Skip to main content

Advertisement

SpringerLink
Log in

Heavy metal and abiotic stress inducible metallothionein isoforms from Prosopis juliflora (SW) D.C. show differences in binding to heavy metals in vitro

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Prosopis juliflora is a tree species that grows well in heavy metal laden industrial sites and accumulates heavy metals. To understand the possible contribution of metallothioneins (MTs) in heavy metal accumulation in P. juliflora, we isolated and compared the metal binding ability of three different types of MTs (PjMT1-3). Glutathione S-transferase fusions of PjMTs (GSTMT1-3) were purified from Escherichia coli cells grown in the presence of 0.3 mM cadmium, copper or zinc. Analysis of metal bound fusion proteins using atomic absorption spectrometry showed that PjMT1 bound higher levels of all three heavy metals as compared to PjMT2 and PjMT3. A comparative analysis of the genomic regions (including promoter for all three PjMTs) is also presented. All three PjMTs are induced by H2O2 and ABA applications. PjMT1 and PjMT2 are induced by copper and zinc respectively while PjMT3 is induced by copper, zinc and cadmium. Variation in induction of PjMTs in response to metal exposure and their differential binding to metals suggests that each MT has a specific role in P. juliflora. Of the three MTs analyzed, PjMT1 shows maximum heavy metal sequestration and is thus a potential candidate for use in heavy metal phytoremediation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdullah SNA, Cheah SC, Murphy DJ (2002) Isolation and characterization of two divergent type 3 metallothioneins from oil palm, Elaeis guineenis. Plant Physiol Biochem 40:255–263

    Article  CAS  Google Scholar 

  • Akashi K, Nishimura N, Ishida Y, Yokota A (2004) Potent hydroxyl radical scavenging activity of drought-induced type-2 metallothionein in wild watermelon. Biochem Biophys Res Commun 323:72–78

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Bessega C, Saidman BO, Vilardi JC (2000) Isozyme and RAPD studies in Prosopis glandulosa and P. velutina (Leguinosae, Mimosoideae). Genet Mol Biol 23:639–648

    Article  CAS  Google Scholar 

  • Chen HJ, Hou WC, Yang CY, Huang DJ, Liu JS, Lin YH (2003) Molecular cloning of two metallothionein-like protein genes with differential expression patterns from sweet potato (Ipomoea batatas) leaves. J Plant Physiol 160:547–555

    Article  PubMed  CAS  Google Scholar 

  • Chyan CL, Lee TTT, Liu CP, Yang YC, Tzen JTC, Chou WM (2005) Cloning and expression of a seed-specific metallothionein-like protein from sesame. Biosci Biotechnol Biochem 69:2319–2325

    Article  PubMed  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182

    Article  PubMed  CAS  Google Scholar 

  • Coyle P, Philcox JC, Carey LC, Rofe AM (2002) Metallothionein: the multi purpose protein. Cell Mol Life Sci 59:627–647

    Article  PubMed  CAS  Google Scholar 

  • Evans IM, Gatehouse LN, Gatehouse JA, Robinson NJ, Croy RR (1990) A gene from pea (Pisum sativum L.) with homology to metallothionein genes. FEBS Lett 262:29–32

    Article  PubMed  CAS  Google Scholar 

  • Fabisiak JP, Borisenko GG, Liu SX, Tyurin VA, Pitt BR, Kagan VE (2002) Redox sensor function of metallothioneins. Methods Enzymol 353:268–281

    Article  PubMed  CAS  Google Scholar 

  • Garibaldi C (2003) Prosopis juliflora (Sw.) DC.657–659. http://www.rngr.net/Publications

  • Giordani T, Natali L, Maserti BE, Taddei S, Cavallini A (2000) Characterization and expression of DNA sequences encoding putative type II metallothioneins in the seagrass Posidinia oceanica. Plant Physiol 123:1571–1581

    Article  PubMed  CAS  Google Scholar 

  • Guo WJ, Bundithya W, Goldsborough PB (2003) Characterization of the Arabidopsis metallothionein gene family: tissue-specific expression and induction during senescence and in response to copper. New Phytol 159:369–381

