Skip to main content
SpringerLink
Log in

Gene expression profiling of a Zn-tolerant and a Zn-sensitive Suillus luteus isolate exposed to increased external zinc concentrations

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Complementary DNA (cDNA)-amplified fragment-length polymorphism (AFLP) was applied to analyze transcript profiles of a Zn-tolerant and a Zn-sensitive isolate of the ectomycorrhizal basidiomycete Suillus luteus, both cultured with and without increased external zinc concentrations. From the obtained transcript profiles that covered approximately 2% of the total expected complement of genes in S. luteus, 144 nonredundant, differentially expressed transcript-derived fragments (TDFs), falling in different classes of expression pattern, were isolated and sequenced. Thirty-six of the represented genes showed homology to function-known genes, whereas 6 matched unknown protein coding sequences, and 102 were possibly novel. Although relatively few TDFs were found to be responsive to the different zinc treatments, their modulated expression levels may suggest a different transcriptional response to zinc treatments in both isolates. Among the identified genes that could be related to heavy-metal detoxification or the tolerance trait were genes encoding for homologues of a heat-shock protein, a putative metal transporter, a hydrophobin, and several proteins involved in ubiquitin-dependent proteolysis.

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

Similar content being viewed by others

References

  • Adriaensen K, Vrålstad T, Noben JP, Vangronsveld J, Colpaert JV (2005) Copper-adapted Suillus luteus, a symbiotic solution for pines colonising Cu mine spoils. Appl Environ Microbiol 11:7279–7284

    Article  Google Scholar 

  • Adriaensen K, Vangronsveld J, Colpaert JV (2006) Zinc-tolerant Suillus bovinus improves growth of Zn-exposed Pinus sylvestris seedlings. Mycorrhiza 16:553–558

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bachem CW, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M, Visser RG (1996) Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J 9:745–753

    Article  CAS  PubMed  Google Scholar 

  • Bachem CW, Oomen RJF, Visser RG (1998) Transcript imaging with cDNA–AFLP: a step-by-step protocol. Plant Mol Biol Rep 16:157–173

    Article  CAS  Google Scholar 

  • Breyne P, Zabeau M (2001) Genome-wide expression analysis of plant cell cycle modulated genes. Curr Opin Plant Biol 4:136–142

    Article  CAS  PubMed  Google Scholar 

  • Cabiscol E, Belli G, Tamarit J, Echave P, Herrero E, Ros J (2002) Mitochondrial Hsp60, resistance to oxidative stress, and the labile iron pool are closely connected in Saccharomyces cerevisiae. J Biol Chem 277:44531–44538

    Article  CAS  PubMed  Google Scholar 

  • Chondrogianni N, Tzavelas C, Pemberton AJ, Nezis IP, Rivett AJ, Gonos ES (2005) Overexpression of a proteasome β5 subunit increases the amount of assembled proteasome and confers ameliorated response to oxidative stress and higher survival rates. J Biol Chem 280:11840–11850

    Article  CAS  PubMed  Google Scholar 

  • Colpaert JV, Vandenkoornhuyse P, Adriaensen K, Vangronsveld J (2000) Genetic variation and heavy metal tolerance in the ectomycorrhizal basidiomycete Suillus luteus. New Phytol 147:367–379

    Article  CAS  Google Scholar 

  • Colpaert JV, Muller LAH, Lambaerts M, Adriaensen K, Vangronsveld J (2004) Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytol 162:549–560

    Article  CAS  Google Scholar 

  • Colpaert JV, Adriaensen K, Muller LAH, Lambaerts M, Faes C, Carleer R, Vangronsveld J (2005) Element profiles and growth in Zn-sensitive and Zn-resistant Suilloid fungi. Mycorrhiza 15:628–634

    Article  CAS  PubMed  Google Scholar 

  • Ditt RF, Nester RW, Comai L (2001) Plant gene expression response to Agrobacterium tumefaciens. Proc Natl Acad Sci USA 98:10954–10959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JDG (2000) cDNA–AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12:963–977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frost MR, Guggenheim JA (1999) Prevention of depurination during elution facilitates the re-amplification of DNA from differential display gels. Nucleic Acids Res 27:e6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujs S, Gazdag Z, Poljsak B, Stibilj V, Milacic R, Pesti M, Raspor P, Batic M (2005) The oxidative stress response of the yeast Candida intermedia to copper, zinc, and selenium exposure. J Basic Microbiol 45:125–135

    Article  CAS  PubMed  Google Scholar 

  • Godon C, Langniel G, Lee J, Buhler JM, Kieffer S, Perrot M, Boucherie H, Toledano MB, Labarre J (1998) The H2O2 stimulon in Saccharomyces cerevisiae. J Biol Chem 273:22480–22489

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Heuchel R, Radtke F, Georgiev O, Stark M, Aguet M, Schaffner W (1994) The transcription factor MTF-1 is essential for basal and heavy metal-induced metallothionein gene expression. EMBO J 13:2870–2875

