, Ishida J, Narusaka M, Fujita M, Nanjo T, Umezawa T, Kamiya A, Nakajima M, Enju A, Sakurai T et al (2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2(6):282–291PubMedGoogle Scholar
  253. Shan W, Kuang JF, Lu WJ, Chen JY (2014) Banana fruit NAC transcription factor MaNAC1 is a direct target of MaICE1 and involved in cold stress through interacting with MaCBF1. Plant Cell Environ 37(9):2116–2127PubMedGoogle Scholar
  254. Sharma P, Sharma N, Deswal R (2005) The molecular biology of the low-temperature response in plants. Bioessays 27:1048–1059PubMedGoogle Scholar
  255. Shen YG, Zhang WK, He SJ, Zhang JS, Liu Q, Chen SY (2003) An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theor Appl Genet 106:923–930PubMedGoogle Scholar
  256. Shi H, Ye T, Zhong B, Liu X, Jin R, Chan Z (2014) AtHAP5A modulates freezing stress resistance in Arabidopsis through binding to CCAAT motif of AtXTH21. New Phytol 203:554–567PubMedGoogle Scholar
  257. Shimamura C, Ohno R, Nakamura C, Takumi S (2006) Improvement of freezing tolerance in tobacco plants expressing a cold-responsive and chloroplast-targeting protein WCOR15 of wheat. J Plant Physiol 163:213–219PubMedGoogle Scholar
  258. Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7:161–167PubMedGoogle Scholar
  259. Si J, Wang J-H, Zhang L-J, Zhang H, Liu Y-J, An L-Z (2009) CbCOR15, A cold-regulated gene from alpine chorispora bungeana, confers cold tolerance in transgenic tobacco. J Plant Biol 52:593–601Google Scholar
  260. Siddiqua M, Nassuth A (2011) Vitis CBF1 and Vitis CBF4 differ in their effect on Arabidopsis abiotic stress tolerance, development and gene expression. Plant Cell Environ 34:1345–1359PubMedGoogle Scholar
  261. Signora L, Galtier N, Skøt L, Lucas H, Foyer CH (1998) Over-expression of sucrose phosphate synthase in Arabidopsis thaliana results in increased foliar sucrose/starch ratios and favours decreased foliar carbohydrate accumulation in plants after prolonged growth with CO enrichment. J Exp Bot 49:669–680Google Scholar
  262. Skinner DZ (2009) Post-acclimation transcriptome adjustment is a major factor in freezing tolerance of winter wheat. Funct Integr Genomics 9:513–523PubMedGoogle Scholar
  263. 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 59:533–551PubMedGoogle Scholar
  264. Skinner JS, Szucs P, von Zitzewitz J, Marquez-Cedillo L, Filichkin T, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2006) Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theor Appl Genet 112:832–842PubMedGoogle Scholar
  265. Solanke AU, Sharma AK (2008) Signal transduction during cold stress in plants. Physiol Mol Biol Plants 14:69–79PubMedCentralPubMedGoogle Scholar
  266. Soltesz A, Smedley M, Vashegyi I, Galiba G, Harwood W, Vagujfalvi A (2013) Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. J Exp Bot 64:1849–1862PubMedCentralPubMedGoogle Scholar
  267. Song Y, Chen Q, Ci D, Zhang D (2013) Transcriptome profiling reveals differential transcript abundance in response to chilling stress in Populus simonii. Plant Cell Rep 32:1407–1425PubMedGoogle Scholar
  268. 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 211–312Google Scholar
  269. Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domaincontaining transcription 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 U S A 94:1035–1040PubMedCentralPubMedGoogle Scholar
  270. Strand A, Hurry V, Gustafsson P, Gardeström P (1997) Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J 12:605–614PubMedGoogle Scholar
  271. Strand A, Hurry V, Henkes S, Huner N, Gustafsson P, Gardeström P, Stitt M (1999) Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway. Plant Physiol 119:1387–1398PubMedCentralPubMedGoogle Scholar
  272. Strand A, Zrenner R, Trevanion S, Stitt M, Gustafsson P, Gardeström P (2000) Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 23:759–770PubMedGoogle Scholar
  273. Strand Å, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2003) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Envi 26:523–535Google Scholar
  274. Stushnoff C, Remmele RL Jr, Essensee V, Mcneil M (1993) Low temperature induced biochemical mechanisms: implications for cold acclimation and de-acclimation. Springer NATO ASI series 16:647–657Google Scholar
