The CBFs: Three arabidopsis transcription factors to cold acclimate

Plant Science

Volumn 180, Issue 1, 2011, Pages 3-11

  Medina, Joaquín ^b   Catalá, Rafael ^a   Salinas, Julio ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b ETSI MontesTechnical University of Madrid   (Spain)

Author keywords

Abiotic stress; Arabidopsis; CBF DREB1; Cold acclimation; Freezing tolerance; Transcriptional regulation

Indexed keywords

ARABIDOPSIS PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BIOLOGICAL MODEL; COLD; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ARABIDOPSIS PROTEINS; COLD TEMPERATURE; GENE EXPRESSION REGULATION, PLANT; MODELS, BIOLOGICAL; TRANSCRIPTION FACTORS;

ARABIDOPSIS;

EID: 78149499913     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2010.06.019     Document Type: Article

References (112)

1. Levitt J. Responses of Plants to Environmental Stresses: Chilling, Freezing and High Temperatures Stresses 1980, Academic press, New York. second ed.
2. Thomashow M.F. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50:571-599.
3. Salinas J. Molecular mechanisms of signal transduction in cold acclimation. Plant Signal Transduction 2002, 116-134. Oxford University press, Oxford. D. Scheel, C. Westernack (Eds.).
4. Kaplan F., Kopka J., Haskell D.W., Zhao W., Schiller K.C., Gatzke N., Sung D.Y., Guy C.L. Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 2004, 136:4159-4168.
5. Nishida I., Murata N. Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47:541-568.
6. Mita T., Shibaoka H. Gibberellin stabilizes microtubules in onion leaf sheath cells. Proteoplasma 1984, 119:100-109.
7. Schoner S., Krause G.H. Protective systems against active oxygen species in spinach: responses to cold acclimation in excess light. Planta 1990, 180:383-389.
8. Christie P.J., Alfenito M.R., Walbot W. Impact of low-temperature stress on general phenylpropanoid and anthocyanin pathways: enhancement of transcript abundance and anthocyanin pigmentation in maize seedlings. Planta 1994, 194:541-549.
9. Król M., Ivanov A.G., Jansson S., Kloppstech K., Huner N.P.A. Greening under high light or cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the Chlorina f2 mutant. Plant Physiol. 1999, 120:193-203.
10. Prasad T.K. Role of catalase in inducing chilling tolerance in pre-emergent maize seedlings. Plant Physiol. 1997, 114:1369-1376.
11. Llorente F., Lopez-Cobollo R.M., Catalá R., Martinez-Zapater J.M., Salinas J. A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance. Plant J. 2002, 32:13-24.
12. Ristic Z., Ashworth E.N. Ultrastructural evidence that intracellular ice formation and possibly cavitation are the sources of freezing injury in supercooling wood tissue of Cornus florida L. Plant Physiol. 1993, 103:753-761.
13. Sauter J.J., Wisniewski M., Witt W. Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus × canaiensis Moench "robusta") wood. J. Plant Physiol. 1996, 149:451-461.
14. Xin Z., Browse J. Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl. Acad. Sci. USA 1998, 95:7799-7804.
15. Wanner L.A., Junttila O. Cold-induced freezing tolerance in Arabidopsis. Plant Physiol. 1999, 120:391-400.
16. Gilmour S.J., Sebolt A.M., Salazar M.P., Everard J.D., Thomashow M.F. Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 2000, 124:1854-1865.
17. Garg A.K., Kim J.K., Owens T.G., Ranwala A.P., Choi Y.D., Kochian L.V., Wu R.J. Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc. Natl. Acad. Sci. USA 2002, 99:15898-15903.
18. Smallwood M., Bowles D.J. Plants in a cold climate. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2002, 357:831-847.
19. Matsui A., Ishida J., Morosawa T., Mochizuki Y., Kaminuma E., Endo T.A., Okamoto M., Nambara E., Nakajima M., Kawashima M., Satou M., Kim J.M., Kobayashi N., Toyoda T., Shinozaki K., Seki M. Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol. 2008, 49:1135-1149.
