Orthologs of the class A4 heat shock transcription factor HsfA4a confer cadmium tolerance in wheat and rice

Plant Cell

Volumn 21, Issue 12, 2009, Pages 4031-4043

  Shim, Donghwan ^a   Hwang, Jae Ung ^a   Lee, Joohyun ^a,c   Lee, Sichul ^a   Choi, Yunjung ^a   An, Gynheung ^a   Martinoia, Enrico ^a,b   Lee, Youngsook ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LILIOPSIDA; ORYZA SATIVA; TRITICUM AESTIVUM;

EID: 75649125258     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.066902     Document Type: Article

References (52)

1. Alscher, R.G., Erturk, N., and Heath, L.S. (2002). Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53: 1331-1341.
2. Baniwal, S.K., 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., and Nover, L. (2007). Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 282: 3605-3613.
4. Braman, J., Papworth, C., and Greener, A. (1996). Site-directed mutagenesis using double-stranded plasmid DNA templates. Methods Mol. Biol. 57: 31-44.
5. Butt, T.R., and Ecker, D.J. (1987). Yeast metallothionein and applications in biotechnology. Microbiol. Rev. 51: 351-364.
6. Chen, T., and Parker, C.S. (2002). Dynamic association of transcriptional activation domains and regulatory regions in Saccharomyces cerevisiae heat shock factor. Proc. Natl. Acad. Sci. USA 99: 1200-1205.
7. Clemens, S. (2001). Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212: 475-486.
8. Clemens, S., Kim, E.J., Neumann, D., and Schroeder, J.I. (1999). Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 18: 3325-3333.
9. Clemens, S., Palmgren, M.G., and Kramer, U. (2002). A long way ahead: Understanding and engineering plant metal accumulation. Trends Plant Sci. 7: 309-315.
10. Dalton, T.P., Solis, W.A., Nebert, D.W., and Carvan III, M.J. (2000). Characterization of the MTF-1 transcription factor from zebrafish and trout cells. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 126: 325-335.
11. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V., Schlauch, K., and Mittler, R. (2005). Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17: 268-281.
12. Ecker, D.J., Butt, T.R., Sternberg, E.J., Neeper, M.P., Debouck, C., Gorman, J.A., and Crooke, S.T. (1986). Yeast metallothionein function in metal ion detoxification. J. Biol. Chem. 261: 16895-16900.
13. Egli, D., Selvaraj, A., Yepiskoposyan, H., Zhang, B., Hafen, E., Georgiev, O., and Schaffner, W. (2003). Knockout of'metal-responsive transcription factor' MTF-1 in Drosophila by homologous recombination reveals its central role in heavy metal homeostasis. EMBO J. 22: 100-108.
14. Goyer, R.A. (1997). Toxic and essential metal interactions. Annu. Rev. Nutr. 17: 37-50.
15. Ha, S.B., Smith, A.P., Howden, R., Dietrich, W.M., Bugg, S., O'Connell, M.J., Goldsbrough, P.B., and Cobbett, C.S. (1999). Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11: 1153-1164.
16. Hart, B.A., Lee, C.H., Shukla, G.S., Shukla, A., Osier, M., Eneman, J. D., and Chiu, J.F. (1999). Characterization of cadmium-induced apoptosis in rat lung epithelial cells: evidence for the participation of oxidant stress. Toxicology 133: 43-58.
17. Herbette, S., et al. (2006). Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88: 1751-1765.
18. Imura, N., Naganuma, A., and Satoh, M. (1989). Metallothionein as a resistance factor for antitumor drugs. Gan To Kagaku Ryoho 16: 599-604.
19. Jarup, L., Berglund, M., Elinder, C.G., Nordberg, G., and Vahter, M. (1998). Health effects of cadmium exposure-A review of the literature and a risk estimate. Scand. J. Work Environ. Health 24 (Suppl. 1): 1-51.
20. Jeyaprakash, A., Welch, J.W., and Fogel, S. (1991). Multicopy CUP1 plasmids enhance cadmium and copper resistance levels in yeast. Mol. Gen. Genet. 225: 363-368.
21. Jin, S., Cheng, Y., Guan, Q., Liu, D., Takano, T., and Liu, S. (2006). A metallothionein-like protein of rice (rgMT) functions in E. coli and its gene expression is induced by abiotic stresses. Biotechnol. Lett. 28: 1749-1753.
22. Kim, D.Y., Bovet, L., Maeshima, M., Martinoia, E., and Lee, Y. (2007). The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 50: 207-218.
23. Kim, Y.Y., Kim, D.Y., Shim, D., Song, W.Y., Lee, J., Schroeder, J.I., Kim, S., Moran, N., and Lee, Y. (2008). Expression of the novel wheat gene TM20 confers enhanced cadmium tolerance to bakers' yeast. J. Biol. Chem. 283: 15893-15902.
24. Kotak, S., Port, M., Ganguli, A., Bicker, F., and von Koskull-Doring, 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.
25. Kotak, S., Vierling, E., Baumlein, H., and von Koskull-Doring, P. (2007). A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19: 182-195.
26. Langmade, S.J., Ravindra, R., Daniels, P.J., and Andrews, G.K. (2000). The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J. Biol. Chem. 275: 34803-34809.
