Skip to main content
SpringerLink
Log in

A transporter for abiotic stress and plant metabolite resistance in the ectomycorrhizal fungus Tricholoma vaccinum

  • Alteration and element mobility at the microbe-mineral interface
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Fungi exposed to toxic substances including heavy metals, xenobiotics, or secondary metabolites formed by co-occurring plants or other microorganisms require a detoxification system provided by exporters of several classes of transmembrane proteins. In case of mycorrhiza, plant metabolites need to be exported at the plant interface, while the extraradical hyphae may prevent heavy metal uptake, thus acting as a biofilter to the host plant at high environmental concentrations. One major family of such transporter proteins is the multidrug and toxic compound extrusion (MATE) class, a member of which, Mte1, was studied in the ectomycorrhizal fungus Tricholoma vaccinum. Phylogenetic analyses placed the protein in a subgroup of basidiomycete MATE sequences. The gene mte1 was found to be induced during symbiotic interaction. It mediated detoxification of xenobiotics and metal ions such as Cu, Li, Al, and Ni, as well as secondary plant metabolites if heterologously expressed in Saccharomyces cerevisiae.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Agerer R (2001) Exploration types of ectomycorrhizae: a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114

    Article  Google Scholar 

  • Arita A, Zhou X, Ellen TP, Liu X, Bai J, Rooney JP, Kurtz A, Klein CB, Dai W, Begley TJ, Costa M (2009) A genome-wide deletion mutant screen identifies pathways affected by nickel sulfate in Saccharomyces cerevisiae. BMC Genomics 10:524

    Article  Google Scholar 

  • Asensio J, Ruiz-Argüeso T, Rodríguez-Navarro A (1976) Sensitivity of yeasts to lithium. Anton van Lee J M S 42:1–8

    Article  CAS  Google Scholar 

  • Asiimwe T, Krause K, Schlunk I, Kothe E (2012) Modulation of ethanol stress tolerance by aldehyde dehydrogenase in the mycorrhizal fungus Tricholoma vaccinum. Mycorrhiza 22:471–484

    Article  CAS  Google Scholar 

  • Burse A, Weingart H, Ullrich MS (2004) NorM, an Erwinia amylovora multidrug efflux pump involved in in vitro competition with other epiphytic bacteria. AEM 70:693–703

    Article  CAS  Google Scholar 

  • Cannon RD, Lamping E, Holmes AR, Niimi K, Baret PV, Keniya MV, Tanabe K, Niimi M, Goffeau A, Monk BC (2009) Efflux-mediated antifungal drug resistance. Clin Microbiol Rev 22:291–321

    Article  CAS  Google Scholar 

  • de Waard MA, Andrade AC, Hayashi K, Schoonbeek HJ, Stergiopoulos I, Zwiers LH (2006) Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manag Sci 62:195–207

    Article  Google Scholar 

  • Del Sorbo G, Schoonbeek H, De Waard MA (2000) Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet Biol 30:1–15

    Article  Google Scholar 

  • Dichtl B, Stevens A, Tollervey D (1997) Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J 16:7184–7195

    Article  CAS  Google Scholar 

  • Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    Article  CAS  Google Scholar 

  • Fischer R, Timberlake WE (1995) Aspergillus nidulans apsA (anucleate primary sterigmata) encodes a coiled-coil protein required for nuclear positioning and completion of asexual development. J Cell Biol 128:485–498

    Article  CAS  Google Scholar 

  • Frohman MA (1993) Rapid amplification of complementary DNA ends for generation of full-length complementary DNAs: thermal RACE. Method Enzymol 218:340–356

    Article  CAS  Google Scholar 

  • Gherghel F, Krause K (2012) Role of mycorrhiza in re-forestation at heavy metal-contaminated sites. In: Kothe E and Varma A (eds) Bio-geo interactions in metal-contaminated soils, soil biology 31, Springer, Berlin, Heidelberg, pp 183–199

  • Gietz RD, Schiestl RH, Willems AR, Woods RA (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11:355–360

    Article  CAS  Google Scholar 

  • González-Guerrero M, Benabdellah K, Valderas A, Azcón-Aguilar C, Ferrol N (2010) GintABC1 encodes a putative ABC transporter of the MRP subfamily induced by Cu, Cd, and oxidative stress in Glomus intraradices. Mycorrhiza 20:137–146

    Article  Google Scholar 

  • Gorfer M, Persak H, Berger H, Brynda S, Bandian D, Strauss J (2009) Identification of heavy metal regulated genes from the root associated ascomycete Cadophora finlandica using a genomic microarray. Mycol Res 113:1377–1388

    Article  CAS  Google Scholar 

  • Hall JL (2001) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  Google Scholar 

  • Huda MN, Morita Y, Kuroda T, Mizushima T, Tsuchiya T (2001) Na+-driven multidrug efflux pump VcmA from Vibrio cholerae non-O1, a non-halophilic bacterium. FEMS Microbiol Lett 203:235–239

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  Google Scholar 

  • Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou XF, Saier MH Jr (2003) The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Bioch 270:799–813

    Article  CAS  Google Scholar 

  • Kottke I, Guttenberger M, Hampp R, Oberwinkler F (1987) An in vitro method for establishing mycorrhiza on coniferous seedlings. Trees 1:191–194

    Article  Google Scholar 

  • Krause K, Kothe E (2006) Use of RNA fingerprinting to identify fungal genes specifically expressed during ectomycorrhizal interaction. J Basic Microb 46:387–399

