Natural Variation in Freezing Tolerance and Cold Acclimation Response in Arabidopsis thaliana and Related Species

  • Ellen Zuther
  • Yang Ping Lee
  • Alexander Erban
  • Joachim Kopka
  • Dirk K. HinchaEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1081)


During low-temperature exposure, temperate plant species increase their freezing tolerance in a process termed cold acclimation. The molecular mechanisms involved in cold acclimation have been mostly investigated in Arabidopsis thaliana. In addition, other Brassicaceae species related to A. thaliana have been employed in recent years to study plant stress responses on a phylogenetically broader basis and in some cases with extremophile species with a much higher stress tolerance. In this paper, we briefly summarize cold acclimation responses in A. thaliana and current knowledge about cold acclimation in A. thaliana relatives with special emphasis on Eutrema salsugineum and two closely related Thellungiella species. We then present a transcriptomic and metabolomic analysis of cold acclimation in five A. thaliana and two E. salsugineum accessions that differ widely in their freezing tolerance. Differences in the cold responses of the two species are discussed.


Arabidopsis thaliana Cold acclimation Eutrema salsugineum Gene expression Metabolomics Transcriptomics 



Arabidopsis gene identifier




C-repeat binding factor


Cold regulated


Doubled haploid


Dehydration-responsive element binding


Ethylene response factor


Gas chromatography-mass spectrometry


Genome-wide association study


Independent components analysis


Inducer of CBF expression


Lethal temperature of 50% electrolyte leakage


Quantitative trait loci


Recombinant inbred line


RNA sequencing



We would like to thank Ines Fehrle for excellent technical assistance with the GC-MS measurements.