    Article  CAS  Google Scholar 

  • Hamer DA (1986) Metallothionein. Annu Rev Biochem 55:913–951

    PubMed  CAS  Google Scholar 

  • Haq F, Mahoney M, Koropatnick J (2003) Signaling events for metallothionein induction. Mutat Res 523:211–226

    Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA element (PLACE) database. Nucleic Acids Res 27:297–300

    Article  PubMed  CAS  Google Scholar 

  • Kohler A, Blaudez D, Chalot M, Martin F (2004) Cloning and expression of multiple metallothioneins from hybrid poplar. New Phytol 164:83–93

    Article  CAS  Google Scholar 

  • Lee J, Shim D, Song WY, Hwang I, Lee Y (2004) Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Mol Biol 54:805–815

    Article  PubMed  CAS  Google Scholar 

  • Lu S, Gu H, Yuan X, Wang X, Wu A, Qu LJ, Liu JY (2006) The GUS reporter-aided analysis of the promoter activities of a rice metallothionein gene reveals different regulatory regions responsible for tissue-specific and inducible expression in transgenic Arabidopsis. Transgenic Res 16:177–191

    Article  PubMed  Google Scholar 

  • Ma M, Lau PS, Jia YT, Tsang WK, Lam KS, Tam FY, Wong YS (2003) The isolation and characterization of type 1 metallothionein (MT) cDNA from a heavy-metal-tolerant plant, Festuca rubra cv. Merlin. Plant Sci 164:51–60

    Article  CAS  Google Scholar 

  • Mett VL, Lochhead LP, Reynalds PH (1993) Copper-controllable gene expression system for whole plants. Proc Natl Acad Sci USA 90:4567–4571

    Article  PubMed  CAS  Google Scholar 

  • Mir G, Dome`nech J, Huguet G, Guo WJ, Goldsbrough P, Atrian S, Molinas M (2004) A plant type 2 metallothionein (MT) from cork tissue responds to oxidative stress. J Exp Bot 55:2483–2493

    Article  PubMed  CAS  Google Scholar 

  • Moyle R, Fairbairn DJ, Ripi J, Crowe M, Botella JR (2005) Developing pineapple fruit has a small transcriptome dominated by metallothionein. J Exp Bot 56:101–112

    PubMed  CAS  Google Scholar 

  • Ozturk ZN, Talamé V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573

    Article  CAS  Google Scholar 

  • Palmiter RD (1998) The elusive function of metallothioneins. Proc Natl Acad Sci USA 95:8428–8430

    Article  PubMed  CAS  Google Scholar 

  • Pasiecznik NM, Felker P, Harris PJC, Harsh LN, Cruz G, Tewari JC, Cadoret K, Maldonado LJ (2001) The Prosopis juliflora–Prosopis pallida complex: a monograph. HDRA, Coventry

    Google Scholar 

  • Quan XQ, Wang ZL, Zhang H, Bi YP (2007) Cloning and characterization of TsMT3, a type 3 metallothionein gene from salt cress (Thellungiella salsuginea). DNA Seq 13:1

    Google Scholar 

  • Rai UN, Pandey K, Sinha S, Singh A, Saxena R, Gupta DK (2004) Revegetating fly ash landfills with Prosopis juliflora L.: impact of different amendments and rhizobium inoculation. Environ Int 30:293–300

    Article  PubMed  CAS  Google Scholar 

  • Reynolds TL, Crawford RL (1996) Changes in abundance of an abscisic acid-responsive, early cysteine-labeled metallothionein transcript during pollen embryogenesis in bread wheat (Triticum aestivum). Plant Mol Biol 32:823–829

    Article  PubMed  CAS  Google Scholar 

  • Robinson NJ, Tommey AM, Kuske C, Jackson PJ (1993) Plant metallothioneins. Biochem J 295:1–10

    PubMed  CAS  Google Scholar 

  • Robinson NJ, Wilson JR, Turner JS (1996) Expression of the type 2 metallothionein-like gene MT2 from Arabidopsis thaliana in Zn2+ metallothionein deficient Synechococcus PCC 7942: putative role for MT2 in Zn2+ metabolism. Plant Mol Biol 30:1169–1179

