Combined expression of the Arabidopsis metallothionein MT2b and the heavy metal transporting ATPase HMA4 enhances cadmium tolerance and the root to shoot translocation of cadmium and zinc in tobacco

Environmental and Experimental Botany

Volumn 72, Issue 1, 2011, Pages 71-76

  Grispen, Veerle M J ^a   Hakvoort, Henk W J ^a   Bliek, Tijs ^a   Verkleij, Jos A C ^a   Schat, Henk ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

AtHMA4; AtMT2b; Cadmium; Ectopic expression; Nicotiana tabacum; Tolerance and root to shoot translocation; Zinc

Indexed keywords

CADMIUM; DICOTYLEDON; NUTRIENT UPTAKE; PHENOTYPE; SYNERGISM; TOBACCO; VIRUS; ZINC;

ARABIDOPSIS; CAULIFLOWER MOSAIC VIRUS; NICOTIANA TABACUM;

EID: 79955086670     PISSN: 00988472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.envexpbot.2010.01.005     Document Type: Article

References (28)

1. Assuncao A.G.L., Pieper B., Vromans J., Lindhout P., Aarts M.G.M., Schat H. Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytologist 2006, 170(1):21-32.
2. Becher M., Talke I.N., Krall L., Kramer U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. The Plant Journal 2004, 37(2):251-268.
3. Courbot M., Willems G., Motte P., Arvidsson S., Roosens N., Saumitou-Laprade P., Verbruggen N. A major QTL for Cd tolerance in Arabidopsis halleri co-localizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiology 2007, 144(2):1052-1065.
4. Deniau A.X., Pieper B., Ten Bookum W.M., Lindhout P., Aarts M.G.M., Schat H. QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theoretical and Applied Genetics 2006, 113(5):907-920.
5. Grispen V.M.J., Irtelli B., Hakvoort H.W.J., Vooijs R., Bliek T., ten Bookum W.M., Verkleij J.A.C., Schat H. Expression of the Arabidopsis metallothionein 2b enhances arsenite sensitivity and root to shoot translocation in tobacco. Environmental and Experimental Botany 2009, 66(1):69-73.
6. Halpin C. Gene stacking in transgenic plants-the challenge for 21st century plant biotechnology. Plant Biotechnology Journal 2005, 3(2):141-155.
7. Hammond J.P., Bowen H.C., White P.J., Mills V., Pyke K.A., Baker A.J.M., Whiting S.N., May S.T., Broadley M.R. A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytologist 2006, 170(2):239-260.
8. Hanikenne M., Talke I.N., Haydon M.J., Lanz C., Nolte A., Motte P., Kroymann J., Weigel D., Kramer U. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 2008, 453(7193):391-395.
9. Hassinen V.H., Tuomainen M., Peraniemi S., Schat H., Karenlampi S.O., Tervahauta A.I. Metallothioneins 2 and 3 contribute to the metal-adapted phenotype but are not directly linked to Zn accumulation in the metal hyperaccumulator, Thlaspi caerulescens. Journal of Experimental Botany 2009, 60(1):187-196.
10. Hussain D., Haydon M.J., Wang Y., Wong E., Sherson S.M., Young J., Camakaris J., Harper J.F., Cobbett C.S. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 2004, 16(5):1327-1339.
11. Jack E., Hakvoort H.W.J., Reumer A., Verkleij J.A.C., Schat H., Ernst W.H.O. Real-time PCR analysis of metallothionein-2b expression in metallicolous and non-metallicolous populations of Silene vulgaris (Moench) Garcke. Environmental and Experimental Botany 2007, 59(1):84-91.
12. Karimi M., Inze D., Depicker A. GATEWAY (TM) vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 2002, 7(5):193-195.
13. Meagher R.B., Heaton A.C.P. Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic. Journal of Industrial Microbiology & Biotechnology 2005, 32(11-12):502-513.
14. Mengoni A., Gonnelli C., Hakvoort H.W.J., Galardi F., Bazzicalupo M., Gabbrielli R., Schat H. Evolution of copper-tolerance and increased expression of a 2b-type metallothionein gene in Silene paradoxa L. populations. Plant and Soil 2003, 257(2):451-457.
15. Mills R.F., Francini A., da Rocha P., Baccarini P.J., Aylett M., Krijger G.C., Williams L.E. The plant P-1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. Febs Letters 2005, 579(3):783-791.
16. Papoyan A., Kochian L.V. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance, characterization of a novel heavy metal transporting ATPase. Plant Physiology 2004, 136(3):3814-3823.
17. Pilon-Smits E., Pilon M. Phytoremediation of metals using transgenic plants. Critical Reviews in Plant Sciences 2002, 21(5):439-456.
18. Rugh C.L. Genetically engineered phytoremediation: one man's trash is another man's transgene. Trends in Biotechnology 2004, 22(10):496-498.
19. Schat H., Ten Bookum W.M. Genetic-control of copper tolerance in Silene vulgaris. Heredity 1992, 68:219-229.
20. Sokal R.R., Rohlf F.J. Biometry 1981, Freeman, San Francisco. 2nd ed.
21. Talke I.N., Hanikenne M., Kramer U. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiology 2006, 142(1):148-167.
22. van de Mortel J.E., Almar Villanueva L., Schat H., Kwekkeboom J., Coughlan S., Moerland P.D., Ver Loren van Themaat E., Koornneef M., Aarts M.G.M. Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiology 2006, 142(3):1127-1147.
23. van Hoof N.A.L.M., Hassinen V.H., Hakvoort H.W.J., Ballintijn K.F., Schat H., Verkleij J.A.C., Ernst W.H.O., Karenlampi S.O., Tervahauta A.I. Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiology 2001, 126(4):1519-1526.
24. Verbruggen N., Hermans C., Schat H. Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist 2009, 181(4):759-776.
25. Verret F., Gravot A., Auroy P., Leonhardt N., David P., Nussaume L., Vavasseur A., Richaud P. Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Letters 2004, 576(3):306-312.
26. Willems G., Drager D., Courbot M., Gode C., Verbruggen N., Saumitou-Laprade P. The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 2007, 176(1):659-674.
27. Wojas S., Clemens S., Hennig J., Skodowska A., Kopera E., Schat H., Bal W., Antosiewicz D.M. Overexpression of phytochelatin synthase in tobacco: distinctive effects of AtPCS1 and CePCS genes on plant response to cadmium. Journal of Experimental Botany 2008, 59(8):2205-2219.
28. Zhou J.M., Goldsbrough P.B. Arabidopsis metallothionein genes are functional in Saccharomyces cerevisiae. Plant Physiology 1993, 102(1):30-130.