  1. Ahmed NU, Park J-I, Jung H-J, Yang T-J, Hur Y, Nou I-S (2014) Characterization of dihydroflavonol 4-reductase (DFR) genes and their association with cold and freezing stress in Brassica rapa. Gene 550:46–55PubMedCrossRefGoogle Scholar
  2. Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martinez-Zapater JM (2005) Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol 139:1304–1312PubMedPubMedCentralCrossRefGoogle Scholar
  3. Al-Shehbaz IA, O’Kane SL, Price RA (1999) Generic placement of species excluded from Arabidopsis (Brassicaceae). Novon 9:296–307CrossRefGoogle Scholar
  4. Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol Plant 2:3–12PubMedPubMedCentralCrossRefGoogle Scholar
  5. Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci U S A 93:13404–13409PubMedPubMedCentralCrossRefGoogle Scholar
  6. Baduel P, Arnold B, Weisman CM, Hunter B, Bomblies K (2016) Habitat-associated life history and stress-tolerance variation in Arabidopsis arenosa. Plant Physiol 171:437–451PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bailey CD, Koch MA, Mayer M, Mummenhoff K, O’Kane SL, Warwick SI, Windham MD, Al-Shehbaz IA (2006) Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 23:2142–2160PubMedCrossRefGoogle Scholar
  8. Bender M, Heber U, Dietz K-J (1992) Saline growth conditions favour supercooling and increase the freezing tolerance of leaves of barley and wheat. Z Naturforsch 47c:695–700CrossRefGoogle Scholar
  9. Benina M, Obata T, Mehterov N, Ivanov I, Petrov V, Toneva V, Fernie AR, Gechev TS (2013) Comparative metabolic profiling of Haberlea rhodopensis, Thellungiella halophyla, and Arabidopsis thaliana exposed to low temperature. Front Plant Sci 4:499PubMedPubMedCentralCrossRefGoogle Scholar
  10. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300Google Scholar
  11. Bremer A, Kent B, Hauß T, Thalhammer A, Yepuri NR, Darwish TA, Garvey CJ, Bryant G, Hincha DK (2017a) Intrinsically disordered stress protein COR15A resides at the membrane surface during dehydration. Biophys J 113:572–579PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bremer A, Wolff M, Thalhammer A, Hincha DK (2017b) Folding of intrinsically disordered plant LEA proteins is driven by glycerol-induced crowding and the presence of membranes. FEBS J 284:919–936PubMedCrossRefGoogle Scholar
  13. Bressan RA, Zhang C, Zhang H, Hasegawa PM, Bohnert HJ, Zhu JK (2001) Learning from the Arabidopsis experience: the next gene search paradigm. Plant Physiol 127:1354–1360PubMedPubMedCentralCrossRefGoogle Scholar
  14. Candat A, Poupart P, Andrieu J-P, Chevrollier A, Reynier P, Rogniaux H, Avelange-Macherel M-H, Macherel D (2013) Experimental determination of organelle targeting-peptide cleavage sites using transient expression of green fluorescent protein translational fusions. Anal Biochem 434:44–51PubMedCrossRefGoogle Scholar
  15. Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451PubMedCrossRefGoogle Scholar
  16. Clauss MJ, Koch MA (2006) Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci 11:449–459PubMedCrossRefGoogle Scholar
  17. 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 101:15243–15248PubMedPubMedCentralCrossRefGoogle Scholar
  18. Dassanayake M, Oh D-H, Haas JS, Hernandez A, Hong H, Ali S, Yun D-J, Bressan RA, Zhu J-K, Bohnert HJ, Cheeseman JM (2011) The genome of the extremophile crucifer Thellungiella parvula. Nat Genet 43:913–918PubMedPubMedCentralCrossRefGoogle Scholar
  19. Daub CO, Kloska S, Selbig J (2003) MetaGeneAlyse: analysis of integrated transcriptional and metabolite data. Bioinformatics 19:2332–2333PubMedCrossRefGoogle Scholar
  20. Davey MP, Woodward IF, Quick PW (2009) Intraspecific variation in cold-temperature metabolic phenotypes of Arabidopsis lyrata ssp. petraea. Metabolomics 5:138–149CrossRefGoogle Scholar
