Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators W inside box sign

Plant Cell

Volumn 16, Issue 8, 2004, Pages 2176-2191

  Freeman, John L ^a   Persans, Michael W ^a,c   Nieman, Ken ^a   Albrecht, Carrie ^a   Peer, Wendy ^a   Pickering, Ingrid J ^b,d   Salt, David E ^a  

^a PURDUE UNIVERSITY   (United States)

^b SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^c UNIVERSITY OF TEXAS PAN AMERICAN   (United States)

^d UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; BIOCHEMISTRY; BIOSYNTHESIS; METABOLISM; METALLOIDS; NICKEL; OXIDATION; SULFUR;

GLUTATHIONE; HYPERACCUMULATORS;

PLANT CELL CULTURE;

ACETYLATION; BIOCHEMISTRY; BIOSYNTHESIS; CELLS; METABOLISM; OXIDATION; SULFUR;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICACEAE; THLASPI; THLASPI ARVENSE; THLASPI GOESINGENSE; THLASPI OXYCERAS; THLASPI PERFOLIATUM; THLASPI ROSULARE;

EID: 3242697870     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.023036     Document Type: Article

References (85)

1. An, G., Watson, B.C., Stachel, S., Gordon, M.P., and Nester, E.W. (1985). New cloning vehicles for transformation of higher plants. EMBO J. 4, 277-284.
2. Assunção, A.G.L., Martins, P.D.C., Folter, S.D., Vooijs, R., Schat, H., and Aarts, M.G.M. (2001). Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ. 24, 217-226.
3. Assunção, A.G.L., Ten Bookum, W.M., Nelissen, H.J.M., Vooijs, R., Schat, H., and Ernst, W.H.O. (2003). A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caesrulescens. New Phytol. 159, 383-390.
4. Awazuhara, M., Hirai, M.Y., Hayshi, H., Chino, M., Naito, S., and Fujiwara, T. (2000). O-acetyl-L-serine content in rosette leaves of Arabidopsis thaliana affected by S and N nutrition. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants, C. Brunold, H. Rennenberg, L.J. De Kok, I. Stulen, and J.C. Davidian, eds (Bern, Switzerland: Paul Haupt), pp. 331-333.
5. Baccouch, S., Chaoui, A., and El Ferjani, E. (1998). Nickel-induced oxidative damage and antioxidant responses in Zea mays shoots. Plant Physiol. Biochem. 36, 689-694.
6. Becher, M., Talke, I.N., Krall, L., and Krämer, U. (2004). Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 37, 251-268.
7. Bert, V., Macnair, M.R., De Laguerie, P., Samumitou-Laprade, P., and Petit, D. (2000). Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Physiol. 146, 225-233.
8. Bert, V., Saumitou-Laprade, P., Salis, P., Gruber, W., and Verbruggen, N. (2003). Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri. Plant Soil 249, 9-18.
9. Błaszczyk, A., Brodzik, R., and Sirko, A. (1999). Increased resistance to oxidative stress in transgenic tobacco plants overexpressing bacterial serine acetyltransferase. Plant J. 20, 237-243.
10. Błaszczyk, A., Sirko, L., Hawkesford, M.J., and Sirko, A. (2002). Biochemical analysis of transgenic tobacco lines producing bacterial serine acetyltransferase. Plant Sci. 162, 589-597.
11. Bogdanova, N., and Hell, R. (1997). Cysteine synthesis in plants: Protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J. 11, 251-262.
12. Boominathan, R., and Doran, P.M. (2002). Ni-induced oxidative stress in roots of the Ni hyperaccumulator, Alyssum bertolonii. New Phytol. 156, 205-215.
13. Boyd, R.S., and Martens, S.N. (1998). Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae): A constitutive trait. Am. J. Bot. 85, 259-265.