    Article  CAS  Google Scholar 

  • Kuroda T, Tsuchiya T (2009) Multidrug efflux transporters in the MATE family. Biochim Biophys Acta 1794:763–768

    Article  CAS  Google Scholar 

  • Magalhaes JV (2010) How a microbial drug transporter became essential for crop cultivation on acid soils: aluminum tolerance conferred by the multidrug and toxic compound extrusion (MATE) family. Ann Bot 106:199–203

    Article  CAS  Google Scholar 

  • Mankel A, Kost G, Kothe E (1998) Re-evaluation of the phylogenetic relationship among species of the genus Tricholoma. Microbiol Res 153:377–388

    Article  Google Scholar 

  • Martin F, Kohler A, Duplessis S (2007) Living in harmony in the wood underground: ectomycorrhizal genomics. Curr Opin Plant Biol 10:204–210

    Article  CAS  Google Scholar 

  • Matsumoto T, Kanamoto T, Otsuka M, Omote H, Moriyama Y (2009) Role of glutamate residues in substrate recognition by human MATE1 polyspecific H+/organic cation exporter. Am J Physiol Cell Ph 294:C1074–1078

  • Morita Y, Kodama K, Shiota S, Mine T, Kataoka A, Mizushima T, Tsuchiya T (1998) NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Ch 42:1778–1782

    CAS  Google Scholar 

  • Morita Y, Kataoka A, Shiota S, Mizushima T, Tsuchiya T (2000) NorM of Vibrio parahaemolyticus is an Na+-driven multidrug efflux pump. J Bacteriol 182:6694–6697

    Article  CAS  Google Scholar 

  • Morita M, Shitan N, Sawada K, van Montagu MC, Inzé D, Rischer H, Goossens A, Oksman-Caldentey KM, Moriyama Y, Yazaki K (2009) Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc Natl Acad Sci U S A 106:2447–2452

    Article  CAS  Google Scholar 

  • Moriyama Y, Hiasa M, Matsumoto T, Omote H (2008) Multidrug and toxic compound extrusion (MATE)-type proteins as anchor transporters for the excretion of metabolic waste products and xenobiotics. Xenobiotica 38:1107–1118

    Article  CAS  Google Scholar 

  • Nehls U, Göhringer F, Wittulsky S, Dietz S (2010) Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biol 12:292–301

    Article  CAS  Google Scholar 

  • Omote H, Hiasa M, Matsumoto T, Otsuka M, Moriyama Y (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci 27:587–593

    Article  CAS  Google Scholar 

  • Paumi CM, Chuk M, Snider J, Stagljar I, Michaelis S (2009) ABC transporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily. Microbiol Mol Biol R 73:577–593

    Article  CAS  Google Scholar 

  • Penninckx M (2000) A short review on the role of glutathione in the response of yeasts to nutritional, environmental, and oxidative stresses. Enzyme Microb Technol 26:737–742

    Article  CAS  Google Scholar 

  • Perrone GG, Grant CM, Daws IW (2005) Genetic and environmental factors influencing glutathione homeostasis in Saccharomyces cerevisiae. Mol Biol Cell 16:218–230

    Article  CAS  Google Scholar 

  • Pócsi I, Prade RA, Penninckx MJ (2004) Glutathione, altruistic metabolite in fungi. Adv Microb Physiol 49:1–76

    Article  Google Scholar 

  • Rieger S (1995) Veränderungen des Monoterpenspektrums in verletzten Fichtenwurzeln und ihre potentielle Bedeutung für die Resistenz gegenüber Heterobasidion annosum. Eur J Forest Pathol 25:367–380

    Article  Google Scholar 

  • Rozman D, Komel R (1994) Isolation of genomic DNA from filamentous fungi with high glucan level. Bio Tech 16:382

    CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning—a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

  • Shaefer B (1995) Revolution in rapid amplification of cDNA ends: new strategies for polymerase chain reaction cloning of full-length cDNA ends. Anal Biochem 227:255–273

    Article  Google Scholar 

  • Shiomi N, Fukuda H, Fukuda Y, Murata K, Kimura A (1991) Nucleotide sequence and characterization of a gene conferring resistance to ethionine in yeast Saccharomyces cerevisiae. J Ferment Bioeng 71:211–215

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, New York

    Google Scholar 

  • Zhao J, Dixon RA (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 21:2323–2340

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by the German Research Foundation with Graduate School 214. We want to thank Prof. H. Deising from the Martin Luther University Halle-Wittenberg for discussion and supply with fungicide substances and Dr. C Hertweck and Dr. Michael Ramm from the Hans Knöll Institute, Jena, for the supply with secondary metabolites.

Author information

Authors and Affiliations

  1. Institute of Microbiology, Microbial Communication, Friedrich Schiller University, Neugasse 25, 07743, Jena, Germany

    Ines Schlunk, Katrin Krause, Sophia Wirth & Erika Kothe

Authors
  1. Ines Schlunk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katrin Krause
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sophia Wirth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Erika Kothe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erika Kothe.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 10553 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schlunk, I., Krause, K., Wirth, S. et al. A transporter for abiotic stress and plant metabolite resistance in the ectomycorrhizal fungus Tricholoma vaccinum . Environ Sci Pollut Res 22, 19384–19393 (2015). https://doi.org/10.1007/s11356-014-4044-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-4044-8

Keywords

Search

Navigation