  21. Du C, Hu K, Xian S, Liu C, Fan J, Tu J, Fu T (2016) Dynamic transcriptome analysis reveals AP2/ERF transcription factors responsible for cold stress in rapeseed (Brassica napus L.). Mol Gen Genomics 291:1053–1067CrossRefGoogle Scholar
  22. Dyson BC, Miller MAE, Feil R, Rattray N, Bowsher CG, Goodacre R, Lunn JE, Johnson GN (2016) FUM2, a cytosolic fumarase, is essential for acclimation to low temperature in Arabidopsis thaliana. Plant Physiol 172:118–127PubMedPubMedCentralCrossRefGoogle Scholar
  23. Gao M-J, Allard G, Byass L, Flannagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459–471PubMedCrossRefGoogle Scholar
  24. 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 230:1033–1046PubMedCrossRefGoogle Scholar
  25. Gehan MA, Park S, Gilmour SJ, An C, Lee C-M, Thomashow MF (2015) Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes. Plant J 84:682–693PubMedCrossRefGoogle Scholar
  26. Gery C, Zuther E, Schulz E, Legoupi J, Chauveau A, McKhann H, Hincha DK, Teoule E (2011) Natural variation in the freezing tolerance of Arabidopsis thaliana: effects of RNAi-induced CBF depletion and QTL localisation vary among accessions. Plant Sci 180:12–23PubMedCrossRefGoogle Scholar
  27. 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 124:1854–1865PubMedPubMedCentralCrossRefGoogle Scholar
  28. Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781PubMedCrossRefGoogle Scholar
  29. Guevara DR, Champigny MJ, Tattersall A, Dedrick J, Wong CE, Li Y, Labbe A, Ping C-L, Wang Y, Nuin P, Golding GB, McCarry BE, Summers PS, Moffat BA, Weretilnyk EA (2012) Transcriptomic and metabolomic analysis of Yukon Thellungiella plants grown in cabinets and their natural habitat show phenotypic plasticity. BMC Plant Biol 12:175PubMedPubMedCentralCrossRefGoogle Scholar
  30. Guy CL, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235PubMedGoogle Scholar
  31. Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1:e26PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112PubMedPubMedCentralCrossRefGoogle Scholar
  33. He F, Arce AL, Schmitz G, Koornneef M, Novikova P, Beyer A, de Meaux J (2016) The footprint of polygenic adaptation on stress-responsive cis-regulatory divergence in the Arabidopsis genus. Mol Biol Evol 33:2088–2101PubMedCrossRefGoogle Scholar
  34. Heo J-Y, Feng D, Niu X, Mitchell-Olds T, van Tienderen PH, Tomes D, Schranz ME (2014) Identification of quantitative trait loci and a candidate locus for freezing tolerance in controlled and outdoor environments in the overwintering crucifer Boechera stricta. Plant Cell Environ 37:2459–2469PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hincha DK (1994) Rapid induction of frost hardiness in spinach seedlings under salt stress. Planta 194:274–278CrossRefGoogle Scholar
  36. Hincha DK, Espinoza C, Zuther E (2012) Transcriptomic and metabolomic approaches to the analysis of plant freezing tolerance and cold acclimation. In: Tuteja N, Gill SS, Tiburcio AF, Tuteja R (eds) Improving crop resistance to abiotic stress, vol 1. Wiley-Blackwell, Berlin, pp 255–287CrossRefGoogle Scholar
  37. Horton MW, Willems G, Sasaki E, Koornneef M, Nordborg M (2016) The genetic architecture of freezing tolerance varies across the range of Arabidopsis thaliana. Plant Cell Environ 39:2570–2579PubMedCrossRefGoogle Scholar
  38. Hwang I, Manoharan RK, Kang J-G, Chung M-Y, Kim Y-W, Nou I-S (2016) Genome-wide identification and characterization of bZIP transcription factors in Brassica oleracea under cold stress. Biomed Res Int 2016:4376598PubMedPubMedCentralGoogle Scholar
  39. 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 127:910–917PubMedPubMedCentralCrossRefGoogle Scholar
