Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development

Plant Biotechnology Journal

Volumn 9, Issue 1, 2011, Pages 50-63

  Navarro, Marie ^a   Ayax, Céline ^a   Martinez, Yves ^a   Laur, Joan ^a   El Kayal, Walid ^b   Marque, Christiane ^a   Teulières, Chantal ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

CBF overexpression; Oil gland; Reduced growth; Stress tolerance; Transgenic Eucalyptus; Wax

Indexed keywords

TRANSACTIVATOR PROTEIN;

ARTICLE; COLD; EUCALYPTUS; FREEZING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TRANSGENE; UPREGULATION;

COLD TEMPERATURE; EUCALYPTUS; FREEZING; GENE EXPRESSION REGULATION, PLANT; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS; TRANSGENES; UP-REGULATION;

EUCALYPTUS; EUCALYPTUS GUNNII; EUCALYPTUS HYBRIDA;

EID: 78650048926     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2010.00530.x     Document Type: Article

References (49)

1. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P. and 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.
2. Agarwal, P.K., Agarwal, P., Reddy, M.K. and Sopory, S.K. (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep., 25, 1263-1274.
3. Aharoni, A., Dixit, S., Jetter, R., Thoenes, E., Van Arkel, G. and Pereira, A. (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell, 16, 2463-2480.
4. Banks, J.C.G. and Whitecross, M.I. (1971) Ecotypic Variation in Eucalyptus-viminalis Labill.1. Leaf Surface Waxes, a Tempera-ture×Origin Interaction. Aust. J. Bot., 19, 327-334.
5. Benedict, C., Skinner, J.S., Meng, R., Chang, Y., Bhalerao, R., Huner, N.P., Finn, C.E., Chen, T.H. and 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, 1259-1272.
6. Bouchabke-Coussa, O., Quashie, M.L., Seoane-Redondo, J., Fortabat, M.N., Gery, C., Yu, A., Linderme, D., Trouverie, J., Granier, F., Teoule, E. and Durand-Tardif, M. (2008) ESKIMO1 is a key gene involved in water economy as well as cold acclimation and salt tolerance. BMC Plant Biol., 8, 125.
7. Burley, J., Wood, P.J. and Hans, A.S. (1971) Variation in Leaf Characteristics among Provenances of Eucalyptus-camaldulensis Dehn Grown in Zambia. Aust. J. Bot., 19, 237-249.
8. Champ, K.I., Febres, V.J. and Moore, G.A. (2007) The role of CBF transcriptional activators in two Citrus species (Poncirus and Citrus) with contrasting levels of freezing tolerance. Physiol. Plant, 129, 529-541.
9. Close, D.C. and Beadle, C.L. (2003) The ecophysiology of foliar anthocyanin. Bot. Rev., 69(2), 149-161.
10. Close, D.C., Beadle, C.L., Brown, P.H. and Holz, G.K. (2000) Cold-induced photoinhibition affects establishment of Eucalyptus nitens (Deane and Maiden) Maiden and Eucalyptus globulus Labill. Trees - Struct. Funct., 15, 32-41.
11. Costa e Silva, F., Shvaleva, A., Broetto, F., Ortuno, M.F., Rodrigues, M.L., Almeida, M.H., Chaves, M.M. and Pereira, J.S. (2009) Acclimation to short-term low temperatures in two Eucalyptus globulus clones with contrasting drought resistance. Tree Physiol., 29, 77-86.
12. El Kayal, W., Navarro, M., Marque, G., Keller, G., Marque, C. and Teulieres, C. (2006) Expression profile of CBF-like transcriptional factor genes from Eucalyptus in response to cold. J. Exp. Bot., 57, 2455-2469.
13. Fowler, S. and Thomashow, M.F. (2002) Arabidopsis transcrip-tome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell, 14, 1675-1690.
14. Gamboa, M.C., Rasmussen-Poblete, S., Valenzuela, P.D. and Krauskopf, E. (2007) Isolation and characterization of a cDNA encoding a CBF transcription factor from E. globulus. Plant Physiol. Biochem., 45, 1-5.
15. Gao, M.J., Allard, G., Byass, L., Flanagan, A.M. and Singh, J. (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol. Biol., 49, 459-471.
16. Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D. and Thomashow, M.F. (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol., 124, 1854-1865.
17. Gilmour, S.J., Fowler, S.G. and Thomashow, M.F. (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol. Biol., 54, 767-781.
18. Hannah, M.A., Wiese, D., Freund, S., Fiehn, O., Heyer, A.G. and Hincha, D.K. (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol., 142, 98-112.
19. Hsieh, T.H., Lee, J.T., Charng, Y.Y. and Chan, M.T. (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol., 130, 618-626.
20. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O. and Thomashow, M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science, 280, 104-106.
21. Karimi, M., Inzé, D. and Depicker, A. (2002) GATEWAY(TM) vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci., 7, 193-195.
22. Kasuga, M., Miura, S., Shinozaki, K. and 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, 346-350.
23. Keller, G., Marchal, T., SanClemente, H., Navarro, M., Ladouce, N., Wincker, P., Couloux, A., Teulieres, C. and Marque, C. (2009) Development and functional annotation of an 11, 303-EST collection from Eucalyptus for studies of cold tolerance. Tree Genet. Genomes, 5, 317-327.