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jacob C, Courbot M, Brun A, Steinman HM, Jacquot JP, Botton B, Chalot M (2001) Molecular cloning, characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus. Eur J Biochem 268:3223–3232

    Article  CAS  PubMed  Google Scholar 

  • Joseph P, Lei Y-X, Whong W-Z, Ong TM (2002) Oncogenic potential of mouse translation elongation factor-1δ, a novel cadmium-responsive proto-oncogene. J Biol Chem 277:6131–6136

    Article  CAS  PubMed  Google Scholar 

  • Kupfer DM, Reece CA, Clifton SW, Roe BA, Prade RA (1997) Multicellular ascomycetous fungal genomes contain more than 8000 genes. Fungal Genet Biol 21:364–372

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Godon C, Langniel G, Spector D, Garin J, Labarre J, Toledano MB (1999) Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem 274:16040–16046

    Article  CAS  PubMed  Google Scholar 

  • Lee SH, Kim BG, Kim KJ, Lee JS, Yun DW, Hahn JH, Kim GH, Lee KH, Suh DS, Kwon ST, Lee CS, Yoo YB (2002) Comparative analysis of sequences expressed during the liquid-cultured mycelia and fruit body stages of Pleurotus ostreatus. Fungal Genet Biol 35:115–134

    Article  CAS  PubMed  Google Scholar 

  • Le Quéré A, Johansson T, Tunlid A (2002) Size and complexity of the nuclear genome of the ectomycorrhizal fungus Paxillus involutus. Fungal Genet Biol. 36:234–241

    Article  PubMed  Google Scholar 

  • Marrs KA (1996) The function and regulation of glutathione S-transferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158

    Article  CAS  PubMed  Google Scholar 

  • Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genet Res 23:23–35

    Article  Google Scholar 

  • Muller LAH, Lambaerts M, Vangronsveld J, Colpaert JV (2004) AFLP-based assessment of the effects of environmental heavy metal pollution on the genetic structure of pioneer populations of Suillus luteus. New Phytol 164:297–303

    Article  CAS  Google Scholar 

  • Ospina-Giraldo MD, Collopy PD, Romaine CP, Royse DJ (2000) Classification of sequences expressed during the primordial and basidiome stages of the cultivated mushroom Agaricus bisporus. Fungal Genet Biol 29:81–94

    Article  CAS  PubMed  Google Scholar 

  • Pawlik-Skowroñńska B, Sanitaà di Toppi L, Favali MA, Fossati F, Pirszel J, Skowroñski T (2002) Lichens respond to heavy metals by phytochelatin synthesis. New Phytol 156:95–102

    Article  Google Scholar 

  • Quesada H, Ramiréz UEM, Rozas J, Aguadé M (2003) Large-scale adaptive hitchhiking upon high recombination in Drosophila simulans. Genetics 165:895–900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosen R, Büttner K, Becher D, Nakahigashi K, Yura T, Hecker M, Ron EZ (2002) Heat shock proteome of Agrobacterium tumefaciens: evidence for new control systems. J Bacteriol 184:1772–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roxas VP, Lohdi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41:1229–1234

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky JH (1996) Primer3. http://www-genome.wi.mit.edu/genome_software/other.primer3.html

  • Skinner W, Keon J, Hargreaves J (2001) Gene information for fungal plant pathogens from expressed sequences. Curr Opin Microbiol 4:381–386

    Article  CAS  PubMed  Google Scholar 

  • Townsend JP, Cavalieri D, Hartl DL (2003) Population genetic variation in genome-wide gene expression. Mol Biol Evol 20:955–963

    Article  CAS  PubMed  Google Scholar 

  • Vallino M, Drogo V, Abba’ S, Perotto S (2005) Gene expression of the ericoid mycorrhizal fungus Oidiodendron maius in the presence of high zinc concentrations. Mycorrhiza 15:333–344

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Environmental Biology Group, Centre for Environmental Sciences, Hasselt University, Agoralaan, Gebouw D, 3590, Diepenbeek, Belgium

    L. A. H. Muller, J. Ruytinx, M. Lambaerts, J. Vangronsveld & J. V. Colpaert

  2. Laboratoire de Physiologie et de Génétique Moléculaire des Plantes, Université Libre de Bruxelles, 1050, Brussels, Belgium

    A. R. Craciun & N. Verbruggen

  3. Department of Molecular Genetics and Microbiology, Duke University Medical Center, DUMC Box 3020, Durham, NC, 27710, USA

    L. A. H. Muller

Authors
  1. L. A. H. Muller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. R. Craciun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Ruytinx
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Lambaerts
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. Verbruggen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Vangronsveld
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. V. Colpaert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. V. Colpaert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muller, L.A.H., Craciun, A.R., Ruytinx, J. et al. Gene expression profiling of a Zn-tolerant and a Zn-sensitive Suillus luteus isolate exposed to increased external zinc concentrations. Mycorrhiza 17, 571–580 (2007). https://doi.org/10.1007/s00572-007-0134-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-007-0134-5

Keywords

Search

Navigation