  40. Jaglo-Ottosen K, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106PubMedCrossRefPubMedCentralGoogle Scholar
  41. Jung H-J, Dong X, Park J-I, Thamilarasan SK, Lee SS, Kim Y-K, Lim Y-P, Nou I-S, Hur Y (2014) Genome-wide transcriptome analysis of two contrasting Brassica rapa doubled haploid lines under cold-stresses using Br135K oligomeric chip. PLoS One 9:e106069PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168PubMedPubMedCentralCrossRefGoogle Scholar
  43. 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 50:967–981PubMedCrossRefPubMedCentralGoogle Scholar
  44. Kasianov AS, Klepikova AV, Kulakovskiy IV, Gerasimov ES, Fedotova AV, Besedina EG, Kondrashov AS, Logacheva MD, Penin AA (2017) High-quality genome assembly of Capsella bursa-pastoris reveals asymmetry of regulatory elements at early stages of polyploid genome evolution. Plant J 91:278–291PubMedCrossRefPubMedCentralGoogle Scholar
  45. 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 17:287–291PubMedCrossRefPubMedCentralGoogle Scholar
  46. Kazachkova Y, Batushansky A, Cisneros A, Tel-Zur N, Fait A, Barak S (2013) Growth platform-dependent and -independent phenotypic and metabolic responses of Arabidopsis and its halophilic relative, Eutrema salsugineum, to salt stress. Plant Physiol 162:1583–1598PubMedPubMedCentralCrossRefGoogle Scholar
  47. Khanal N, Moffat BA, Gray GR (2015) Acquisition of freezing tolerance in Arabidopsis and two contrasting ecotypes of the extremophile Eutrema salsugineum (Thellungiella salsuginea). J Plant Physiol 180:35–44PubMedCrossRefPubMedCentralGoogle Scholar
  48. Koch MA, German DA (2013) Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. Front Plant Sci 4:267PubMedPubMedCentralCrossRefGoogle Scholar
  49. Koch MA, Wernisch M, Schmickl R (2008) Arabidopsis thaliana’s wild relatives: an updated overview on systematics, taxonomy and evolution. Taxon 57:933–943Google Scholar
  50. Kole C, Thormann CE, Karlsson BH, Palta JP, Gaffney P, Yandell B, Osborn TC (2002) Comparative mapping of loci controlling winter survival and related traits in oilseed Brassica rapa and B. napus. Mol Breed 9:201–210CrossRefGoogle Scholar
  51. Korn M, Peterek S, Mock H-P, 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 31:813–827PubMedPubMedCentralCrossRefGoogle Scholar
  52. Korn M, Gärtner T, Erban A, Kopka J, Selbig J, Hincha DK (2010) Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant 3:224–235PubMedCrossRefPubMedCentralGoogle Scholar
  53. Lee S-C, Lim M-H, Yu J-G, Park B-S, Yang T-J (2012a) Genome-wide characterization of the CBF/DREB1 gene family in Brassica rapa. Plant Physiol Biochem 61:142–152PubMedCrossRefPubMedCentralGoogle Scholar
  54. Lee YP, Babakov A, de Boer B, Zuther E, Hincha DK (2012b) Comparison of freezing tolerance, compatible solutes and polyamines in geographically diverse collections of Thellungiella spec. and Arabidopsis thaliana accessions. BMC Plant Biol 12:131PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lee YP, Giorgi FM, Lohse M, Kvederaviciute K, Klages S, Usadel B, Meskiene I, Reinhardt R, Hincha DK (2013) Transcriptome sequencing and microarray design for functional genomics in the extremophile Arabidopsis relative Thellungiella salsuginea (Eutrema salsugineum). BMC Genomics 14:793PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lee YP, Funk C, Erban A, Kopka J, Köhl KI, Zuther E, Hincha DK (2016) Salt stress responses in a geographically diverse collection of Eutrema/Thellungiella spp. accessions. Funct Plant Biol 43:590–606CrossRefGoogle Scholar
  57. Levitt J (1980) Responses of plants to environmental stresses. Volume I: chilling, freezing, and high temperature stresses. Physiological ecology, 2nd edn. Academic, OrlandoGoogle Scholar