  275. 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 153:145–158PubMedCentralPubMedGoogle Scholar
  276. Sung DY, Vierling E, Guy CL (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126:789–800PubMedCentralPubMedGoogle Scholar
  277. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51Google Scholar
  278. Tähtiharju S, Palva T (2001) Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J 26:461–470PubMedGoogle Scholar
  279. Tahtiharju S, Sangwan V, Monroy AF, Dhindsa RS, Borg M (1997) The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. Planta 203:442–447PubMedGoogle Scholar
  280. Takahashi D, Li B, Nakayama T, Kawamura Y, Uemura M (2013) Plant plasma membrane proteomics for improving cold tolerance. Front Plant Sci 4:90PubMedCentralPubMedGoogle Scholar
  281. Takumi S, Shimamura C, Kobayashi F (2008) Increased freezing tolerance through up-regulation of downstream genes via the wheat CBF gene in transgenic tobacco. Plant Physiol Biochem 46:205–211PubMedGoogle Scholar
  282. 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 15:141–152PubMedGoogle Scholar
  283. Thakur P, Nayyar H (2013) Facing the cold stress by plants in the changing environment: sensing, signalling, and defending mechanisms. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, New York, pp 29–69Google Scholar
  284. Theocharis A, Clement C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105PubMedGoogle Scholar
  285. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8PubMedCentralPubMedGoogle Scholar
  286. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599PubMedGoogle Scholar
  287. Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71:391–411PubMedGoogle Scholar
  288. Tominaga Y, Nakagawara C, Kawamura Y, Uemura M (2006) Effect of plasma membrane-associated proteins on acquisition of freezing tolerance in Arabidopsis thaliana. In: Chen THH, Uemura M, Fujikawa S (eds) Cold hardiness in plants: molecular genetics, cell biology and physiology. CABI Publishing, Oxfordshire, pp 235–249Google Scholar
  289. Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454PubMedGoogle Scholar
  290. Töpfer N, Caldana C, Grimbs S, Willmitzer L, Fernie AR, Nikoloski Z (2013) Integration of genome-scale modeling and transcript profiling reveals metabolic pathways underlying light and temperature acclimation in Arabidopsis. Plant Cell 25:1197–1211PubMedCentralPubMedGoogle Scholar
  291. Townley HE, Knight MR (2002) Calmodulin as a potential negative regulator of Arabidopsis COR gene expression. Plant Physiol 128:1169–1172PubMedGoogle Scholar
  292. Tsvetkova NM, Horvath I, Torok Z, Wolkers WF, Balogi Z, Shigapova N, Crowe LM, Tablin F, Vierling E, Crowe JH et al (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci U S A 99(21):13504–13509PubMedCentralPubMedGoogle Scholar
  293. Tuteja N, Mahajan S (2007) Further characterization of calcineurin B-like protein and its interacting partner CBL-interacting protein kinase from Pisum sativum. Plant Signal Behav 2:358–361PubMedCentralPubMedGoogle Scholar
  294. Uemura M, Steponkus PL (1994) A contract of the plasma membrane lipid composition of oat and rye leaves inrelation to freezing tolerance. Plant Physiol 104:479–496PubMedCentralPubMedGoogle Scholar
  295. Uemura M, Yoshida S (1984) Involvement of plasma membrane alterations in cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 75:818–826PubMedCentralPubMedGoogle Scholar
  296. Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-lnduced lesions). Plant Physiol 109:15–30PubMedCentralPubMedGoogle Scholar
  297. 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 131:1800–1807PubMedCentralPubMedGoogle Scholar
  298. Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89Google Scholar
  299. Urzua U, Kersten PJ, Vicuna R (1998) Manganese peroxidase-dependent oxidation of glyoxylic and oxalic acids synthesized by ceriporiopsis subvermispora produces extracellular hydrogen peroxide. Appl Environ Microbiol 64:68–73PubMedCentralPubMedGoogle Scholar
  300. Vannini C, Locatelli F, Bracale M, Magnani E, Marsoni M, Osnato M, Mattana M, Baldoni E, Coraggio I (2004) Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant J 37:115–127PubMedGoogle Scholar
  301. 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 580:4218–4223PubMedGoogle Scholar
