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Yeast copper-dependent transcription factor ACE1 enhanced copper stress tolerance in Arabidopsis

  • Xu, Jing (State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University) ;
  • Tian, Yong-Sheng (Agro-Biotechnology Research Center, Shanghai Academy of Agricultural Sciences) ;
  • Peng, Ri-He (Agro-Biotechnology Research Center, Shanghai Academy of Agricultural Sciences) ;
  • Xiong, Ai-Sheng (Agro-Biotechnology Research Center, Shanghai Academy of Agricultural Sciences) ;
  • Zhu, Bo (Agro-Biotechnology Research Center, Shanghai Academy of Agricultural Sciences) ;
  • Jin, Xiao-Fen (Agro-Biotechnology Research Center, Shanghai Academy of Agricultural Sciences) ;
  • Gao, Jian-Jie (State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University) ;
  • Hou, Xi-Lin (State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University) ;
  • Yao, Quan-Hong (Agro-Biotechnology Research Center, Shanghai Academy of Agricultural Sciences)
  • Published : 2009.11.30

Abstract

Copper is essential but toxic in excess for aerobic organisms. Yeast transcription factor ACE1 functions as a sensor for copper and an inducer for the transcription of CUP1. In addition, ACE1 can activate the transcription of superoxide dismutase gene (sod1) in response to copper. In this study, we introduced the yeast ACE1 into Arabidopsis and analyzed its function in plant. Under high copper stress, the transgenic plants over-expressing ACE1 showed higher survival rate than the wild-type. We also found that over-expression of ACE1 in Arabidopsis increased the activities of SOD and POD, which were beneficial to the cell in copper buffering. Excess copper would suppress the expression of chlorophyll biosynthetic genes in Arabidopsis, RT-PCR analysis revealed that over-expression of ACE1 decrease the suppression. Together, our results indicate that ACE1 may play an important role in response to copper stress in Arabidopsis.