24. Kim, J.S., Jung, H.J., Lee, H.J., Kim, K.A., Goh, C.-H., Woo, Y., Oh, S.H., Han, Y.S. and Kang, H. (2008) Glycine-rich RNA-binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J., 55, 455-466.
25. Kitashiba, H., Ishizaka, T., Isuzugawa, K., Nishimura, K. and Suzuki, T. (2004) Expression of a sweet cherry DREB1/CBF ortholog in Arabidopsis confers salt and freezing tolerance. J. Plant Physiol., 161, 1171-1176.
26. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. and 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. Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods, 25, 402-408.
28. Louro, R.P., Santiago, L.J.M., Dos Santos, A.V. and Machado, R.D. (2003) Ultrastructure of E. grandis-×-E. urophylla plants cultivated ex vitro in greenhouse and field conditions. Trees - Struc. Func., 17, 11-22.
29. Mancinelli, A.L., Yang, C.-P.H., Lindquist, P., Anderson, O.R. and Rabino, I. (1975) Photocontrol of Anthocyanin Synthesis: III. The Action of Streptomycin on the Synthesis of Chlorophyll and Anthocyanin. Plant Physiol., 55, 251-257.
30. Marque, G. (2008) Isolement et caractérisation chez l'Eucalyptus de gènes codant les facteurs de transcription CBF impliqués dans la réponse au froid. Université de Toulouse, Toulouse
31. McCauley, M.M. and Evert, R.F. (1988) The Anatomy of the Leaf of Potato, Solanum-Tuberosum-L Russet Burbank. Bot. Gaz., 149, 179-195.
32. Miller, A.K., Galiba, G. and Dubcovsky, J. (2006) A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-A (m) 2 in Triticum monococcum. Mol. Genet. Genomics, 275, 193-203.
33. Navarro, M., Marque, G., Ayax, C., Keller, G., Borges, J.P., Marque, C. and Teulieres, C. (2009) Complementary regulation of four Eucalyptus CBF genes under various cold conditions. J. Exp. Bot., 60, 2713-2724.
34. Novillo, F., Medina, J. and 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. USA, 104, 21002-21007.
35. Pino, M.T., Skinner, J.S., Jeknic, Z., Hayes, P.M., Soeldner, A.H., Thomashow, M.F. and Chen, T.H. (2008) Ectopic AtCBF1 over-expression enhances freezing tolerance and induces cold acclimation-associated physiological modifications in potato. Plant Cell Environ., 31, 393-406.
36. Savitch, L.V., Allard, G., Seki, M., Robert, L.S., Tinker, N.A., Huner, N.P., Shinozaki, K. and Singh, J. (2005) The effect of over-expression of two Brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus. Plant Cell Physiol., 46, 1525-1539.
37. Skinner, J.S., Szucs, P., Von Zitzewitz, J., Marquez-Cedillo, L., Filichkin, T., Stockinger, E.J., Thomashow, M.F., Chen, T.H. and Hayes, P.M. (2006) Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theor. Appl. Genet., 12, 832-842.
38. Tom Shepherd, D.W.G. (2006) The effects of stress on plant cuticular waxes. New Phytol., 171, 469-499.
39. Tournier, V., Grat, S., Marque, C., El Kayal, W., Penchel, R., De Andrade, G., Boudet, A.-M. and Teulières, C. (2003) An efficient procedure to stably introduce genes into an economically important pulp tree (Eucalyptus grandis-×-Eucalyptus urophylla). Transgenic Res., 12, 403-411.
40. Wilkinson, S., Clephan, A.L. and 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 Physiol., 126, 1566-1578.
41. Xiao, H., Tattersall, E.A., Siddiqua, M.K., Cramer, G.R. and Nassuth, A. (2008) CBF4 is a unique member of the CBF transcription factor family of Vitis vinifera and Vitis riparia. Plant Cell Environ., 31, 1-10.
42. Xin, Z. and Browse, J. (1998) eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl Acad. Sci. USA, 95, 7799-7804.
43. Yu, H., Chen, X., Hong, Y.Y., Wang, Y., Xu, P., Ke, S.D., Liu, H.Y., Zhu, J.K., Oliver, D.J. and Xiang, C.B. (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell, 20, 1134-1151.
44. Zarka, D.G., Vogel, J.T., Cook, D. and Thomashow, M.F. (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, 910-918.
45. Zhang, X., Fowler, S.G., Cheng, H., Lou, Y., Rhee, S.Y., Stockinger, E.J. and Thomashow, M.F. (2004) Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J., 39, 905-919.
46. Zhang, J.Y., Broeckling, C.D., Sumner, L.W. and Wang, Z.Y. (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol. Biol., 64, 265-278.
47. Zhou, X.F., Wang, G.D., Sutoh, K., Zhu, J.K. and Zhang, W.X. (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms, 1779, 780-788.
48. Zhu, J., Shi, H., Lee, B.H., Damsz, B., Cheng, S., Stirm, V., Zhu, J.K., Hasegawa, P.M. and Bressan, R.A. (2004) An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc. Natl Acad. Sci. USA, 101, 9873-9878.
49. Zhu, J., Verslues, P.E., Zheng, X., Lee, B.H., Zhan, X., Manabe, Y., Sokolchik, I., Zhu, Y., Dong, C.H., Zhu, J.K., Hasegawa, P.M. and Bressan, R.A. (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc. Natl Acad. Sci. USA, 102, 9966-9971.