Overexpression of AtATM3 in Brassica juncea confers enhanced heavy metal tolerance and accumulation

Plant Cell, Tissue and Organ Culture

Volumn 107, Issue 1, 2011, Pages 69-77

  Bhuiyan, Mohammed Shafi Ullah ^a   Min, Sung Ran ^a   Jeong, Won Joong ^a   Sultana, Sayeda ^b   Choi, Kwan Sam ^b   Lee, Youngsook ^c   Liu, Jang R ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Chungnam National University   (South Korea)

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

Author keywords

ABC transporter; AtATM3; Biomass; Brassica juncea; Phytoremediation

Indexed keywords

35S PROMOTER; A PLANTS; ABC TRANSPORTER; ARABIDOPSIS THALIANA; ATATM3; ATP-BINDING CASSETTE TRANSPORTERS; BRASSICA JUNCEA; CAULIFLOWER MOSAIC VIRUS; CONTAMINATED SOILS; EXPRESSION LEVELS; GENETIC TRANSFORMATION; GLUTATHIONE SYNTHETASE; HEAVY METAL STRESS; HEAVY METAL TOLERANCE; INDIAN MUSTARD; IRON HOMEOSTASIS; METAL TRANSPORTERS; MITOCHONDRIAL MEMBRANES; OVER-EXPRESSION; PHYTOCHELATIN SYNTHASE; PHYTOREMEDIATION; SHOOT TISSUE; TRANSGENIC PLANTS; TRANSGENIC SEEDLINGS; TRANSGENICS; WILD TYPES;

BIOMASS; BIOREMEDIATION; CADMIUM; CELL MEMBRANES; GENES; HEAVY METALS; METALS; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; TISSUE; VIRUSES;

SOIL POLLUTION;

AGROBACTERIUM; ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA; BRASSICA JUNCEA; CAULIFLOWER MOSAIC VIRUS; RHIZOBIUM;

EID: 80052801114     PISSN: 01676857     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11240-011-9958-y     Document Type: Article

References (58)