20. Zeller G., Henz S.R., Widmer C.K., Sachsenberg T., Rätsch G., Weigel D., Laubinger S. Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J. 2009, 58:1068-1082.
21. Lee B.H., Henderson D.A., Zhu J.K. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 2005, 17:3155-3175.
22. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 1998, 10:1391-1406.
23. Gilmour S.J., Zarka D.G., Stockinger E.J., Salazar M.P., Houghton J.M., Thomashow M.F. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 1998, 16:433-442.
24. Medina J., Bargues M., Terol J., Perez-Alonso M., Salinas J. 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. 1999, 119:463-470.
25. Jaglo-Ottosen K.R., Gilmour S.J., Zarka D.G., Schabenberger O., Thomashow M.F. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 1998, 280:104-106.
26. Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 1999, 17:287-291.
27. Fowler S., Thomashow M.F. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 2002, 14:1675-1690.
28. Gilmour S.J., Fowler S.G., Thomashow M.F. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol. Biol. 2004, 54:767-781.
29. Yamaguchi-Shinozaki K., Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 2006, 57:781-803.
30. Van Buskirk H.A., Thomashow M.F. Arabidopsis transcription factors regulating cold acclimation. Physiol. Plant. 2006, 126:72-80.
31. Zhu J., Dong C.H., Zhu J.K. Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr. Opin. Plant Biol. 2007, 10:290-295.
32. Catala R., Salinas J. Regulatory mechanisms involved in cold acclimation response. Span. J. Agric. Res. 2008, 6:211-220.
33. Mazzucotelli E., Mastrangelo A.M., Crosatti C., Guerra D., Stanca A.M., Cattivelli L. Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci. 2008, 174:420-431.
34. Penfield S. Temperature perception and signal transduction in plants. New Phytol. 2008, 179:615-628.
35. Ruelland E., Vaultier M.-N., Zachowski A., Hurry V. Cold signalling and cold acclimation in Plants. Adv. Bot. Res. 2009, 49:35-150.
36. Yamaguchi-Shinozaki K., Shinozaki K. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 1994, 6:251-264.
37. Baker S.S., Wilhelm K.S., Thomashow M.F. The 5'-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol. Biol. 1994, 24:701-713.
38. Jiang C., Iu B., Singh J. Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant Mol. Biol. 1996, 30:679-684.
39. Ouellet F., Vazquez-Tello A., Sarhan F. The wheat wcs120 promoter is cold-inducible in both monocotyledonous and dicotyledonous species. FEBS Lett. 1998, 423:324-328.
40. Knight H., Zarka D.G., Okamoto H., Thomashow M.F., Knight M.R. Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol. 2004, 135:1710-1717.
41. Stockinger E.J., Gilmour S.J., Thomashow M.F. Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. USA 1997, 94:1035-1040.
42. Raikhel N. Nuclear targeting in plants. Plant Physiol. 1992, 100:1627-1632.
43. Wang Z., Triezenberg S.J., Thomashow M.F., Stockinger E.J. Multiple hydrophobic motifs in Arabidopsis CBF1 COOH-terminus provide functional redundancy in trans-activation. Plant Mol. Biol. 2005, 58:543-559.
44. Ohme-Takagi M., Shinshi H. Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 1995, 7:173-182.
45. Okamuro J.K., Caster B., Villarroel R., Van Montagu M., Jofuku K.D. The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc. Natl. Acad. Sci. USA 1997, 94:7076-7081.
46. Riechmann J.L., Meyerowitz E.M. The AP2/EREBP family of plant transcription factors. Biol. Chem. 1998, 379:633-646.
47. Sakuma Y., Liu Q., Dubouzet J.G., Abe H., Shinozaki K., Yamaguchi-Shinozaki K. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem. Biophys. Res. Commun. 2002, 29:998-1009.
