Vitis CBF1 and Vitis CBF4 differ in their effect on Arabidopsis abiotic stress tolerance, development and gene expression

Plant, Cell and Environment

Volumn 34, Issue 8, 2011, Pages 1345-1359

  Siddiqua, Mahbuba ^a   Nassuth, Annette ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

CBF pathway; COR; Drought stress; Freezing stress; ICE1; Plant development

Indexed keywords

ARABIDOPSIS PROTEIN; ATGA2OX7 PROTEIN, ARABIDOPSIS; COR47 PROTEIN, ARABIDOPSIS; COR6.6 PROTEIN, ARABIDOPSIS; ELECTROLYTE; FLF PROTEIN, ARABIDOPSIS; ICE1 PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN; MIXED FUNCTION OXIDASE; RD29A PROTEIN, ARABIDOPSIS; RGL3 PROTEIN, ARABIDOPSIS; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

BIOLOGICAL DEVELOPMENT; CHEMICAL BINDING; DEHYDRATION; DICOTYLEDON; DROUGHT RESISTANCE; DROUGHT STRESS; ELECTROLYTE; FLOWERING; FREEZE TOLERANCE; GENE EXPRESSION; MORPHOLOGY; STOMATA; TEMPERATE ENVIRONMENT; VINE;

ARABIDOPSIS; ARTICLE; COLD SHOCK RESPONSE; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT STOMA; REGULON; TRANSGENIC PLANT; VITIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; COLD-SHOCK RESPONSE; DROUGHTS; ELECTROLYTES; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; MIXED FUNCTION OXYGENASES; PLANT PROTEINS; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; REGULON; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VITIS;

ARABIDOPSIS; VITACEAE; VITIS;

EID: 79960244339     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2011.02334.x     Document Type: Article

References (63)