  58. Lin C, Thomashow MF (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide. Plant Physiol 99:519–525PubMedPubMedCentralCrossRefGoogle Scholar
  59. Liu T, Li Y, Duan W, Huang F, Hou X (2017) Cold acclimation alters DNA methylation patterns and confers tolerance to heat and increases growth rate in Brassica rapa. J Exp Bot 68:1213–1224PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lohse M, Nunes-Nesi A, Krüger P, Nagel A, Hannemann J, Giorgi FM, Childs L, Osorio S, Walther D, Selbig J, Sreenivasulu N, Stitt M, Fernie AR, Usadel B (2010) Robin: an intuitive wizard application for R-based expression microarray quality assessment and analysis. Plant Physiol 153:642–651PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lugan R, Niogret MF, Leport L, Guégan JP, Larher FR, Savouré A, Kopka J, Bouchereau A (2010) Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. Plant J 64:215–229PubMedCrossRefPubMedCentralGoogle Scholar
  62. Man L, Xiang D, Wang L, Zhang W, Wang X, Qi G (2017) Stress-responsive gene RsICE1 from Raphanus sativus increases cold tolerance in rice. Protoplasma 254:945–956PubMedCrossRefPubMedCentralGoogle Scholar
  63. Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano S, Fujita M, Yoshiwara K, Matsukura S, Morishita Y, Sasaki R, Suzuki H, Saito K, Shibata D, Shinozaki K, Yamaguchi-Shinozaki K (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150:1972–1980PubMedPubMedCentralCrossRefGoogle Scholar
  64. Meissner M, Orsini E, Ruschhaupt M, Melchinger AE, Hincha DK, Heyer AG (2013) Mapping quantitative trait loci for freezing tolerance in a recombinant inbred line population of Arabidopsis thaliana accessions Tenela and C24 reveals REVEILLE1 as negative regulator of cold acclimation. Plant Cell Environ 36:1256–1267PubMedCrossRefPubMedCentralGoogle Scholar
  65. Mitchell-Olds T (2001) Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution. Trends Ecol Evol 16:693–700CrossRefGoogle Scholar
  66. Nakayama K, Okawa K, Kakizaki T, Honma T, Itoh H, Inaba T (2007) Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers. Plant Physiol 144:513–523PubMedPubMedCentralCrossRefGoogle Scholar
  67. Oakley CG, Ågren J, Atchison RA, Schemske DW (2014) QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs. Mol Ecol 23(1):4304–4315PubMedCrossRefPubMedCentralGoogle Scholar
  68. Ometto L, Li M, Bresadola L, Varotto C (2012) Rates of evolution in stress-related genes are associated with habitat preference in two Cardamine lineages. BMC Evol Biol 12:7PubMedPubMedCentralCrossRefGoogle Scholar
  69. Ometto L, Li M, Bresadola L, Barbaro E, Neteler M, Varotto C (2015) Demographic history, population structure, and local adaptation in alpine populations of Cardamine impatiens and Cardamine resedifolia. PLoS One 10:e0125199PubMedPubMedCentralCrossRefGoogle Scholar
  70. Pearce RS, Willison JHM (1985) Wheat tissues freeze-etched during exposure to extracellular freezing: distribution of ice. Planta 163:295–303PubMedCrossRefPubMedCentralGoogle Scholar
  71. Preston JC, Sanve SR (2013) Adaptation to seasonality and the winter freeze. Front Plant Sci 4:167PubMedPubMedCentralGoogle Scholar
  72. Saha G, Park J-I, Jung H-J, Ahmed NU, Kayum MA, Kang J-G, Nou I-S (2015) Molecular characterization of BZR transcription factor family and abiotic stress induced expression profiling in Brassica rapa. Plant Physiol Biochem 92:92–104PubMedCrossRefPubMedCentralGoogle Scholar
  73. Schmidt JE, Schmitt JM, Kaiser WM, Hincha DK (1986) Salt treatment induces frost hardiness in leaves and isolated thylakoids from spinach. Planta 168:50–55PubMedCrossRefPubMedCentralGoogle Scholar
  74. Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK (2015) Natural variation in flavonol and anthocyanin metabolism during cold acclimation in Arabidopsis thaliana accessions. Plant Cell Environ 38:1658–1672PubMedCrossRefPubMedCentralGoogle Scholar