  302. Venu RC, Sreerekha MV, Sheshu Madhav M, Nobuta K, Mohan KM, Chen S, Jia Y, Meyers BC, Wang G-L (2013) Deep transcriptome sequencing reveals the expression of key functional and regulatory genes involved in the abiotic stress signaling pathways in rice. J Plant Biol 56:216–231Google Scholar
  303. 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 41:195–211PubMedGoogle Scholar
  304. Wahl MC, Moller W (2002) Structure and function of the acidic ribosomal stalk proteins. Curr Protein Pept Sci 3:93–106PubMedGoogle Scholar
  305. Wang X, Li W, Li M, Welti R (2006) Profiling lipid changes in plant response to low temperatures. Physiol Plant 126:90–96Google Scholar
  306. Wang Y, Jiang CJ, Li YY, Wei CL, Deng WW (2012) CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis. Plant Cell Rep 31:27–34PubMedGoogle Scholar
  307. Wang XC, Zhao QY, Ma CL, Zhang ZH, Cao HL, Kong YM, Yue C, Hao XY, Chen L, Ma JQ, Jin JQ, Li X, Yang YJ (2013) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics 14:415PubMedCentralPubMedGoogle Scholar
  308. Webb MS, Steponkus PL (1993) Freeze-induced membrane ultrastructural alterations in rye (Secale cereale) leaves. Plant Physiol 101:955–963PubMedCentralPubMedGoogle Scholar
  309. Welin BV, Olson A, Nylander M, Palva ET (1994) Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131–144PubMedGoogle Scholar
  310. Welling A, Palva ET (2008) Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol 147:1199–1211PubMedCentralPubMedGoogle Scholar
  311. Wisniewski J, Orosz A, Allada R, Wu C (1996) The C-terminal region of Drosophila heat shock factor (HSF) contains a constitutively functional transactivation domain. Nucleic Acids Res 24:367–374PubMedCentralPubMedGoogle Scholar
  312. Wisniewski ME, Bassett CL, Renaut J, Farrell R, Tworkoski T, Artlip TS (2006) Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol 26:575–584PubMedGoogle Scholar
  313. Wittmann-Liebold B, Graack HR, Pohl T (2006) Two-dimensional gel electrophoresis as tool for proteomics studies in combination with protein identification by mass spectrometry. Proteomics 6:4688–4703PubMedGoogle Scholar
  314. Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428PubMedCentralPubMedGoogle Scholar
  315. Xiang DJ, Hu XY, Zhang Y et al (2008) Overexpression of ICE1 gene in transgenic rice improves cold tolerance. Rice Sci 15(3):173–178Google Scholar
  316. Xiang D, Man L, Yin K, Song Q, Wang L, Zhao M, Xu Z (2013) Overexpression of a ItICE1 gene from Isatis tinctoria enhances cold tolerance in rice. Mol Breeding 32:617–628Google Scholar
  317. Xin Z, Browse J (1998) Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc Natl Acad Sci U S A 95(13):7799–7804PubMedCentralPubMedGoogle Scholar
  318. Xin Z, Mandaokar A, Chen J, Last RL, Browse J (2007) Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. Plant J 49(5):786–799PubMedGoogle Scholar
  319. Xin H, Zhu W, Wang L, Xiang Y, Fang L, Li J, Sun X, Wang N, Londo JP, Li S (2013) Genome wide transcriptional profile analysis of Vitis amurensis and Vitis vinifera in response to cold stress. PLoS One 8:e58740PubMedCentralPubMedGoogle Scholar
  320. Xiong Y, Fei SZ (2006) Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). Planta 224:878–888PubMedGoogle Scholar
  321. Xiong L, Ishitani M, Zhu JK (1999) Interaction of osmotic stress, temperature, and abscisic acid in the regulation of gene expression in Arabidopsis. Plant Physiol 119:205–212PubMedCentralPubMedGoogle Scholar
  322. Xiong L, Lee H, Ishitani M, Tanaka Y, Stevenson B, Koiwa H, Bressan RA, Hasegawa PM, Zhu JK (2002) Repression of stress-responsive genes by FIERY2, a novel transcriptional regulator in Arabidopsis. Proc Natl Acad Sci U S A 99:10899–10904PubMedCentralPubMedGoogle Scholar
  323. Xiong AS, Jiang HH, Zhuang J, Peng RH, Jin XF, Zhu B, Wang F, Zhang J, Yao QH (2013) Expression and function of a modified AP2/ERF transcription factor from Brassica napus enhances cold tolerance in transgenic Arabidopsis. Mol Biotechnol 53:198–206PubMedGoogle Scholar
  324. Xu W, Jiao Y, Li R, Zhang N, Xiao D, Ding X, Wang Z (2014) Chinese wild-growing vitis amurensis ICE1 and ICE2 encode MYC-type bHLH transcription activators that regulate cold tolerance in Arabidopsis. PLoS One 9:e102303PubMedCentralPubMedGoogle Scholar
