Evolution and function of phytochelatin synthases

Journal of Plant Physiology

Volumn 163, Issue 3, 2006, Pages 319-332

  Clemens, Stephan ^a  

^a LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

Glutathione; Metal homeostasis; Metal hyperaccumulation; Metal tolerance; Phytoremediation

Indexed keywords

DETOXIFICATION; ENZYMES; GENES; TISSUE; TOXICITY;

GLUTATHIONE; METAL HOMEOSTASIS; METAL HYPERACCUMULATION; METAL TOLERANCE; PHYTOREMEDIATION;

PROTEINS;

DETOXICATION; ENZYMES; GENES; METALS; PROTEINS; TISSUE; TOXICITY;

EUKARYOTA; FUNGI; NEMATODA; PROKARYOTA;

EID: 30944455261     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2005.11.010     Document Type: Article

References (66)

1. A. Beck, K. Lendzian, M. Oven, A. Christmann, and E. Grill Phytochelatin synthase catalyzes key step in turnover of glutathione conjugates Phytochemistry 62 2003 423 431
2. J. Berg, and Y. Shi The galvanization of biology: a growing appreciation for the roles of zinc Science 271 1996 1081 1085
3. A. Bush Metals and neuroscience Curr Opin Chem Biol 4 2000 184 191
4. A. Cazalé, and S. Clemens Arabidopsis thaliana expresses a second functional phytochelatin synthase FEBS Lett 507 2001 215 219
5. R. Chaney, M. Malik, Y.M. Li, S.L. Brown, E.P. Brewer, and J.S. Angle Phytoremediation of soil metals Curr Opin Biotechnol 8 1997 279 284
6. J. Chen, J. Zhou, and P.B. Goldsbrough Characterization of phytochelatin synthase from tomato Physiol Plant 101 1997 165 172
7. S. Clemens Molecular mechanisms of plant metal homeostasis and tolerance Planta 212 2001 475 486
8. S. Clemens, D.M. Antosiewicz, J.M. Ward, D.P. Schachtman, and J.I. Schroeder The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast Proc Natl Acad Sci USA 95 1998 12043 12048
9. S. Clemens, E.J. Kim, D. Neumann, and J.I. Schroeder Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast EMBO J 18 1999 3325 3333
10. S. Clemens, M.G. Palmgren, and U. Krämer A long way ahead: understanding and engineering plant metal accumulation Trends Plant Sci 7 2002 309 315
11. S. Clemens, J. Schroeder, and T. Degenkolb Caenorhabditis elegans expresses a functional phytochelatin synthase Eur J Biochem 268 2001 3640 3643
12. S. Clemens, C. Simm, and T. Maier Heavy metal binding proteins and peptides A. Steinbüchel S.R. Fahnestock Biopolymers, vol. 8: polyamides and complex proteinaceous materials II 2003 Wiley-VCH Weilheim 255 288
13. C. Cobbett Phytochelatins and their roles in heavy metal detoxification Plant Physiol 123 2000 825 833
14. C. Cobbett, and P. Goldsbrough Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis Annu Rev Plant Physiol Plant Mol Biol 53 2002 159 182
15. J.A. de Knecht, M. van Dillen, P.L.M. Koevoets, H. Schat, J.A.C. Verkleij, and W.H.O. Ernst Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris Plant Physiol 104 1994 255 261
16. L.A. Finney, and T.V. O'Halloran Transition metal speciation in the cell: insights from the chemistry of metal ion receptors Science 300 2003 931 936
17. J.J.R. Frausto da Silva, and R.J.P. Williams The biological chemistry of the elements 2nd ed 2001 Clarendon Press Oxford, UK
18. W. Gekeler, E. Grill, E.-L. Winnacker, and M.H. Zenk Survey of the plant kingdom for the ability to bind heavy metals through phytochelatins Z Naturforsch 44c 1989 361 369
19. J.M. Gong, D.A. Lee, and J.I. Schroeder Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis Proc Natl Acad Sci USA 100 2003 10118 10123
20. E. Grill, S. Löffler, E.-L. Winnacker, and M.H. Zenk Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gamma-glutamylcysteine dipeptidyl transpeptidase (phytochelatin synthase) Proc Natl Acad Sci USA 86 1989 6838 6842
21. E. Grill, J. Thumann, E.-L. Winnacker, and M.H. Zenk Induction of heavy-metal binding phytochelatins by inoculation of cell cultures in standard media Plant Cell Rep 7 1988 375 378