14. Brooks, R.R., Lee, J., Reeves, R.D., and Jaffré, T. (1977). Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J. Geochem. Explor. 7, 49-77.
15. Byers, H.G. (1935). Selenium occurrence in certain soils in the United States, with a discussion of related topics. U.S. Dept. Agric. Tech. Bull. 482, 1-47.
16. Chardonnens, A.N., Koevoets, P.L.M., van Zanten, A., Schat, H., and Verkleij, J.A.C. (1999). Properties of enhanced tonoplast zinc transport in naturally selected zinc-tolerant Silene vulgaris. Plant Physiol. 120, 779-785.
17. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
18. Cobbett, C., and Goldsbrough, P. (2002). Phytochelatins and metallothioneins: Role in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 53, 159-182.
19. Cobbett, C.S. (2000). Phytochelatins and their role in heavy metal detoxification. Plant Physiol. 123, 825-832.
20. De Knecht, J.A., Koevoets, P.L.M., Verkleij, J.A.C., and Ernst, W.H.O. (1992). Evidence against a role for phytochelatins in naturally selected increased cadmium tolerance in Silene vulgaris (Moench) Garcke. New Phytol. 122, 681-688.
21. Ebbs, S., Lau, I., Ahner, B., and Kochian, L. (2002). Phytochelatins synthesis is not responsible for Cd tolerance in Zn/Cd hyperaccumulator Thlaspi caerulescens (J. & C. Presl). Planta 214, 635-640.
22. Foyer, C.H., Souriau, N., Perrer, S., Lelandais, M., Kunert, K.-J., Pruvost, C., and Jouanin, L. (1995). Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in Poplar trees. Plant Physiol. 109, 1047-1057.
23. Guerinot, M.L., and Salt, D.E. (2001). Fortified foods and phytoremediation: Two sides of the same coin. Plant Physiol. 125, 164-167.
24. 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, 1153-1163.
25. Harmens, H., Hartog, P.R.D., Ten Bookum, W.M.T., and Verkleij, J.A.C. (1993). Increased zinc tolerance in Silene vulgaris (Moench) Garcke is not due to increased production of phytochelatins. Plant Physiol. 103, 1305-1309.
26. Harms, K., von Ballmoos, P., Brunold, C., Hofgen, R., and Hesse, H. (2000). Expression of a bacterial serine acetyltransferase in transgenic potato plants leads to increased levels of cysteine and glutathione. Plant J. 22, 335-343.
27. Hell, R. (1997). Review: Molecular physiology of plant sulfur metabolism. Planta 202, 138-148.
28. Hesse, H., Harms, K., Von Ballmoos, P., Brunold, C., Willmitzer, L., and Höfgen, R. (2000). Serine acetyltransferase: A bottleneck for cysteine and glutathione synthesis. In Sulfur Nutrition and Sulfur Assimilation in Higher Plants, C. Brunold, H. Rennenberg, L.J. De Kok, I. Stulen, and J.C. Davidian, eds (Bern, Switzerland: Paul Haupt), pp. 321-323.
29. Hirai, M.Y., Fujiwara, T., Awazuhara, M., Kimura, T., Noji, M., and Saito, K. (2003). Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33, 651-663.
30. Howarth, J.R., Domínguez-Solís, J.R., Gutíerrez- Alcalá, G., Wray, J.L., Romero, L.C., and Gotor, C. (2003). The serine acetyltransferase family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Mol. Biol. 51, 589-598.
31. Howden, R., and Cobbett, C.S. (1992). Cadmium-sensitive mutants of Arabidopsis thaliana. Plant Physiol. 99, 100-107.
32. Howden, R., Goldbrough, P.B., Anderson, C.R., and Cobbett, C.S. (1995). Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol. 107, 1059-1066.
33. Inoue, K., Noji, M., and Saito, K. (1999). Determination of the sites required for the alloseric inhibition of serine acetyltransferase by L-cysteine in plants. Eur. J. Biochem. 266, 220-227.