1. Achard P. & Genschik P. (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. Journal of Experimental Botany 60, 1085-1092.
2. Achard P., Gong F., Cheminant S., Alioua M., Hedden P. & Genschik P. (2008) 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 20, 2117-2129.
3. Alonso-Blanco C., Gomez-Mena C., Llorente F., Koornneef M., Salinas J. & Martinez-Zapater J.M. (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 Physiology 139, 1304-1312.
4. Benedict C., Skinner J.S., Meng R., Chang Y., Bhalerao R., Huner N.P.A., Finn C.E., Chen T.H.H. & Hurry V. (2006) The CBF1-dependent low temperature signaling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant, Cell & Environment 29, 1259-1272.
5. Chinnusamy V., Ohta M., Kanrar S., Lee B., Hong X., Agarwal M. & Zhu J.-K. (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Development 17, 1043-1054.
6. Clough S.J. & Bent A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16, 735-743.
7. Des Marais D.L. & Juenger T.E. (2010) Pleiotropy, plasticity, and the evolution of plant abiotic stress tolerance. Annals of the New York Academy of Sciences 1206, 56-79.
8. Gao M.-J., Allard G., Byass L., Flanagan A.M. & Singh J. (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Molecular Biology 49, 459-471.
9. Gilmour S.J., Zarka D.G., Stockinger E.J., Salazar M.P., Houghton J.M. & Thomashow M.F. (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant Journal 16, 433-442.
10. Gilmour S.J., Fowler S.G. & Thomashow M.F. (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Molecular Biology 54, 767-781.
11. Haake V., Cook D., Riechmann J.L., Pineda O., Thomashow M.F. & Zhang J.Z. (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiology 130, 639-648.
12. Hannah M.A., Wiese D., Freund S., Fiehn S., Heyer A.G. & Hincha D.K. (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiology 142, 98-112.
13. Hedden P. & Phillips A.L. (2000) Gibberellin metabolism: new insights revealed by the genes. Trends in Plant Sciences 5, 523-530.
14. Hong J.-P. & Kim W.T. (2005) Isolation and functional characterization of the Ca-DREBLP1 gene encoding a dehydration-responsive element binding-factor-like protein 1 in hot pepper (Capsicum annuum L. cv. Pukang). Planta 220, 875-888.
15. Hsieh T.H., Lee J., Charng Y. & Chan M.T. (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiology 130, 618-626.
16. Huang B., Jin L. & Liu J. (2007) Molecular cloning and functional characterization of a DREB1/CBF-like gene (GhDREB1L) from cotton. Science in China, Series C: Life Sciences 50, 7-14.
17. Huang J.-G., Yang M., Yang G.-D., Wu C. & Zheng C.-C. (2009) GhDREB1 enhances abiotic stress tolerance, delays GA-mediated development and represses cytokinin signalling in transgenic Arabidopsis. Plant, Cell & Environment 32, 1132-1145.
18. Huttunen P., Kärkkäinen K., Løe G., Rautio P. & Ågren J. (2010) Leaf trichome production and responses to defoliation and drought in Arabidopsis lyrata (Brassicaceae). Annales Botanici Fennici 47, 199-207.
19. Jaglo-Ottosen K.R., Gilmour S.J., Zarka D.G., Schabenberger O. & Thomashow M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280, 104-106.
20. Kanaoka M.M., Pillitteri L.J., Fujii H., Yoshida Y., Bogenschutz N.L., Takabayashi J., Zhu J.-K. & Torii K.U. (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20, 1775-1785.
21. 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. Nature Biotechnology 17, 287-291.
22. Kasuga M., Setsuko M., 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 Physiology 45, 346-350.
23. Kim J.S., Jung H.J., Lee H.J., Kim K.A., Goh C.-H., Woo Y., Oh S.H., Han Y.S. & Kang H. (2008) Glycine-rich RNAbinding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant Journal 55, 455-466.
24. 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. Journal of Plant Physiology 161, 1171-1176.
25. Li R.H., Guo P.G., Michael B., Stefania G. & Salvatore C. (2006) Evaluation of chlorophyll content and fluorescence parameters as indicators of drought tolerance in barley. Agricultural Sciences in China 5, 751-757.
26. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K. & Shinozaki K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391-1406.
27. Liu X., Wang Z., Wang L., Wu R., Phillips J. & Deng X. (2009) LEA 4 group genes from the resurrection plant Boea hygrometrica confer dehydration tolerance in transgenic tobacco. Plant Science 176, 90-98.
28. McKersie B.D., Bowley S.R., Harjanto E. & Leprince O. (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiology 111, 1177-1181.
29. Magome H., Yamaguchi S., Hanada A., Kamiya Y. & Oda K. (2004) Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant Journal 37, 720-729.
30. Magome H., Yamaguchi S., Hanada A., Kamiya Y. & Oda K. (2008) DDF1 transcriptional activator upregulates expression of a gibberellin deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant Journal 56, 613-626.
31. Manning C.E., Miller D.G. & Teare I.D. (1977) Effect of moisture stress on leaf anatomy and water use efficiency of peas. Journal of the American Society for Horticultural Science 102, 756-760.
32. Mouradov A., Cremer F. & Coupland G. (2002) Control of flowering time: interacting pathways as a basic for diversity. Plant Cell 14, S111-S130.
33. Nakashima K. & Yamaguchi-Shinozaki K. (2010) Promoters and transcription factors in abiotic stress-responsive gene expression. In Abiotic Stress Adaptation in Plants: Physiological, Molecular and Genomic Foundation (eds A. Pareek, S.K. Sopory, H.J. Bohnert & Govindjee), pp. 199-216. Springer, Dordrecht, The Netherlands.