27. Lee, J., Bae, H., Jeong, J., Lee, J.Y., Yang, Y.Y., Hwang, I., Martinoia, E., and Lee, Y. (2003). Functional expression of a bacterial heavy metal transporter in Arabidopsis enhances resistance to and decreases uptake of heavy metals. Plant Physiol. 133: 589-596.
28. Li, Z.S., Lu, Y.P., Zhen, R.G., Szczypka, M., Thiele, D.J., and Rea, P. A. (1997). A new pathway for vacuolar cadmium sequestration in Saccharomyces cerevisiae: YCF1-catalyzed transport of bis(glutathionato)cadmium. Proc. Natl. Acad. Sci. USA 94: 42-47.
29. Miller, G., and Mittler, R. (2006). Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. (Lond.) 98: 279-288.
30. Mishra, S.K., Tripp, J., Winkelhaus, S., Tschiersch, B., Theres, K., Nover, L., and 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: 1555-1567.
31. Nakai, A. (1999). New aspects in the vertebrate heat shock factor system: Hsf3 and Hsf4. Cell Stress Chaperones 4: 86-93.
32. Nover, L., Bharti, K., Doring, P., Mishra, S.K., Ganguli, A., and Scharf, K.D. (2001). Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6: 177-189.
33. Ogawa, D., Yamaguchi, K., and Nishiuchi, T. (2007). High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J. Exp. Bot. 58: 3373-3383.
34. Ortiz, D.F., Ruscitti, T., McCue, K.F., and Ow, D.W. (1995). Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem. 270: 4721-4728.
35. Preveral, S., Gayet, L., Moldes, C., Hoffmann, J., Mounicou, S., Gruet, A., Reynaud, F., Lobinski, R., Verbavatz, J.M., Vavasseur, A., and Forestier, C. (2009). A common highly conserved cadmium detoxification mechanism from bacteria to humans: heavy metal tolerance conferred by the ATP-binding cassette (ABC) transporter SpHMT1 requires glutathione but not metal-chelating phytochelatin peptides. J. Biol. Chem. 284: 4936-4943.
36. Qi, X., Zhang, Y., and Chai, T. (2007). Characterization of a novel plant promoter specifically induced by heavy metal and identification of the promoter regions conferring heavy metal responsiveness. Plant Physiol. 143: 50-59.
37. Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual, 3rd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
38. Sandalio, L.M., Dalurzo, H.C., Gomez, M., Romero-Puertas, M.C., and del Rio, L.A. (2001). Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J. Exp. Bot. 52: 2115-2126.
39. Schutzendubel, A., Schwanz, P., Teichmann, T., Gross, K., Langenfeld-Heyser, R., Godbold, D.L., and Polle, A. (2001). Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol. 127: 887-898.
40. Sewell, A.K., Yokoya, F., Yu, W., Miyagawa, T., Murayama, T., and Winge, D.R. (1995). Mutated yeast heat shock transcription factor exhibits elevated basal transcriptional activation and confers metal resistance. J. Biol. Chem. 270: 25079-25086.
41. Tang, W., Charles, T.M., and Newton, R.J. (2005). Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus Virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol. Biol. 59: 603-617.
42. Vido, K., Spector, D., Lagniel, G., Lopez, S., Toledano, M.B., and Labarre, J. (2001). A proteome analysis of the cadmium response in Saccharomyces cerevisiae. J. Biol. Chem. 276: 8469-8474.
43. von Koskull-Doring, P., Scharf, K.D., and Nover, L. (2007). The diversity of plant heat stress transcription factors. Trends Plant Sci. 12: 452-457.
44. Weber, M., Trampczynska, A., and Clemens, S. (2006). Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd(2+)-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ. 29: 950-963.
45. Wimmer, U., Wang, Y., Georgiev, O., and Schaffner, W. (2005). Two major branches of anti-cadmium defense in the mouse: MTF-1/ metallothioneins and glutathione. Nucleic Acids Res. 33: 5715-5727.
46. Wu, C. (1995). Heat shock transcription factors: structure and regulation. Annu. Rev. Cell Dev. Biol. 11: 441-469.
47. Yamanouchi, U., Yano, M., Lin, H., Ashikari, M., and Yamada, K. (2002). A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc. Natl. Acad. Sci. USA 99: 7530-7535.
48. Yepiskoposyan, H., Egli, D., Fergestad, T., Selvaraj, A., Treiber, C., Multhaup, G., Georgiev, O., and Schaffner, W. (2006). Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res. 34: 4866-4877.
49. Yokotani, N., Ichikawa, T., Kondou, Y., Matsui, M., Hirochika, H., Iwabuchi, M., and Oda, K. (2008). Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227: 957-967.
50. Zhang, B., Georgiev, O., Hagmann, M., Gunes, C., Cramer, M., Faller, P., Vasak, M., and Schaffner, W. (2003). Activity of metalresponsive transcription factor 1 by toxic heavy metals and H2O2 in vitro is modulated by metallothionein. Mol. Cell. Biol. 23: 8471-8485.
51. Zhou, G., Xu, Y., Li, J., Yang, L., and Liu, J.Y. (2006). Molecular analyses of the metallothionein gene family in rice (Oryza sativa L.). J. Biochem. Mol. Biol. 39: 595-606.
52. Zhou, J., and Goldsbrough, P.B. (1994). Functional homologs of fungal metallothionein genes from Arabidopsis. Plant Cell 6: 875-884.