34. Jaffré, T., Brooks, R.R., Lee, J., and Reeves, R.D. (1976). Sebertia acuminate: A hyperaccumulator of nickel from New Caledonia. Science 193, 579-580.
35. Krämer, U., Pickering, I.J., Prince, R.C., Raskin, I., and Salt, D.E. (2000). Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol. 122, 1343-1353.
36. Krämer, U., Smith, R.D., Wenzel, W., Raskin, I., and Salt, D.E. (1997). The role of nickel transport and tolerance in nickel hyperaccumulation by Thlaspi goesingense Hélácsy. Plant Physiol. 115, 1641-1650.
37. Küpper, H., Lombi, E., Zhao, F.-J., Wieshammer, G., and McGrath, S.P. (2001). Cellular compartmentalization of nickel in the hyperaccumulator Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J. Exp. Bot. 52, 2291-2300.
38. Lahner, B., Gong, J., Mahmoudian, M., Smith, E.L., Abid, K.B., Rogers, E.E., Guerinot, M.L., Harper, J.F., Ward, J.M., McIntyre, L., Schroeder, J.I., and Salt, D.E. (2003). Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat. Biotechnol. 21, 1215-1221.
39. -2 uptake, and oxidative stress response in intact canola roots. Plant Physiol. 114, 177-183.
40. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680-685.
41. Leustek, T. (2002). Sulfate metabolism. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Rockville, MD; American Society of Plant Biologists), doi/10.1199/tab.0017, http://www.aspb. org/publications/ arabidopsis/.
42. Luck, H. (1963). A spectrophotometric method for the estimation of catalase. In Methods of Enzymatic Analysis, H. Bergmeyer, ed (New York: Academic Press), pp. 886-887.
43. Macnair, M.R., Bert, V., Huitson, S.B., Saumitou-Laprade, P., and Petit, D. (1999). Zinc tolerance and hyperaccumulation are genetically independent characters. Proc. R. Soc. Lond. B Biol. Sci. 266, 2175-2179.
44. Meister, A. (1988). Glutathione metabolism and its selective modification. J. Biol. Chem. 263, 17205-17208.
45. Minguzzi, C., and Vergnano, O. (1948). II contenuto di nichel nelle ceneri di Alyssum bertolonii Desv. Mem. Soc. Tosc. Sci. Nat. Ser. A 55, 49-77.
46. Mullineaux, P., Creissen, G., Broadbent, P., Reynolds, H., Kular, B., and Wellburn, A. (1994). Elucidation of the role of glutathione reductase using transgenic plants. Biochem. Soc. Trans. 22, 931-936.
47. Mummenhoff, K., Franzke, A., and Koch, M. (1997). Molecular phyogenetics of Thlaspi s.l. (Brassicaceae) based on chloroplast DNA restriction site variation and sequences of the internal transcribed spacers of nuclear ribosomal DNA. Can. J. Bot. 75, 469-482.
48. Mummenhoff, K., and Koch, M. (1994). Chloroplast DNA restriction site variation and phylogenetic relationships in the genus Thlaspi sensu lato (Brassicaceae). Syst. Biol. 19, 73-88.
49. Mummenhoff, K., and Zunk, K. (1991). Should Thlaspi (Brassicaceae) be split? Preliminary evidence from isoelectric focusing analysis of Rubisco. Taxon 40, 427-434.
50. + from Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux. Plant Physiol. 121, 1375-1382.
51. Noctor, G., Strohm, M., Jouanin, L., Kunert, K.-J., Foyer, C.H., and Rennenberg, H. (1996). Synthesis of glutathione in leaves of transgenic poplar overexpressing γ-glutamylcysteien synthetase. Plant Physiol. 112, 1071-1078.
52. Noji, M., Inoue, K., Kimura, N., Gouda, A., and Saito, K. (1998). Isoform-dependant differences in feedback regulation and subcellular localization of serine acetyltransferase involved in cysteine biosynthesis from Arabidopsis thaliana. J. Biol. Chem. 273, 32739-32745.