  75. Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK (2016) Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana. Sci Rep 6:34027PubMedPubMedCentralCrossRefGoogle Scholar
  76. Shamustakimova AO, Leonova TG, Taranov VV, de Boer AH, Babakov AV (2017) Cold stress increases salt tolerance of the extremophytes Eutrema salsugineum (Thellungiella salsuginea) and Eutrema (Thellungiella) botschantzevii. J Plant Physiol 208:128–138PubMedCrossRefGoogle Scholar
  77. Sharma N, Cram D, Huebert T, Zhou N, Parkin IAP (2007) Exploiting the wild crucifer Thlaspi arvense to identify conserved and novel genes expressed during a plant’s response to cold stress. Plant Mol Biol 63:171–184PubMedCrossRefGoogle Scholar
  78. Shi Y, Ding Y, Yang S (2015) Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol 56:7–15PubMedCrossRefPubMedCentralGoogle Scholar
  79. Sinha S, Raxwal VK, Joshi B, Jagannath A, Katiyar-Agarwal S, Goel S, Kumar A, Agarwal M (2015) De novo transcriptome profiling of cold-stressed siliques during pod filling stages in Indian mustard (Brassica juncea L.). Front Plant Sci 6:932PubMedPubMedCentralGoogle Scholar
  80. Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584CrossRefGoogle Scholar
  81. Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Natl Acad Sci U S A 95:14570–14575PubMedPubMedCentralCrossRefGoogle Scholar
  82. Teutonico RA, Yandell B, Satagopan JM, Ferreira ME, Palta JP, Osborn TC (1995) Genetic analysis and mapping of genes controlling freezing tolerance in oilseed Brassica. Mol Breed 1:329–339CrossRefGoogle Scholar
  83. Thalhammer A, Hundertmark M, Popova AV, Seckler R, Hincha DK (2010) Interaction of two intrinsically disordered plant stress proteins (COR15A and COR15B) with lipid membranes in the dry state. Biochim Biophys Acta 1798:1812–1820PubMedCrossRefGoogle Scholar
  84. Thalhammer A, Bryant G, Sulpice R, Hincha DK (2014a) Disordered cold Regulated15 proteins protect chloroplast membranes during freezing through binding and folding, but do not stabilize chloroplast enzymes in vivo. Plant Physiol 166:190–201PubMedPubMedCentralCrossRefGoogle Scholar
  85. Thalhammer A, Hincha DK, Zuther E (2014b) Measuring freezing tolerance: electrolyte leakage and chlorophyll fluorescence assays. In: Hincha DK, Zuther E (eds) Methods in molecular biology, vol 1166. Springer, New York, pp 15–24Google Scholar
  86. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939PubMedCrossRefGoogle Scholar
  87. Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577PubMedPubMedCentralCrossRefGoogle Scholar
  88. Wang X-J, Shi D-C, Wang X-Y, Wang J, Sun Y-S, Liu J-Q (2015) Evolutionary migration of the disjunct salt cress Eutrema salsugineum (= Thellungiella salsuginea, Brassicaceae) between Asia and North America. PLoS One 10:e0124010PubMedPubMedCentralCrossRefGoogle Scholar
  89. Wang X, Bi C, Xu Y, Wei S, Dai X, Yin T, Ye N (2016) The whole genome assembly and comparative genomic research of Thellungiella parvula (extremophile crucifer) mitochondrion. Int J Genomics 2016:5283628PubMedPubMedCentralGoogle Scholar
  90. Wang J, Zhang Q, Cui F, Hou L, Zhao S, Xia H, Qiu J, Li T, Zhang Y, Wang X, Zhao C (2017) Genome-wide analysis of gene expression provides new insights into cold responses in Thellungiella salsuginea. Front Plant Sci 8:713PubMedPubMedCentralCrossRefGoogle Scholar
  91. Warwick SI, Francis A, Susko DJ (2002) The biology of Canadian weeds. 9. Thlaspi arvense L. (updated). Can J Plant Sci 82:803–823CrossRefGoogle Scholar
  92. Wilhelm KS, Thomashow MF (1993) Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought. Plant Mol Biol 23:1073–1077PubMedCrossRefGoogle Scholar