Keywords

References

  1. Maksymiec, W. (1997) Effect of copper on cellular processes in higher plants. Photosynthetica. 34, 321-342 https://doi.org/10.1023/A:1006818815528
  2. Mocquot, B., Vangronsveld, J., Clijsters, H. and Mench, M. (1996) Copper toxicity in young maize (Zea mays L.) plants: effects on growth, mineral and chlorophyll contents, and enzyme activities. Plant. Soil. 182, 287-300 https://doi.org/10.1007/BF00029060
  3. Weckx, J. E. J. and Clijsters, H. M. M. (1996) Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as result of root assimilation of toxic amounts of copper. Physiol. Plant. 96, 506-512 https://doi.org/10.1111/j.1399-3054.1996.tb00465.x
  4. Chen, L. M., Lin, C. C. and Kao, C. H. (2000) Copper toxicity in rice seedlings: changes in antioxidative enzyme activies, $H_2O_2$ level, and cell wall peroxidase activity in roots. Bot. Bull. Acad. Sin. 41, 99-103
  5. Sandmann, G. and Böger, P. (1980) Copper-mediated Lipid Peroxidation Processes in Photosynthetic Membranes. Plant. Physiol. 66, 797-800 https://doi.org/10.1104/pp.66.5.797
  6. Cuyers, A., Vangronsveld, J. and Clijsters, H. (2000) Biphasic effect of copper on the ascorbate-glutathione pathway in primary leaves of Phaseolus vulgaris seedlings during the early stages of metal assimilation. Physiol. Plant. 110, 512-517 https://doi.org/10.1111/j.1399-3054.2000.1100413.x
  7. Groppa, M. D., Tomaro, M. L. and Benavides, M. P. (2001) Polyamines as protectors against cadmium or coper-induced oxidative damage in sunflower leaf discs. Plant. Sci. 161, 481-488 https://doi.org/10.1016/S0168-9452(01)00432-0
  8. De Vos, C. H. R., Schat, H., De Waal, M. A. M., Vooijs, R. and Ernst, W. H. O. (1991) Increased resistance to copper-induced damage of the root cell plasmalemma in copper tolerant Silene cucubalus. Physiol. Plant. 82, 523-528 https://doi.org/10.1111/j.1399-3054.1991.tb02942.x
  9. Murphy, A. and Taiz, L. (1997) Correlation between potassium efflux and copper sensitivity in ten Arabidopsis ecotypes. New Phytol. 136, 211-222 https://doi.org/10.1046/j.1469-8137.1997.00738.x
  10. Drazkiewicz, M., Skorzynska-Polit, E. and Krupa, Z. (2004) Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. BioMetals. 17, 379-387 https://doi.org/10.1023/B:BIOM.0000029417.18154.22
  11. Foyer, C. H., Lopez-Delgado, H., Dat, J. F. and Scott, I. M. (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling. Physiol. Plant. 100, 241-254 https://doi.org/10.1111/j.1399-3054.1997.tb04780.x
  12. Clemens, S. (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta. 212, 475-486 https://doi.org/10.1007/s004250000458
  13. Cobbett, C. and Goldsbrough, P. (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant. Biol. 53, 159-182 https://doi.org/10.1146/annurev.arplant.53.100301.135154
  14. Hall, J. L. and Williams, L. E. (2003) Transition metal transporters in plants. J. Exp. Bot. 54, 2601-2613 https://doi.org/10.1093/jxb/erg303
  15. Hu, S., Furst, P. and Hamer, D. (1990) The DNA and Cu binding functions of ACE1 are interdigitated within a single domain. New Biol. 2, 544-555
  16. Thiele, D. J. (1988) ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol. Cell. Biol. 8, 2745-2752 https://doi.org/10.1128/MCB.8.7.2745
  17. Culotta, V. C., Hsu, T., Hu, S., Furst, P. and Hamer, D. (1989) Copper and ACE1 regulatory protein reversibly induce yeast metallothionein gene transcription in a mouse extract. Proc. Natl. Acad. Sci. U.S.A. 86, 8377-8381 https://doi.org/10.1073/pnas.86.21.8377
  18. Evans, C. F., Engelke, D. R. and Thiele, D. J. (1990) ACE1 transcription factor produced in E. coli binds multiple regions within yeast metallothionein upstream activation sequences. Mol. Cell. Biol. 10, 426-429 https://doi.org/10.1128/MCB.10.1.426
  19. Thorvaldsen, J. L., Sewell, A. K., McGowen, C. L. and Winge, D. R. (1993) Regulation of metallothionein genes by the ACE1 and AMT1 transcription factors. J. Biol. Chem. 268, 12512-12518
  20. Culotta, V. C., Howard, W. R. and Liu, X. F. (1994) CRS5 encodes a metallothionein-like protein in Saccharomyces cerevisiae. J. Biol. Chem. 269, 25295-25302
  21. Gralla, E. B., Thiele, D. J., Silar, P. and Valentine, J. S. (1991) ACE1, a copper-dependent transcription factor, activates expression of the yeast copper zinc superoxide dismutase gene. Proc. Natl. Acad. Sci. U.S.A. 88, 8558-8562 https://doi.org/10.1073/pnas.88.19.8558
  22. Carri, M. T., Galiazzo, F., Ciriolo, M. R. and Rotilio, G. (1991) Evidence for co-regulation of Cu, Zn superoxide dismutase and metallothionein gene expression in yeast through transcriptional control by copper via the ACE1 factor. FEBS. Lett. 278, 263-266 https://doi.org/10.1016/0014-5793(91)80131-L
  23. Canessa, P., Alvarez, J. M., Polanco, R., Bull, P. and Vicuna, R. (2008) The copper-dependent ACE1 transcription factor activates the transcription of the mco1 gene from the basidiomycete Phanerochaete chrysosporium. Microbiology. 154, 491-499 https://doi.org/10.1099/mic.0.2007/013128-0
