A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis

Plant Journal

Volumn 53, Issue 2, 2008, Pages 264-274

  Schramm, Franziska ^a   Larkindale, Jane ^b   Kiehlmann, Elke ^a   Ganguli, Arnab ^a   Englich, Gisela ^a   Vierling, Elizabeth ^b   Von Koskull Döring, Pascal ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Arabidopsis; C repeat binding proteins; DRE binding proteins; Heat stress proteins; Heat stress response; Heat stress transcription factors

Indexed keywords

ARABIDOPSIS; C-REPEAT BINDING PROTEINS; DRE-BINDING PROTEINS; HEAT STRESS PROTEINS; HEAT STRESS RESPONSE; HEAT STRESS TRANSCRIPTION FACTORS;

ASSAYS; DEHYDRATION; ELECTROPHORETIC MOBILITY; SODIUM CHLORIDE; TRANSCRIPTION FACTORS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; DNA BINDING PROTEIN; DREB2A PROTEIN, ARABIDOPSIS; HEAT SHOCK PROTEIN; HEAT STRESS TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEAT; METABOLISM; PROMOTER REGION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HEAT; HEAT-SHOCK PROTEINS; PLANT PROTEINS; PROMOTER REGIONS (GENETICS); TRANSCRIPTION FACTORS;

ARABIDOPSIS;

EID: 37749025808     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03334.x     Document Type: Article

References (62)