48. Jaglo K.R., Kleff S., Amundsen K.L., Zhang X., Haake V., Zhang J.Z., Deits T., Thomashow M.F. 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. 2001, 127:910-917.
49. Canella D., Gilmour S.J., Kuhn L.A., Thomashow M.F. DNA binding by the Arabidopsis CBF1 transcription factor requires the PKKP/RAGRxKFxETRHP signature sequence. Biochim. Biophys. Acta. 2010, doi:10.1016/j.bbagrm.2009.11.017.
50. Allen M.D., Yamasaki K., Ohme-Takagi M., Tateno M., Suzuki M. A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J. 1998, 17:5484-5496.
51. Novillo F., Alonso J.M., Ecker J.R., Salinas J. CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. USA 2004, 101:3985-3990.
52. Novillo F., Medina J., Salinas J. Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc. Natl. Acad. Sci. USA 2007, 104:21002-21007.
53. Zarka D.G., Vogel J.T., Cook D., Thomashow M.F. 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. 2003, 133:910-918.
54. Franklin K.A., Whitelam G.C. Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat. Genet. 2007, 39:1410-1413.
55. Harmer S.L., Hogenesch J.B., Straume M., Chang H.S., Han B., Zhu T., Wang X., Kreps J.A., Kay S.A. Orchestrated transcription of key pathways in Arabidosis by the circadian clock. Science 2000, 290:2110-2113.
56. Beniaswka Z., Spinoza C., Schlereth A., Sulpice R., Hincha D.K., Hannah M.A. Disruption of Arabidopsis circadian clock is responsible for extensive variation in cold-responsive transcriptome. Plant Physiol. 2008, 147:263-279.
57. Fowler S.G., Cook D., Thomashow M.F. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 2005, 137:961-968.
58. Haake V., Cook D., Riechmann J.L., Pineda O., Thomashow M.F., Zhang J.Z. Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol. 2002, 130:639-648.
59. Magome H., Yamaguchi S., Hanada A., Kamiya Y., Oda K. dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J. 2004, 37:720-729.
60. Cook D., Fowler S., Fiehn O., Thomashow M.F. A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc. Natl. Acad. Sci. USA 2004, 101:15243-15248.
61. Sharabi-Schwager M., Lers A., Samach A., Guy C.L., Porat R. Overexpression of the CBF2 transcriptional activator in Arabidopsis delays leaf senescence and extends plant longevity. J. Exp. Bot. 2010, 61:261-273.
62. Lers A. Environmental regulation of leaf senescence. Senescence Processes in Plants 2007, 109-144. Blackwell, Oxford. S. Gan (Ed.).
63. Vogel J.T., Zarka D.G., Van Buskirk H.A., Fowler S.G., Thomashow M.F. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 2005, 41:195-211.
64. Maruyama K., Sakuma Y., Kasuga M., Ito Y., Seki M., Goda H., Shimada Y., Yoshida S., Shinozaki K., Yamaguchi-Shinozaki K. Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J. 2004, 38:982-993.
65. Alonso-Blanco C., Gomez-Mena C., Llorente F., Koornneef M., Salinas J., Martínez-Zapater J.M. 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. 2005, 139:1304-1312.
66. Doherty C.J., Van Buskirk H.A., Myers S.J., Thomashow M.F. Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 2009, 21:972-984.
67. Chinnusamy V., Ohta M., Kanrar S., Lee B.H., Hong X., Agarwal M., Zhu J.K. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 2003, 15:1043-1054.
68. Fursova O.V., Pogorelko G.V., Tarasov V.A. Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 2009, 429:98-103.
69. Agarwal M., Hao Y., Kapoor A., Dong C.H., Fujii H., Zheng X., Zhu J.K. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J. Biol. Chem. 2006, 281:37636-37645.
70. Kidokoro S., Maruyama K., Nakashima K., Imura Y., Narusaka Y., Shinwari Z.K., Osakabe Y., Fujita Y., Mizoi J., Shinozaki K., Yamaguchi-Shinozaki K. The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol. 2009, 151:2046-2057.