  24. Esterbauer, H., Schauer, R. J. and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free. Radical. Bio. Med. 11, 81-128 https://doi.org/10.1016/0891-5849(91)90192-6
  25. Fogel, S. and Welch, J. W. (1982) Tandem gene amplification mediates copper resistance in yeast. Proc. Natl. Acad. Sci. U.S.A. 79, 5342-5346 https://doi.org/10.1073/pnas.79.17.5342
  26. Fogel, S., Welch, J. W., Cathala, G. and Karin, M. (1983) Gene amplification in yeast. Development of copper resistance is mediated by an increase in CUPI gene copy number. Curr. Genet. 7, 1-9 https://doi.org/10.1007/BF00365673
  27. Welch, J. W., Fogel, S., Cathala, G. and Karin, M., (1983) Industrial yeasts display tandem gene iteration at the CUPI region. Mol. Cell. Biol. 3, 1353-1361 https://doi.org/10.1128/MCB.3.8.1353
  28. Casella, S., Frassinetti, S., Lupi, F. and Squartini, A. (1988) Effect of cadmium, chromium and copper on symbiotic and free-living Rhizobium leguminosarum biovar trifolii. FEMS. Microbiol. Lett. 49, 343-347 https://doi.org/10.1111/j.1574-6968.1988.tb02754.x
  29. Patsikka, E., Kairavuo, M., Sersen, F., Aro, E. M. and Tyystjarvi, E. (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant. Physiol. 129, 1359- 1367 https://doi.org/10.1104/pp.004788
  30. Boddi, B., Oravecz, A. R. and Lehoczki, E. (1995) Effect of cadmium on organization and photoreduction of protochlorophyllide in dark-grown leaves and etioplast inner membrane preparations of wheat. Photosynthetica. 31, 411-420
  31. Beale, S. I. (1999) Enzymes of chlorophyll biosynthesis. Photosynth. Res. 60, 43-73 https://doi.org/10.1023/A:1006297731456
  32. Pontier, D., Albrieux, C., Joyard, J., Lagrange, T. and Block, M. A. (2007) Knock-out of the magnesium protoporphyrin IX methyltransferase gene in Arabidopsis: effects on chloroplast development and on chloroplastto-nucleus signaling. J. Biol. Chem. 282, 2297-2304 https://doi.org/10.1074/jbc.M610286200
  33. Smirnoff, N. (1993) The role of active oxygen in the response of plants to water deficit and dessication. New Phytol. 125, 27-58 https://doi.org/10.1111/j.1469-8137.1993.tb03863.x
  34. Monk, L. S., Fagerstedt, K. V. and Crawford, R. M. M. (1989) Oxygen toxicity and superoxide dismutase as an antioxidant in physiological stress. Plant. Physiol. 76, 456-459 https://doi.org/10.1104/pp.76.2.456
  35. Chaoui, A., Mazhoudi, S., Ghorbal, M. N. and Ferjani, E. E. (1997) Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzymes activities in bean (Phaseolus vulgaris L.). Plant. Sci. 127, 139-147 https://doi.org/10.1016/S0168-9452(97)00115-5
  36. Zhu, B., Xiong, A. S., Peng, R. H., Xu, J., Zhou, J., Xu, J. T., Jin, X. F., Zhang, Y., Hou, X. L. and Yao, Q. H. (2008) Heat stress protection in Aspen sp1 transgenic Arabidopsis thaliana. BMB Rep. 41, 382-387
  37. Fang, W. and Kao, C. H. (2000) Enhanced peroxidase activity in rice leaves in responses to excess iron, copper and zinc. Plant. Sci. 158, 71-76 https://doi.org/10.1016/S0168-9452(00)00307-1
  38. Gupta, M., Cuypers, A., Vangronsveld, J. and Clijsters, H. (1999) Copper affects the enzymes of ascorbate-glutathione cycle and its related metabolites in the roots of Phaseolus vulgaris. Physiol. Plant. 106, 262-267 https://doi.org/10.1034/j.1399-3054.1999.106302.x
  39. Teisseire, H. and Guy, V. (2000) Copper-induced changes in antioxidant enzymes activities in fronds of duckweed (Lemna minor). Plant. Sci. 153, 65-72 https://doi.org/10.1016/S0168-9452(99)00257-5
  40. Becana, M., Moran, J. F. and Iturbe-Ormaetxe, I. (1998) Iron- dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection. Plant Soil. 201, 137-147 https://doi.org/10.1023/A:1004375732137
  41. Gallie, D. R., Sleat, D. E., Watts, J. W., Turner, P. C. and Wilson, T. M. A. (1987) The 5'-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic. Acids. Res.15, 3257-3273 https://doi.org/10.1093/nar/15.8.3257
  42. Zhang, X. and Henriques, R. and Lin, S. S. (2006) Agrobacteriummediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641-646 https://doi.org/10.1038/nprot.2006.97
  43. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497 https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
  44. Lichtenthaler, H. K. (1987) ChlorophyIIs and carotenoids: pigments of photosynthetic biomembranes. Meth. Enzymol. 148, 350-382 https://doi.org/10.1016/0076-6879(87)48036-1
  45. Heath, R. L. and Packer, L. (1968) Photoperoxidation in isolated chloroplast, I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 125, 180-198
  46. Beyer, W. F. and Fridovich, Y. (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Analytical biochemistry. 161, 559- 566 https://doi.org/10.1016/0003-2697(87)90489-1
  47. MacAdam, J. W., Nelson, C. J. and Sharp, R. E. (1992) Peroxidase activity in the leaf elongation zone of tall fescue, Plant. Physiol. 99, 872-878 https://doi.org/10.1104/pp.99.3.872

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