34. Nassuth A. & Siddiqua M. (2009) Regulation of stress responsive signalling pathways by eudicot CBF/DREB1 genes. In Plant Cold Hardiness: From the Laboratory to the Field (eds L. Gusta, M. Wisniewski & K. Tanino), pp. 131-139. CABI Publishing, Wallingford, UK.
35. Navarro M., Marque G., Ayax C., Keller G., Borges J.P., Marque C. & Teulieres C. (2009) Complementary regulation of four Eucalyptus CBF genes under various cold conditions. Journal of Experimental Botany 60, 2713-2724.
36. Navarro M., Ayax C., Martinez Y., Laur J., El Kayal W., Marque C. & Teulieres C. (2011) Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnology 9, 50-63.
37. Novillo F., Alonso J.-M., Ecker J.-R. & 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. Proceedings of the National Academy of Sciences of the United States of America 101, 3985-3990.
38. 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. Proceedings of the National Academy of Sciences of the United States of America 104, 21002-21007.
39. Palta J.P. & Li P.H. (1979) Frost-hardiness in relation to leaf anatomy and natural distribution of several Solanum species. Crop Science 19, 665-671.
40. Pino M.T., Skinner J.S., Jeknic Z., Hayes P.M., Soeldner A.H., Thomashow M.F. & Chen T.H.H. (2008) Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato. Plant, Cell & Environment 31, 393-406.
41. Pukacki P.M. & Rozek E.K. (2005) Effect of drought stress on chlorophyll a fluorescence and electrical admittance of shoots in Norway spruce seedlings. Trees: Structure and Function 19, 539-544.
42. Sakuma Y., Liu Q., Dubouzet J.G., Abe H., Shinozaki K. & Yamaguchi-Shinozaki K. (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochemical and Biophysical Research Communications 290, 998-1009.
43. Savitch L.V., Allard G., Seki M., Robert L.S., Tinker N.A., Huner N.P.A., Shinozaki K. & Singh J. (2005) The effect of overexpression of two Brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus. Plant Cell Physiology 46, 1525-1539.
44. Seo E., Lee H., Jeon J., Park H., Kim J., Noh Y.-S. & Lee I. (2009) Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC. Plant Cell 21, 3185-3197.
45. Silva M.A., Jifon J.L., Silva J.A.G. & Sharma V. (2007) Use of physiological parameters as fast tools to screen for drought tolerance in sugarcane. Brazilian Journal of Plant Physiology 19, 193-201.
46. Steponkus P.L. (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annual Review of Plant Physiology 35, 543-584.
47. Sterky F., Bhalerao R.R. & Unneberg P. (2004) A Populus EST resource for plant functional genomics. Proceedings of the National Academy of Sciences of the United States of America 101, 13951-13956.
48. Stockinger E.J., Gilmour S.J. & Thomashow M.F. (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences of the United States of America 94, 1035-1040.
49. Sun T.-P. (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiology 154, 567-570.
50. Survila M., Heino P. & Palva E.T. (2010) Genes and gene regulation for low-temperature tolerance. In Genes for Plant Abiotic Stress (eds M.A. Jenks & A. Wood), pp. 185-219. Wiley-Blackwell Publishing, New York.
51. Takuhara Y., Kobayashi M. & Suzuki S. (2011) Low-temperature-induced transcription factors in grapevine enhance cold tolerance in transgenic Arabidopsis plants. Journal of Plant Physiology. doi: 10.1016/j.jplph.2010.11.008.
52. Thomashow M.F. (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold-response pathway. Plant Physiology 154, 571-577.
53. Tong Z., Hong B., Yang Y., Li Q., Ma N., Ma C. & Gao J. (2009) Overexpression of two chrysanthemum DgDREB1 group genes caused delayed flowering or dwarfism in Arabidopsis. Plant Molecular Biology 71, 115-129.
54. Uemura M., Joseph R.A. & Stephonkus P.L. (1995) Cold acclimation of Arabidopsis thaliana: effect on plasma membrane lipid composition and freeze-induced lesions. Plant Physiology 109, 15-30.
55. Welling A. & Palva E.T. (2008) Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiology 147, 1199-1211.
56. Wilkinson S., Clephan A.L. & Davies W.J. (2001) Rapid low temperature-induced stomatal closure occurs in cold-tolerant Commelina communis leaves but not in cold-sensitive tobacco leaves, via a mechanism that involves apoplastic calcium but not abscisic acid. Plant Physiology 126, 1566-1578.
57. Xiao H., Siddiqua M., Braybrook S. & Nassuth A. (2006) Three grape CBF/DREB1 genes are regulated by low temperature, drought and abscisic acid. Plant, Cell & Environment 29, 1410-1421.
58. Xiao H., Tattersall E., Siddiqua M., Cramer G.R. & Nassuth A. (2008) CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant, Cell & Environment 31, 1-10.
59. Xin Z. & Browse U.J. (1998) Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proceedings of the National Academy of Sciences of the United States of America 95, 7799-7804.
60. Xue G.P. (2002) Characterisation of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid, quantitative and high-throughput analysis of the DNA-binding activity. Nucleic Acids Research 30, e77.
61. Zhang Y., Yang T.-W., Zhang L.-J., Zhang T.-G., Di C.-X., Xu S.-J. & An L.-Z. (2006) Isolation and expression analysis of two cold-inducible genes encoding putative CBF transcription factors from Chinese cabbage (Brassica pekinensis Rupr.). Journal of Integrative Plant Biology 48, 848-856.
62. Zhao T.J., Sun S., Liu Y., Liu J.M., Liu Q., Yan Y.B. & Zhou H.M. (2006) Regulating the drought-responsive element (DRE)-mediated signaling pathway by synergistic functions of trans-active and trans-inactive DRE binding factors in Brassica napus. Journal of Biological Chemistry 281, 10752-10759.
63. Zhen Y. & Ungerer M.C. (2008) Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana. New Phytology 177, 419-427.