1. Baker, S.S., Wilhelm, K.S. Thomashow, M.F. (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, 701 713.
2. Baniwal, S.K., Bharti, K., Chan, K.Y. et al. (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci. 29, 471 487.
3. Baniwal, S. K., Chan, K. Y., Scharf, K.-D. Nover, L. (2007) Role of heat stress transcirption factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 282, 3605 3613.
4. Bharti, K., Schmidt, E., Lyck, R., Heerklotz, D., Bublak, D. Scharf, K.D. (2000) Isolation and characterization of HsfA3, a new heat stress transcription factor of Lycopersicon peruvianum. Plant J. 22, 355 365.
5. Busch, W., Wunderlich, M. Schöffl, F. (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J. 41, 1 14.
6. Charng, Y., Liu, H., Liu, N., Chi, W., Wang, C., Chang, S. Wang, T. (2007) Heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 143, 251 262.
7. Cook, D., Fowler, S., Fiehn, O. Thomashow, M.F. (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 15248.
8. Czarnecka-Verner, E., Yuan, C.X., Scharf, K.D., Englich, G. Gurley, W.B. (2000) Plants contain a novel multi-member class of heat shock factors without transcriptional activator potential. Plant Mol. Biol. 43, 459 471.
9. Czarnecka-Verner, E., Pan, S., Salem, T. Gurley, W.B. (2004) Plant class B HSFs inhibit transcription and exhibit affinity for TFIIB and TBP. Plant Mol. Biol. 56, 57 75.
10. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V., Schaluch, K. Mittler, R. (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen network of Arabidopsis. Plant Cell, 17, 268 281.
11. Döring, P., Treuter, E., Kistner, C., Lyck, R., Chen, A. Nover, L. (2000) The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2. Plant Cell, 12, 265 278.
12. 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 J. 16, 433 442.
13. 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 Physiol. 130, 639 648.
14. Hartl, F.U. Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science, 295, 1852 1858.
15. Haslbeck, M (2002) sHsps and their role in the chaperone network. Cell. Mol. Life Sci. 59, 1649 1657.
16. Hong, S.W. Vierling, E. (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J. 27, 25 35.
17. Hübel, A. Schöffl, F. (1994) Arabidopsis heat shock factor: isolation and characterization of the gene and the recombinant protein. Plant Mol. Biol. 26, 353 362.
18. Hübel, A., Lee, J.H., Wu, C. Schöffl, F. (1995) Arabidopsis heat shock factor is constitutively active in Drosophila and human cells. Mol. Gen. Genet. 248, 136 141.
19. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature, 436, 793 799.
20. Kim, B.H. Schöffl, F. (2002) Interaction between Arabidopsis heat shock transcription factor 1 and 70 kDa heat shock proteins. J. Exp. Bot. 53, 371 375.
21. Kotak, S., Port, M., Ganguli, A., Bicker, F. von Koskull-Döring, P. (2004) Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J. 39, 98 112.
22. Kotak, S., Vierling, E., Bäumlein, H. von Koskull-Döring, P. (2007a) A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell, 19, 182 195.
23. Kotak, S., Larkindale, J., Lee, U., von Koskull-Doring, P., Vierling, E. Scharf, K.D. (2007b) Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10, 310 316.
24. Larkindale, J., Hall, J.D., Knight, M.R. Vierling, E. (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882 897.
25. Li, C., Chen, Q., Gao, X., Qi, B., Chen, N., Xu, S., Chen, J. Wang, X. (2005) AtHsfA2 modulates expression of stress responsive genes and enhances tolerance to heat and oxidative stress in Arabidopsis. Sci. China C. Life Sci. 48, 540 550.
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. Lohmann, C., Eggers-Schumacher, G., Wunderlich, M. Schöffl, F. (2004) Two different heat shock factors regulate immediate early expression of stress genes in Arabidopsis. Mol. Genet. Genomics, 271, 11 21.
28. Lyck, R., Harmening, U., Höhfeld, I., Treuter, E., Scharf, K.D. Nover, L. (1997) Intracellular distribution and identification of the nuclear localization signals of two plant heat-stress transcription factors. Planta, 202, 117 125.
29. Miller, G. Mittler, R. (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98, 279 288.
30. Mishra, S.K., Tripp, J., Winkelhaus, S., Tschiersch, B., Theres, K., Nover, L. Scharf, K.-D. (2002) In the complex family of heat stress transcription factors HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 16, 1555 1565.
31. 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, 982 993.
32. Morimoto, R.I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones and negative regulators. Genes Dev. 12, 3788 3796.
33. Nakamoto, H. Vígh, L. (2007) The small heat shock proteins and their clients. Cell Mol. Life Sci. 64, 294 306.
34. Nakashima, K., Shinwari, Z.K., Sakuma, Y., Seki, M., Miura, S., Shinozaki, K. Yamaguchi-Shinozaki, K. (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol. Biol. 42, 657 665.
35. Nishizawa, A., Yabuta, Y., Yoshida, E., Maruta, T., Yoshimura, K. Shigeoka, S. (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535 547.
36. Nover, L. Scharf, K.-D. (1997) Heat stress proteins and transcription factors. Cell. Mol. Life Sci. 53, 80 103.
37. Nover, L., Kapil, B., Döring, P., Mishra, S.K., Ganguli, A. Scharf, K.-D. (2001) Arabidopsis and the Hsf world: how many heat stress transcription factors do we need? Cell Stress Chap. 6, 177 189.
38. Panchuk, I. I., Volkov, R. A. Schöffl, F. (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 129, 838 853.
39. Prändl, R., Hinderhofer, K., Eggers-Schumacher, G. Schöffl, F. (1998) Hsf3, a new heat shock factor from Arabidopsis thaliana, derepresses the heat shock response and confers thermotolerance when overexpressed in transgenic plants. Mol. Gen. Genet. 258, 269 278.
40. Qin, F., Kakimoto, M., Sakuma, Y., Maruyama, K., Osakabe, Y., Tran, L.-S. P, Shinozaki, K. Yamaguchi-Shinozaki, K. (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stress in Zea mays L. Plant J. 50, 54 59.
41. Reindl, A. Schöffl, F. (1998) Interaction between the Arabidopsis thaliana heat shock transcription factor HSF1 and the TATA binding protein TBP. FEBS Lett. 436, 318 322.
42. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S. Mittler, R. (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683 1696.
43. 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. Biochem. Biophys. Res. Commun. 290, 998 1009.
44. Sakuma, Y., Maruyama, K., Osakabe, Y., Qin, F., Seki, M., Shinozaki, K. Yamaguchi-Shinozaki, K. (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell, 18, 1292 1309.
45. Sakuma, Y., Maruyama, K., Qin, F., Osakabe, Y., Shinozaki, K. Yamaguchi-Shinozaki, K. (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl Acad. Sci. U.S.A. 103, 18822 18827.
46. Scharf, K.-D., Heider, H., Höhfeld, I., Lyck, R., Schmidt, E. Nover, L. (1998a) The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol. Cell. Biol. 18, 2240 2251.
47. Scharf, K.-D., Höhfeld, I. Nover, L. (1998b) Heat stress response and heat stress transcription factors. J. Biosci. 23, 313 329.
48. Schöffl, F., Prändl, R. Reindl, A. (1998) Regulation of the heat-shock response. Plant Physiol. 117, 1135 1141.
49. Schramm, F., Ganguli, A., Kiehlmann, E., Englich, G., Walch, D. von Koskull-Döring, P. (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol. Biol. 60, 759 772.
50. Shinozaki, K. Yamaguchi-Shinozaki, K. (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3, 217 223.
51. Shinozaki, K., Yamaguchi-Shinozaki, K. Seki, M. (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant Biol. 6, 410 417.
52. 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 water deficit. Proc. Natl Acad. Sci. U.S.A. 94, 1035 1040.
53. The Arabidopsis Genome Initiative. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796 815.
54. Thomashow, M.F. (1999) PLANT COLD ACCLIMATION: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 50, 571 599.
55. Töpfer, R., Schell, J. Steinbiss, H.H. (1988) Versatile cloning vectors for transient gene expression and direct gene transfer in plant cells. Nucleic Acids Res. 16, 8725.
56. Wang, W., Vinocur, B., Shoseyov, O. Altman, A. (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244 252.
57. Wehmeyer, N., Hernandez, L., Finkelstein, R. Vierling, E. (1996) Synthesis of small heat-shock proteins is part of the developmental program of late seed maturation. Plant Physiol. 112, 757 757.
58. Wu, C. (1995) Heat stress transcription factors. Annu. Rev. Cell Biol. 11, 441 469.
59. Wunderlich, M., Werr, W. Schöffl, F. (2003) Generation of dominant-negative effects on the heat shock response in Arabidopsis thaliana by transgenic expression of a chimaeric HSF1 protein fusion construct. Plant J. 35, 442 451.
60. Xiong, Y., Liu, T., Tian, C., Sun, S., Li, J. Chen, M. (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol. Biol. 59, 191 203.
61. 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, 251 264.
62. Yamaguchi-Shinozaki, K. Shinozaki, K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci. 10, 88 94.