  325. Xue GP (2003) The DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature. Plant J 33:373–383PubMedGoogle Scholar
  326. Yaish MW, Doxey AC, McConkey BJ, Moffatt BA, Griffith M (2006) Cold-active winter rye glucanases with ice-binding capacity. Plant Physiol 141:1459–1472PubMedCentralPubMedGoogle Scholar
  327. Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264PubMedCentralPubMedGoogle Scholar
  328. Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20:3389–3404PubMedCentralPubMedGoogle Scholar
  329. 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 5:484–496PubMedGoogle Scholar
  330. Yang T, Poovaiah BW (2003) Calcium/calmodulin mediated signal network in plants. Trends Plant Sci 8:505–512PubMedGoogle Scholar
  331. Yang W, Liu XD, Chi XJ, Wu CA, Li YZ, Song LL, Liu XM, Wang YF, Wang FW, Zhang C, Liu Y, Zong JM, Li HY (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233:219–229PubMedGoogle Scholar
  332. Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556PubMedCentralPubMedGoogle Scholar
  333. Yi AB, Yu LX, Hua T, Hong LW, Wen SL (2011) Comparative profile of Rubisco-interacting proteins from Arabidopsis : photosynthesis under cold conditions. Progr Biochem Biophys 38(5):455–463Google Scholar
  334. Yin Z, Rorat T, Szabala BM, Ziółkowska A, Malepszy S (2006) Expression of a Solanum sogarandinum SK3-type dehydrin enhances cold tolerance in transgenic cucumber seedlings. Plant Sci 170:1164–1172Google Scholar
  335. Yoshida S (1991) Chilling induced inactivation and its recovery of tonoplast H + -ATPase in mung bean cell suspension cultures. Plant Physiol 95:456–460PubMedCentralPubMedGoogle Scholar
  336. Zarka DG, Vogel JT, Cook D, Thomashow MF (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol 133:910–918PubMedCentralPubMedGoogle Scholar
  337. Zhai H, Bai X, Zhu Y, Li Y, Cai H, Ji W, Ji Z, Liu X, Liu X, Li J (2010) A single-repeat R3-MYB transcription factor MYBC1 negatively regulates freezing tolerance in Arabidopsis. Biochem Biophys Res Commun 394(4):1018–1023PubMedGoogle Scholar
  338. Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiol 135(2):615–621PubMedCentralPubMedGoogle Scholar
  339. Zhang W, Jiang B, Li W, Song H, Yu Y, Chen J (2009) Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Sci Hortic (Amsterdam) 122:200–208Google Scholar
  340. Zhang J, Mao Z, Chong K (2013) A global profiling of uncapped mRNAs under cold stress reveals specific decay patterns and endonucleolytic cleavages in Brachypodium distachyon. Genome Biol 14:R92PubMedCentralPubMedGoogle Scholar
  341. Zhao H, Bughrara SS (2008) Isolation and characterization of cold-regulated transcriptional activator LpCBF3 gene from perennial ryegrass (Lolium perenne L.). Mol Genet Genomics 279:585–594PubMedGoogle Scholar
  342. Zhao M-G, Chen L, Zhang L-L, Zhang W-H (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767PubMedCentralPubMedGoogle Scholar
  343. Zhao Z, Tan L, Dang C, Zhang H, Wu Q, An L (2012) Deep-sequencing transcriptome analysis of chilling tolerance mechanisms of a subnival alpine plant, Chorispora bungeana. BMC Plant Biol 12:222PubMedCentralPubMedGoogle Scholar
  344. Zhao ML, Wang JN, Shan W, Fan JG, Kuang JF, Wu KQ, Li XP, Chen WX, He FY, Chen JY, Lu WJ (2013) Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36:30–51PubMedGoogle Scholar
  345. Zhu J, Shi H, Lee BH, Damsz B, Cheng S, Stirm V, Zhu JK, Hasegawa PM, Bressan RA (2004) An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc Natl Acad Sci U S A 101(26):9873–9878PubMedCentralPubMedGoogle Scholar
  346. 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 10:290–295PubMedGoogle Scholar
  347. Zhu Y, Yang H, Mang HG, Hua J (2011) Induction of BAP1 by a moderate decrease in temperature is mediated by ICE1 in Arabidopsis. Plant Physiol 155(1):580–588PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Somya Sinha
    • 1
  • Bharti Kukreja
    • 1
  • Priyanka Arora
    • 1
  • Manisha Sharma
    • 2
  • Girdhar K. Pandey
    • 2
  • Manu Agarwal
    • 1
  • Viswanathan Chinnusamy
    • 3
  1. 1.Department of BotanyUniversity of DelhiNew DelhiIndia
  2. 2.Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia
  3. 3.Division of Plant PhysiologyIndian Agricultural Research InstituteNew DelhiIndia

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