1. Belouchi A, Kwan T, Gros P (1997) Cloning and characterization of the OsNramp family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant Mol Biol 33: 1085-1092.
2. Bennet LE, Burkhead JL, Hale KL, Terry N, Pilon M, Pilon-Smits EAH (2003) Analysis of transgenic Indian mustard plants for phytoremediation of metal-contaminated mine tailings. J Environ Qual 32: 432-440.
3. Bhuiyan MSU, Min SR, Jeong WJ, Sultana S, Choi KS, Song WY, Lee Y, Lim YP, Liu JR (2011a) Overexpression of a yeast cadmium factor 1 (YCF1) enhances heavy metal tolerance and accumulation in Brassica juncea. Plant Cell Tiss Organ Cult 105: 85-91.
4. Bhuiyan MSU, Min SR, Jeong WJ, Sultana S, Choi KS, Lim YP, Song WY, Lee Y, Liu JR (2011b) An improved method for Agrobacterium-mediated genetic transformation from cotyledon explants of Brassica juncea. Plant Biotechnol 28: 17-23.
5. Blaylock MJ, Salt DE, Dushenkov S, Zakharova O, Gussman C, Kapulnik Y, Ensley BD, Raskin I (1997) Enhanced accumulation of Pb in Indian mustard by soil-applied chelating agent. Environ Sci Technol 31: 560-565.
6. Bovet L, Feller U, Martinoia E (2005) Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA sub-microarray approach. Environ Int 31: 263-267.
7. Clemens S, Palmgren MG, Kramer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7: 309-315.
8. Clemente R, Walker DJ, Bernal MP (2005) Uptake of heavy metals and As by Brassica juncea grown on contaminated soil in Aznalcollar (Spain): the effects of soil amendments. Environ Pollut 138: 46-58.
9. Curie C, Alonso JM, Le Jean M, Ecker JR, Briat JF (2000) Involvement of Nramp1 from Arabidopsis thaliana in iron transport. Biochem J 347: 749-755.
10. Darlington DE, Hung C-Y, Xie J (2009) Developing an Agrobacterium tumefaciens-mediated genetic transformation for a selenium-hyperaccumulator Astragalus racemosus. Plant Cell Tiss Organ Cult 99: 157-165.
11. Ebbs SD, Lssat MM, Brady DJ, Cornish J, Gordon R, Kochian LV (1997) Phytoextraction of cadmium and zinc from a contaminated site. J Environ Qual 26: 1424-1430.
12. Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucl Acid Res 19: 1349.
13. Epstein AL, Gussman CD, Blaylock MJ, Yermiyahu U, Huang JW, Kapulnik Y, Orser CS (1999) EDTA and Pb-EDTA accumulation in Brassica juncea grown in Pb-amended soil. Plant Soil 208: 87-94.
14. Farinati S, DalCorso G, Varotto S, Furini A (2010) The Brassica juncea BjCdR15, an ortholog of Arabidopsis TGA3, is a regulator of cadmium uptake, transport and accumulation in shoots and confers cadmium tolerance in transgenic plants. New Phytol 185: 964-978.
15. Fassel VA (1978) Quantitative elemental analyses by plasma emission spectroscopy. Science 202: 183-191.
16. Gasic K, Korban SS (2007) Transgenic Indian mustard (Brassica juncea) plants expressing an Arabidopsis phytochelatin synthase (AtPCS1) exhibit enhanced As and Cd tolerance. Plant Mol Biol 64: 361-369.
17. Ghnaya AB, Hourmant A, Cerantola S, Karvarec N, Cabon JY, Branchrad M, Charles B (2010) Influence of zinc on soluble carbohydrate and free amino acid levels in rapeseed plants regenerated in vitro in the presence of zinc. Plant Cell Tiss Organ Cult 102: 191-197.
18. Giller KE, Witter E, McGrath SP (1998) Toxicity of HMs to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30: 1389-1414.
19. Guan Z, Chai T, Zhang Y, Xu J, Wei W (2009) Enhancement of Cd tolerance in transgenic tobacco plants overexpressing a Cd-induced catalase cDNA. Chemosphere 76: 623-630.
20. Hirchi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124: 125-134.
21. Jiang W, Liu D, Hou W (2000) Hyperaccumulation of lead by roots, hypocotyls, and shoots of Brassica juncea. Biol Plantarum 43: 603-606.
22. Kim D, Gustin JL, Lahner B, Persans MW, Baek D, Yun DJ, Salt DE (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J 39: 237-251.
23. Kim D-Y, Bovet L, Kushnir S, Noh EW, Martinoia E, Lee Y (2006) AtATM3 is involved in heavy metal resistance in Arabidopsis. Plant Physiol 140: 922-932.
24. Kim D-Y, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J 50: 207-218.
25. Klein M, Burla B, Martinoia E (2006) The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett 580: 1112-1122.
26. Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in Zinc homeostasis. Plant Cell Physiol 45: 1749-1758.
27. Kramer U, Talke I, Hanikenne M (2007) Transition metal transport. FEBS Lett 581: 2263-2272.