  93. Wingler A, Juvany M, Cuthbert C, Munné-Bosch S (2015) Adaptation to altitude affects the senescence response to chilling in the perennial plant Arabis alpina. J Exp Bot 66:355–367PubMedCrossRefGoogle Scholar
  94. Wong CE, Li Y, Whitty BR, Díaz-Camino C, Akhter SR, Brandle JE, Golding GB, Weretilnyk EA, Moffatt BA, Griffith M (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol Biol 58:561–574PubMedCrossRefGoogle Scholar
  95. Wong CE, Li Y, Labbe A, Guevara D, Nuin P, Whitty B, Diaz C, Golding GB, Gray GR, Weretilnyk EA, Griffith M, Moffatt BA (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140:1437–1450PubMedPubMedCentralCrossRefGoogle Scholar
  96. Wos G, Willi Y (2015) Temperature-stress resistance and tolerance along a latitudinal cline in North American Arabidopsis lyrata. PLoS One 10:e0131808PubMedPubMedCentralCrossRefGoogle Scholar
  97. Wu H-J, Zhang Z, Wang J-Y, Oh D-H, Dassanayake M, Liu B, Huang Q, Sun H-X, Xia R, Wu Y, Wang Y-N, Yang Z, Liu Y, Zhang W, Zhang H, Chu J, Yan C, Fang S, Zhang J, Wang Y, Zhang F, Wang G, Lee SY, Cheeseman JM, Yang B, Li B, Min J, Yang L, Wang J, Chu C, Chen S-Y, Bohnert HJ, Zhu J-K, Xie Q (2012a) Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci U S A 109:12219–12224PubMedPubMedCentralCrossRefGoogle Scholar
  98. Wu L, Zhou M, Shen C, Liang J, Lin J (2012b) Transgenic tobacco plants over expressing cold regulated protein CbCOR15b from Capsella bursa-pastoris exhibit enhanced cold tolerance. J Plant Physiol 169:1408–1416PubMedCrossRefGoogle Scholar
  99. Yang R, Jarvis DJ, Chen H, Beilstein M, Grimwood J, Jenkins J, Shu SQ, Prochnik S, Xin M, Ma C, Schmutz J, Wing RA, Mitchell-Olds T, Schumaker K, Wang X (2013) The reference genome of the halophytic plant Eutrema salsugineum. Front Plant Sci 4:46PubMedPubMedCentralGoogle Scholar
  100. Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu J-K (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol 171:2744–2759PubMedPubMedCentralGoogle Scholar
  101. Zhen Y, Ungerer MC (2008a) Clinical variation in freezing tolerance among natural accessions of Arabidopsis thaliana. New Phytol 177:419–427PubMedGoogle Scholar
  102. Zhen Y, Ungerer MC (2008b) Relaxed selection on the CBF/DREB1 regulatory genes and reduced freezing tolerance in the Southern range of Arabidopsis thaliana. Mol Biol Evol 25:2547–2555PubMedCrossRefGoogle Scholar
  103. Zhou N, Robinson SJ, Huebert T, Bate NJ, Parkin IAP (2007) Comparative genome organization reveals a single copy of CBF in the freezing tolerant crucifer Thlaspi arvense. Plant Mol Biol 65:693–705PubMedCrossRefGoogle Scholar
  104. Zhou M, Xu M, Wu L, Shen C, Ma H, Lin J (2014) CbCBF from Capsella bursa-pastoris enhances cold tolerance and restrains growth in Nicotiana tabacum by antagonizing with gibberellin and affecting cell cycle signaling. Plant Mol Biol 85:259–275PubMedCrossRefGoogle Scholar
  105. Zhou M, Li W, Zheng Y, Lin P, Yao X, Lin J (2016) CbRCI35, a cold responsive peroxidase from Capsella bursa-pastoris regulates reactive oxygen species homeostasis and enhances cold tolerance in tobacco. Front Plant Sci 7:1599PubMedPubMedCentralGoogle Scholar
  106. Zuther E, Schulz E, Childs LH, Hincha DK (2012) Clinical variation in the nonacclimated and cold acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant Cell Environ 35:1860–1878PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Ellen Zuther
    • 1
  • Yang Ping Lee
    • 1
    • 2
  • Alexander Erban
    • 1
  • Joachim Kopka
    • 1
  • Dirk K. Hincha
    • 1
    Email author
  1. 1.Max-Planck-Institut für Molekulare PflanzenphysiologiePotsdamGermany
  2. 2.FELDA Global Ventures Research and DevelopmentKuala LumpurMalaysia

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