53. Noji, M., Saito, M., Nakamura, M., Aono, M., Saji, H., and Saito, K. (2001). Cysteine synthase overexpression in tobacco confers tolerance to sulfur-containing environmental pollutants. Plant Physiol. 126, 973-980.
54. Peer, W.A., Mahmoudian, M., Lahner, B., Reeves, R.D., Murphy, A.S., and Salt, D.E. (2003). Identifying model metal hyperaccumulating plants: Germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol. 159, 421-430.
55. Pence, M.S., Larsen, P.B., Ebbs, S.D., Letham, D.L., Lasat, M.M., Garvin, D.F., Eide, D., and Kochian, L.V. (2000). The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc. Natl. Acad. Sci. USA 97, 4956-4960.
56. Persans, M.W., Nieman, K., and Salt, D.E. (2001). Identification of a novel family of metal transporters uniquely expressed in metal hyperaccumulating Thlaspi goesingense (Hálácsy). Proc. Natl. Acad. Sci. USA 98, 9995-10000.
57. Persans, M.W., Klange, Y., Patnoe, J.M.M.L., Krämer, U., and Salt, D.E. (1999). Molecular dissection of histidine's role in nickel hyperaccumulation in Thlaspi goesingense (Hálácsy). Plant Physiol. 121, 1-10.
58. Pickering, I.J., Prince, R.C., George, G.N., Rauser, W.E., Wickramasinghe, W.A., Watson, A.A., Dameron, C.T., Dance, I.G., Fairlie, D.P., and Salt, D.E. (1999). X-ray absorption spectroscopy of cadmium phytochelatin and model systems. Biochim. Biophys. Acta 1429, 351-364.
59. Pilon-Smits, E.A.H., Zhu, V.L., Sears, T., and Terry, N. (2000). Overexpression of glutathione reductase in Brassica juncea: Effects on cadmium accumulation and tolerance. Physiol. Plant 110, 455-460.
60. Randhawa, V., Zhou, F., Jin, X., Nalewajko, C., and Kushner, D. (2001). Role of oxidative stress and thiol antioxidant enzymes in nickel toxicity and resistance in strains of the green alga Scenedesmus acutus f. alternans. Can. J. Microbiol. 47, 987-993.
61. Reeves, R.D., and Baker, A.J.M. (1984). Studies on metal uptake by plants from serpentine and non-serpentine populations of Thlaspi goesingense Hálácsy (Cruciferae). New Phytol. 98, 191-204.
62. Reeves, R.D., and Baker, A.J.M. (2000). Phytoremediation of toxic metals. In Using Plants to Clean Up the Environment, I. Raskin and B.D. Ensley, eds (New York; John Wiley & Sons), pp. 193-229.
63. Reeves, R.D., and Brooks, R.R. (1983). European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc. J. Geochem. Explor. 18, 275-283.
64. Reeves, R.D., Schwartz, C., Morel, J.L., and Edmondson, J. (2001). Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int. J. Phytorem. 3, 145-172.
65. Rehr, J.J., Mustre de Leon, J., Zabinsky, S.I., and Albers, R.C. (1991). Theoretical X-ray absorption fine structure standards. J. Am. Chem. Soc. 113, 5135-5140.
66. Rhodes, D., Deal, L., Haworth, P., Jamieson, G.C., Reuter, C.C., and Ericson, M.C. (1986). Amino acid metabolism of Lemna minor L. I. Responses to methionine sulfoximine. Plant Physiol. 82, 1057-1062.
67. Sachs, J. (1865). Handbuch der Experimental-Physiologie der Pflanzen. Handbuch der Physiologischen Botanik. (W. Hofmeister, Engelmann, Leipzig), pp. 153-154.
68. Salt, D.E., Prince, R.C., Baker, A.J.M., Raskin, I., and Pickering, I.J. (1999). Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Env. Sci. Tech. 33, 713-717.