28. Kumar A, Chakrabarti A, Ghanta S, Chattopadhyay S (2009) Agrobacterium-mediated genetic transformation of mint with E. coli gluatathione synthetase gene. Plant Cell Tiss Organ Cult 96: 117-126.
29. Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13: 89-100.
30. Lee S, Moon JS, Domier LL, Korban SS (2002) Molecular characterization of phytochelatin synthase expression in transgenic Arabidopsis. Plant Physiol Biochem 40: 1059-1066.
31. Lee M, Lee K, Lee J, Noh EW, Lee Y (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138: 589-596.
32. -ΔΔCT method. Methods 25: 402-408.
33. Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3: 153-162.
34. Meagher RB, Heaton ACP (2005) Strategies for the engineered phytoremediation of toxic element pollution: mercury and arsenic. J Ind Microbiol Biotechnol 32: 502-513.
35. 1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 597: 783-791.
36. Miyabe S, Izawa S, Inoue Y (2001) The Zrc1 is involved in zinc transport system between vacuole and cytosol in Saccharomyces cerevisiae. Biochem Biophys Res Commun 282: 79-83.
37. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol Plant 15: 473-497.
38. Muthukumar B, Yakubov B, Salt DE (2007) Transcriptional activation and localization of expression of Brassica juncea putative metal transport protein BjMTP1. BMC Plant Biol 7: 32. doi: 10. 1186/1471-2229-7-32.
39. Nriagu JO, Pacyna JM (1998) Quantitative assessment of worldwide contamination of air, water and soils with trace metals. Nature 333: 134-139.
40. Pilon-Smits EAH (1995) Phytoremediation. Annu Rev Plant Biol 56: 15-39.
41. Pilon-Smits EAH, Pilon M (2002) Phytoremediation of metals using transgenic plants. Crit Rev Plant Sci 21: 439-456.
42. Pilon-Smits EAH, Hwang S, Mel Lytle C, Zhu Y, Tai JC, Bravo RC, Chen YC, Leustek T, Terry N (1999) Overexpression of ATP Sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 1999: 123-132.
43. Raskin I, Smith RD, Salt DE (1997) Phytoremediation of metals: using plants to remove pollutants from the environment. Curr Opin Biotechnol 8: 221-226.
44. Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58: 347-375.
45. Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109: 1427-1433.
46. Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wiren N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281: 25532-25540.
47. Song W-Y, Sohn EJ, Martinoia E, Lee YJ, Yang Y-Y, Jasinski M, Forestier C, Hwang I, Lee Y (2003) Engineering tolerance and accumulation of lead and cadmium in transgenic plants. Nat Biotechnol 21: 914-919.
48. Steffens JC (1990) The heavy metal binding peptides of plants. Annu Rev Plant Physiol Plant Mol Biol 41: 553-575.
49. Teschner J, Lachmann N, Schulze J, Geisler M, Selbach K, Santamaria-Araujo J, Balk J, Mendel RR, Bittner F (2010) A novel role for Arabidopsis mitochondrial ABC transporter ATM3 in molybdenum cofactor biosynthesis. Plant Cell 22: 468-480.
50. Verret F, Gravot A, Auroy P, Leonhardt N, David P, Nussaume L, Vavasseur A, Richaud P (2004) Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance. FEBS Lett 576: 306-312.
51. Wangeline AL, Burkhead JL, Hale KL, Lindblom SD, Terry N, Pilon M, Pilon-Smits EAH (2004) Overexpression of ATP Sulfurylase in Indian mustard: effects on tolerance and accumulation of twelve metals. J Environ Qual 33: 54-60.
52. Weigel D, Glazebrook J (2002) Arabidopsis: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, pp 125-127.
53. Xu J, Zhang YX, Wei W, Han L, Guan ZQ, Cong L, Chai TY (2008) BjDHNs confer heavy-metal tolerance in plants. Mol Biotechnol 38: 91-98.
54. Xu J, Chai T, Zhang Y, Lang M, Han L (2009) The cation-efflux transporter BjCET2 mediates zinc and cadmium accumulation in Brassica juncea L. leaves. Plant Cell Rep 28: 1235-1242.
55. Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid digestion and multi-element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plan 18: 131-146.
56. Zhao S-J, Zhang Z-C, Gao X, Toshun G, Qiu B-S (2009) Plant regeneration of the mining ecotype Sedumalfredii and cadmium hyperaccumulation in regenerated plants. Plant Cell Tiss Organ Cult 99: 9-16.
57. Zhu YL, Pilon-Smits EAH, Jouanin L, Terry N (1999a) Overexpression of glutathione synthetase in Indian mustard enhances cadmium accumulation and tolerance. Plant Physiol 119: 73-79.
58. Zhu YL, Pilon-Smits EAH, Tarun AS, Weber SU, Jouanin L, Terry N (1999b) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121: 1169-1177.