22. E. Grill, E.-L. Winnacker, and M.H. Zenk Phytochelatins: the principal heavy-metal complexing peptides of higher plants Science 230 1985 674 676
23. M. Guerinot The ZIP family of metal transporters Biochim Biophys Acta 1465 2000 190 198
24. S.B. Ha, A.P. Smith, R. Howden, W.M. Dietrich, S. Bugg, and M.J. O'Connell Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe Plant Cell 11 1999 1153 1163
25. B. Halliwell, and J.M.C. Gutteridge Role of free radicals and catalytic metal ions in human disease - an overview Methods Enzymol 186 1990 1 85
26. D. Hamer Metallothionein Annu Rev Biochem 55 1986 913 951
27. E. Harada, E. von Roepenack-Lahaye, and S. Clemens A cyanobacterial protein with similarity to phytochelatin synthases catalyzes the conversion of glutathione to gamma-glutamylcysteine and lacks phytochelatin synthase activity Phytochemistry 65 2004 3179 3185
28. J. Hartley-Whitaker, G. Ainsworth, R. Vooijs, W. Bookum, H. Schat, and A. Meharg Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus Plant Physiol 126 2001 299 306
29. R. Howden, C.R. Andersen, P.B. Goldsbrough, and C.S. Cobbett A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana Plant Physiol 107 1995 1067 1073
30. R. Howden, P.B. Goldsbrough, C.R. Andersen, and C.S. Cobbett Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient Plant Physiol 107 1995 1059 1066
31. G. Jackson, I. Murray, L. Hosszu, N. Gibbs, J. Waltho, and A. Clarke Location and properties of metal-binding sites on the human prion protein Proc Natl Acad Sci USA 98 2001 8531 8535
32. N. Kondo, K. Imai, M. Isobe, T. Goto, A. Murasugi, and C. Wada-Nakagawa Cadystin A and B, major unit peptides comprising cadmium binding peptides induced in a fission yeast - separation, revision of structures and synthesis Tetrahed Lett 25 1984 3869 3872
33. T. Lane, and F. Morel A biological function for cadmium in marine diatoms Proc Natl Acad Sci USA 97 2000 4627 4631
34. T.W. Lane, M.A. Saito, G.N. George, I.J. Pickering, R.C. Prince, and F.M. Morel Biochemistry: a cadmium enzyme from a marine diatom Nature 435 2005 42
35. S. Lee, and B.S. Kang Expression of Arabidopsis phytochelatin synthase 2 is too low to complement an AtPCS1-defective cad1-3 mutant Molec Cells 19 2005 81 87
36. S. Lee, J.S. Moon, T.S. Ko, D. Petros, P.B. Goldsbrough, and S.S. Korban Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress Plant Physiol 131 2003 656 663
37. S. Löffler, A. Hochberger, E. Grill, E.-L. Winnacker, and M.H. Zenk Termination of the phytochelatin synthase reaction through sequestration of heavy metals by the reaction product FEBS Lett 258 1989 42 46
38. T. Maier, C. Yu, G. Küllertz, and S. Clemens Localization and functional characterization of metal-binding sites in phytochelatin synthases Planta 218 2003 300 308
39. T. Maitani, H. Kubota, K. Sato, and T. Yamada The composition of metals bound to class III metallothionein (phytochelatin and its desglycyl peptide) induced by various metals in root cultures of Rubia tinctorum Plant Physiol 110 1996 1145 1150
40. D. Mendoza-Cozatl, H. Loza-Tavera, A. Hernandez-Navarro, and R. Moreno-Sanchez Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants FEMS Microbiol Rev 29 2005 653 671
41. D.H. Nies Efflux-mediated heavy metal resistance in prokaryotes FEMS Microbiol Rev 27 2003 313 339
42. T.V. O'Halloran, and V. Culotta Metallochaperones, an intracellular shuttle service for metal ions J Biol Chem 275 2000 25057 25060
43. D.F. Ortiz, L. Kreppel, D.M. Speiser, G. Scheel, G. McDonald, and D.W. Ow Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter EMBO J 11 1992 3491 3499
44. M. Oven, J. Page, M.H. Zenk, and T. Kutchan Molecular characterization of the homo-phytochelatin synthase of soybean Glycine max: relation to phytochelatin synthase J Biol Chem 277 2002 4747 4754
45. R. Palmiter The elusive function of metallothioneins Proc Natl Acad Sci USA 95 1998 8428 8430