71. Dong C.H., Hu X., Tang W., Zheng X., Kim Y.S., Lee B.H., Zhu J.K. A putative Arabidopsis nucleoporin, AtNUP160, is critical for RNA export and required for plant tolerance to cold stress. Mol. Cell Biol. 2006, 26:9533-9543.
72. Gong Z., Dong C.H., Lee H., Zhu J., Xiong L., Gong D., Stevenson B., Zhu J.K. A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 2005, 17:256-267.
73. Guo Y., Xiong L., Ishitani M., Zhu J.K. An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc. Natl. Acad. Sci. USA 2002, 99:7786-7791.
74. Ishitani M., Xiong L., Lee H., Stevenson B., Zhu J.K. HOS1, a genetic locus involved in cold-responsive gene expression in Arabidopsis. Plant Cell 1998, 10:1151-1161.
75. Dong C.H., Agarwal M., Zhang Y., Xie Q., Zhu J.K. The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc. Natl. Acad. Sci. USA 2006, 103:8281-8286.
76. Miura K., Jin J.B., Lee J., Yoo C.Y., Stirm V., Miura T., Ashworth E.N., Bressan R.A., Yun D.J., Hasegawa P.M. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 2007, 19:1403-1414.
77. Kim H.J., Hyun Y., Park J.Y., Park M.J., Park M.K., Kim M.D., Kim H.J., Lee M.H., Moon J., Lee I., Kim J. A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet. 2004, 36:167-171.
78. Achard P., Gong F., Cheminant S., Alioua M., Hedden P., Genschik P. The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 2008, 20:2117-2129.
79. Berberich T., Sano H., Kusano T. Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol. Gen. Genet. 1999, 262:534-542.
80. Masclaux-Daubresse C., Purdy S., Lemaitre T., Pourtau N., Taconnat L., Renou J.P., Wingler A. Genetic variation suggests interaction between cold acclimation and metabolic regulation of leaf senescence. Plant Physiol. 2007, 143:434-446.
81. Wingler A., Roitsch T. Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Plant Biol. 2008, 10:50-62.
82. Sharabi-Schwager M., Samach A., Porat R. Overexpression of the CBF2 transcriptional activator in Arabidopsis suppresses the responsiveness of leaf tissue to the stress hormone ethylene. Plant Biol. 2010, doi:10.1111/j.1438-8677.2009.00255.x.
83. Kitashiba H., Ishizaka T., Isuzugawa K., Nishimura K., Suzuki T. Expression of a sweet cherry DREB1/CBF ortholog in Arabidopsis confers salt and freezing tolerance. J. Plant Physiol. 2004, 161:1171-1176.
84. Zhang X., Fowler S.G., Cheng H., Lou Y., Rhee S.Y., Stockinger E.J., Thomashow M.F. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J. 2004, 39:905-919.
85. Pennycooke J.C., Cheng H., Roberts S.M., Yang Q., Rhee S.Y., Stockinger E.J. 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. 2008, 67:483-497.
86. Pennycooke J.C., Cheng H., Stockinger E.J. Comparative genomic sequence and expression analyses of Medicago truncatula and alfalfa subspecies falcata COLD-ACCLIMATION-SPECIFIC genes. Plant Physiol. 2008, 146:1242-1254.
87. Benedict C., Skinner J.S., Meng R., Chang Y., Bhalerao R., Huner N.P., Finn C.E., Chen T.H., Hurry V. The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ. 2006, 29:1259-1272.
88. Welling A., Palva E.T. Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol. 2008, 147:1199-1211.
89. Huang A., Jin L., Liu J. Molecular cloning and functional characterization of a DREB1/CBF-like gene (GhDREB1L) from cotton. Sci. China C. Life Sci. 2007, 50:7-14.
90. Xue G.P. 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. 2003, 33:373-383.
91. Dubouzet J.G., Sakuma Y., Ito Y., Kasuga M., Dubouzet E.G., Miura S., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J. 2003, 33:751-763.
92. Qin F., Sakuma Y., Li J., Liu Q., Li Y.Q., Shinozaki K., Yamaguchi-Shinozaki K. Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol. 2004, 45:1042-1052.