    Article  PubMed  CAS  Google Scholar 

  • Roosens NH, Leplae R, Bernard C, Verbruggen N (2005) Variations in plant metallothioneins: the heavy metal hyperaccumulator Thlaspi caerulescens as a study case. Planta 222:716–729

    Article  PubMed  CAS  Google Scholar 

  • Senthilkumar P, Prince WSPM, Sivakumar S, Subbhuraam CV (2005) Prosopis julifora—a green solution to decontaminate heavy metal (Cu and Cd) contaminated soils. Chemosphere 60:1493–1496

    Article  PubMed  CAS  Google Scholar 

  • Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, Dietrich B, Ho P, Bacwaden J, Ko C, Clarke JD, Cotton D, Bullis D, Snell J, Miguel T, Hutchison D, Kimmerly B, Mitzel T, Katagiri F, Glazebrook J, Law M, Goff SA (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14:2985–2994

    Article  PubMed  CAS  Google Scholar 

  • Suja G, Venkataraman G, Parida A (2007) Identification of stress induced genes from drought tolerant plant Prosopis juliflora (Swartz) DC. through analysis of expressed sequence tags. Genome 50:470–478

    Article  Google Scholar 

  • Thangavel P, Subburam V, Shanmughavel P, Muthukumar T (2000) Prosopis juliflora—a metallophyte for the biorecovery of aluminium from urban industrial enclaves. XII IUFRO World Congress, Kola Lumpur

    Google Scholar 

  • Usha B, Prashanth SR, Parida A (2007) Differential expression of two metallothionein encoding genes during heavy metal stress in the mangrove species Avicennia marina (Forsk.) Vierh. Curr Sci 93:1215–1218

    CAS  Google Scholar 

  • Wenzel WW, Jockwer F (1999) Accumulation of heavy metals in plants grown on mineralized soils of the Australian Alps. Environ Pollut 104:145–155

    Article  CAS  Google Scholar 

  • Whitelaw CA, Le Huquet JA, Thurman DA, Tomsett AB (1997) The isolation and characterization of type II metallothionein-like genes from tomato(Lycopersicon esculentum L.). Plant Mol Biol 33:503–511

    Article  PubMed  CAS  Google Scholar 

  • Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol 135:1447–1456

    Article  PubMed  CAS  Google Scholar 

  • Yu LH, Liu JY, Umeda M, Uchimiya H (1998) Molecular characterization of metallothionein genes in plants. Plant Biotechnol 15:167–172

    CAS  Google Scholar 

  • Zhang YW, Tam NFY, Wong YS (2004) Cloning and characterization of type 2 metallothionein-like gene from a wetland plant, Typha latifolia. Plant Sci 167:869–877

    Article  CAS  Google Scholar 

  • Zhou J, Goldsbrough PB (1994) Functional homologs of animal and fungal metallothionein genes from Arabidopsis. Plant Cell 6:875–884

    Article  PubMed  CAS  Google Scholar 

  • Zhou GK, Xu YE, Liu JY (2005) Characterization of a rice class II metallothionein gene: tissue expression patterns and induction in response to abiotic factors. J Plant Physiol 162:686–696

    Article  PubMed  CAS  Google Scholar 

  • Zhou GK, Xu YF, Li J, Yang L, Liu JY (2006) Molecular analysis of the metallothionein gene family in rice (Oryza sativa L.). J Biochem Mol Biol 39:595–606

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from Department of Biotechnology, Government of India. Fellowship (JRF/SRF) provided to Usha by the Department of Biotechnology is gratefully acknowledged.

Author information

Authors and Affiliations

  1. M.S. Swaminathan Research Foundation, Third Cross Street, Taramani Institutional Area, Chennai, 600113, India

    B. Usha, Gayatri Venkataraman & Ajay Parida

Authors
  1. B. Usha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gayatri Venkataraman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ajay Parida
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ajay Parida.

Additional information

Communicated by R. Hagemann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Usha, B., Venkataraman, G. & Parida, A. Heavy metal and abiotic stress inducible metallothionein isoforms from Prosopis juliflora (SW) D.C. show differences in binding to heavy metals in vitro. Mol Genet Genomics 281, 99–108 (2009). https://doi.org/10.1007/s00438-008-0398-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-008-0398-2

Keywords

Search

Navigation