46. I.T. Paulsen, and M.H.J. Saier A novel family of ubiquitous heavy metal ion transport proteins J Membr Biol 156 1997 99 103
47. Pomponi M, Censi V, Di Girolamo V, De Paolis A, di Toppi LS, Aromolo R, et al. Overexpression of Arabidopsis phytochelatin synthase in tobacco plants enhances Cd(2+) tolerance and accumulation but not translocation to the shoot. Planta 2005; DOI:10.1007/s00425-005-0073-3.
48. P.A. Rea, O.K. Vatamaniuk, and D.J. Rigden Weeds, worms, and more. Papain's long-lost cousin, phytochelatin synthase Plant Physiol 136 2004 2463 2474
49. N. Roosens, N. Verbruggen, P. Meerts, P. Ximenez-Embun, and J.A.C. Smith Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe Plant Cell Environ 26 2003 1657 1672
50. R. Ruotolo, A. Peracchi, A. Bolchi, G. Infusini, A. Amoresano, and S. Ottonello Domain organization of phytochelatin synthase: functional properties of truncated enzyme species identified by limited proteolysis J Biol Chem 279 2004 14686 14693
51. D.E. Salt, R.D. Smith, and I. Raskin Phytoremediation Annu Rev Plant Physiol Plant Mol Biol 49 1998 643 668
52. D.P. Schachtman, and J.I. Schroeder Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants Nature 370 1994 655 658
53. H. Schat, and M.M.A. Kalff Are phytochelatins involved in differential metal tolerance or do they merely reflect metal-imposed strain? Plant Physiol 99 1992 1475 1480
54. H. Schat, M. Llugany, R. Vooijs, J. Hartley-Whitaker, and P.M. Bleeker The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes J Exp Bot 53 2002 2381 2392
55. M. Schmöger, M. Oven, and E. Grill Detoxification of arsenic by phytochelatins in plants Plant Physiol 122 2000 793 801
56. M. Solioz, and C. Vulpe CPx-type ATPases: a class of P-type ATPases that pump heavy metals Trends Biochem Sci 21 1996 237 241
57. J. Steffens, D. Hunt, and B. Williams Accumulation of non-protein metal-binding polypeptides (gamma-glutamyl-cysteinyl)n-glycine in selected cadmium-resistant tomato cells J Biol Chem 261 1986 13879 13882
58. N. Tsuji, S. Nishikori, O. Iwabe, K. Shiraki, H. Miyasaka, and M. Takagi Characterization of phytochelatin synthase-like protein encoded by alr0975 from a prokaryote, Nostoc sp. PCC 7120 Biochem Biophys Res Commun 315 2004 751 755
59. O. Vatamaniuk, E. Bucher, J. Ward, and P. Rea A new pathway for heavy metal detoxification in animals. Phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans J Biol Chem 276 2001 20817 20820
60. O. Vatamaniuk, E. Bucher, J. Ward, and P. Rea Worms take the 'phyto' out of 'phytochelatins' Trends Biotechnol 20 2002 61 64
61. O. Vatamaniuk, S. Mari, Y. Lu, and P. Rea AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution Proc Natl Acad Sci USA 96 1999 7110 7115
62. O. Vatamaniuk, S. Mari, Y. Lu, and P. Rea Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. Blocked thiols are sufficient for PC synthase-catalyzed transpeptidation of glutathione and related thiol peptides J Biol Chem 275 2000 31451 31459
63. O.K. Vatamaniuk, E.A. Bucher, M.V. Sundaram, and P. Rea CeHMT-1, a putative phytochelatin transporter, is required for cadmium tolerance in Caenorhabditis elegans J Biol Chem 280 2005 23684 23690
64. O.K. Vatamaniuk, S. Mari, A. Lang, S. Chalasani, L.O. Demkiv, and P. Rea Phytochelatin synthase, a dipeptidyl transferase that undergoes multisite acylation with gamma-glutamylcysteine during catalysis. Stoichiometric and site-directed mutagenic analysis of AtPCS1-catalyzed phytochelatin synthesis J Biol Chem 279 2004 22449 22460
65. Vivares D, Arnoux P, Pignol D. A papain-like enzyme at work: native and acyl-enzyme intermediate structures in phytochelatin synthesis. Proc Natl Acad Sci USA (in press).
66. R. Wysocki, S. Clemens, D. Augustyniak, P. Golik, E. Maciaszczyk, and M.J. Tamas Metalloid tolerance based on phytochelatins is not functionally equivalent to the arsenite transporter Acr3p Biochem Biophy Res Commun 304 2003 293 300