69. Schat, H., and Kalff, M.M.A. (1992). Are phytochelatins involved in differential metal tolerance or do they merely reflect metal-imposed strain? Plant Physiol. 99, 1475-1480.
70. Schat, H., Llugany, M., Vooijs, R., Hartley-Whitaker, J., and Bleeker, P.M. (2002). The role of phytochelatins and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. J. Exp. Bot. 53, 2381-2392.
71. Schützendübel, A., and Polle, A. (2002). Plant responses to abiotic stresses: Heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53, 1351-1365.
72. Smith, I.K., Vierheller, T.L., and Thorne, C.A. (1988). Assay of glutathione reductase in crude tissue homogenates using 5,5′-dithiobis(2- nitrobenzoic acid). Anal. Biochem. 175, 408-413.
73. 4 units in cadmium phytochelatin complexes from EXAFS spectroscopy. J. Chem. Soc. Chem. Commun. 16, 1129-1130.
74. Strohm, M., Jouanin, L., Kunert, K.-J., Pruvost, C., Polle, A., Foyer, C.H., and Rennenberg, H. (1995). Regulation of glutathione synthesis in leaves of transgenic polar (Populus tremula x P. alba) overexpressing glutathione synthetase. Plant J. 7, 141-145.
75. Tsakraklides, G., Martin, M., Chalam, R., Tarczynski, M., Schmidt, M., and Leustek, T. (2002). Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J. 32, 879-889.
76. Vacchina, V., Mari, S., Czernic, P., Marquès, L., Pianelli, K., Schaumlöffel, D., Lebrun, M., and Łobiński, R. (2003). Speciation of nickel in a hyperaccumulating plant by high-performance liquid chromatography-inductively coupled plasma mass spectroscopy and electrospray MS/MS assisted by cloning using yeast complementation. Anal. Chem. 75, 2740-2745.
77. Van Hoof, N.A., Koevoets, P.L., Hakvoort, H.W., Ten Bookum, W.M., Schat, H., Verkleij, J.A., and Ernst, W.H.O. (2001). Enhanced ATP-dependent copper efflux across the root cell plasma membrane in copper-tolerant Silene vulgaris. Physiol. Plant 113, 225-232.
78. Vatamaniuk, O.K., Mari, S., Lu, Y.-P., and Rea, P.A. (2000). Mechanism of heavy metal ion activation of phytochelatin (PC) synthase. J. Biol. Chem. 275, 31451-31459.
79. Weber, M., Harada, E., Vess, C., Roepenack-Lahaye, E.V., and Clemens, S. (2004). Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37, 269-281.
80. Wenzel, W.W., and Jockwer, F. (1999). Accumulation of heavy metals in plants grown on mineralized soils of the Austrian Alps. Environ. Pollut. 104, 145-155.
81. Wirtz, M., and Hell, R. (2002). Production of cysteine for bacterial and plant biotechnology. Application of cysteine feedback-insensitive isoforms of serine acetyltransferase. Amino Acids 24, 195-203.
82. Yoo, B.C., and Harmon, A.C. (1997). Regulation of recombinant soybean serine acetyltransferase by CDPK. Plant Physiol. 114 (suppl.), 267.
83. Youssefian, S., Nakamura, M., Orudgev, E., and Kondo, N. (2001). Increased cysteine biosynthesis capacity in transgenic tobacco over expressing an O-acetylserine(thiol) lyase modifies plant responses to oxidative stress. Plant Physiol. 126, 1001-1011.
84. Zacchini, M., Rea, E., Tullio, M., and de Agazio, M. (2003). Increased antioxidative capacity in maize calli during and after oxidative stress induced by a long lead treatment. Plant Physiol. Biochem. 41, 49-54.
85. Zunk, K., Mummenhoff, K., Koch, M., and Hurka, H. (1996). Phytogenetic relationships of Thlaspi s.l. (subtribe Thlaspidinae, Lepidieae) and allied genera based on chloroplast DNA restriction-site variation. Theor. Appl. Genet. 92, 375-381.