93. Bräutigam M., Lindlöf A., Zakhrabekova S., Gharti-Chhetri G., Olsson B., Olsson O. Generation and analysis of 9792 EST sequences from cold acclimated oat, Avena sativa. BMC Plant Biol. 2005, 5:18.
94. Skinner J.S., von Zitzewitz J., Szucs P., Marquez-Cedillo L., Filichkin T., Amundsen K., Stockinger E.J., Thomashow M.F., Chen T.H., Hayes P.M. Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol. Biol. 2005, 59:533-551.
95. Vágújfalvi A., Aprile A., Miller A., Dubcovsky J., Delugu G., Galiba G., Cattivelli L. The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat. Mol. Genet. Genomics 2005, 274:506-514.
96. Xiong Y., Fei S.Z. Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.). Planta 2006, 224:878-888.
97. James V.A., Neibaur I., Altpeter F. Stress inducible expression of the DREB1A transcription factor from xeric, Hordeum spontaneum L. in turf and forage grass (Paspalum notatum Flugge) enhances abiotic stress tolerance. Transgenic Res. 2008, 17:93-104.
98. Zhao H., Bughrara S.S. Isolation and characterization of cold-regulated transcriptional activator LpCBF3 gene from perennial ryegrass (Lolium perenne L.). Mol. Genet. Genomics 2008, 279:585-594.
99. Pellegrineschi A., Reynolds M., Pacheco M., Brito R.M., Almeraya R., Yamaguchi-Shinozaki K., Hoisington D. Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 2004, 47:493-500.
100. Lee S.C., Huh K.W., An K., An G., Kim S.R. Ectopic expression of cold-inducible transcription factor, CBF1/DREB1b, in transgenic rice (Oryza sativa L.). Mol. Cells 2004, 18:107-114.
101. Oh S.J., Song S.I., Kim Y.S., Jang H.J., Kim S.Y., Kim M., Kim Y.K., Nahm B.H., Kim J.K. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol. 2005, 138:341-351.
102. Ito Y., Katsura K., Maruyama K., Taji T., Kobayashi M., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol. 2006, 47:141-153.
103. Zhao J., Ren W., Zhi D., Wang L., Xia G. Arabidopsis DREB1A/CBF3 bestowed transgenic tall fescue increased tolerance to drought stress. Plant Cell Rep. 2007, 26:1521-1528.
104. Sutka J., Snape J.W. Location of a gene for frost resistance on chromosome 5A of wheat. Euphytica 1989, 42:41-44.
105. Roberts D.W.A. Identification of loci on chromosome 5A of wheat involved in control of cold hardiness, vernalization, leaf length, rosette growth habit, and height of hardened plants. Genome 1990, 33:247-259.
106. Galiba G., Quarrie S.A., Sutka J., Morounov A., Snape J.W. RFLP mapping of the vernalization (Vrn1) and frost resistance (Fr1) genes on chromosome 5A of wheat. Theor. Appl. Genet. 1995, 90:1174-1179.
107. Vágújfalvi A., Galiba G., Cattivelli L., Dubcovsky J. The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol. Genet. Genomics 2003, 269:60-67.
108. Francia E., Rizza F., Cattivelli L., Stanca A.M., Galiba G., Toth B., Hayes P.M., Skinner J.S., Pecchioni N. Two loci on chromosome 5H determine low-temperature tolerance in a 'Nure' (winter) X 'Tremois' (spring) barley map. Theor. Appl. Genet. 2004, 108:670-680.
109. Francia E., Barabaschi D., Tondelli A., Laidò G., Rizza F., Stanca A.M., Busconi M., Fogher C., Stockinger E.J., Pecchioni N. Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor. Appl. Genet. 2007, 115:1083-1091.
110. Stockinger E.J., Skinner J.S., Gardner K.G., Francia E., Pecchioni N. Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J. 2007, 51:308-321.
111. Knox A.K., Li C., Vágújfalvi A., Galiba G., Stockinger E.J., Dubcovsky J. Identification of candidate CBF genes for the frost tolerance locus Fr-Am2 in Triticum monococcum. Plant Mol. Biol. 2008, 67:257-270.
112. Fricano A., Rizza F., Faccioli P., Pagani D., Pavan P., Stella A., Rossini L., Piffanelli P., Cattivelli L. Genetic variants of HvCbf14 are statistically associated with frost tolerance in a European germplasm collection of Hordeum vulgare. Theor. Appl. Genet. 2009, 119:1335-1348.