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ABC transporters of the wheat pathogen Mycosphaerella graminicola function as protectants against biotic and xenobiotic toxic compounds

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Abstract

We have studied the role of five ABC transporter genes ( MgAtr to MgAtr5) from the wheat pathogen Mycosphaerella graminicola in multidrug resistance (MDR). Complementation of Saccharomyces cerevisiae mutants with the ABC transporter genes from M. graminicola showed that all the genes tested encode proteins that provide protection against chemically unrelated compounds, indicating that their products function as multidrug transporters with distinct but overlapping substrate specificities. Their substrate range in yeast includes fungicides, plant metabolites, antibiotics, and a mycotoxin derived from Fusarium graminearum (diacetoxyscirpenol). Transformants of M. graminicola in which individual ABC transporter genes were deleted or disrupted did not exhibit clear-cut phenotypes, probably due to the functional redundancy of transporters with overlapping substrate specificity. Independently generated MgAtr5 deletion mutants of M. graminicola showed an increase in sensitivity to the putative wheat defence compound resorcinol and to the grape phytoalexin resveratrol, suggesting a role for this transporter in protecting the fungus against plant defence compounds. Bioassays with antagonistic bacteria indicated that MgAtr2 provides protection against metabolites produced by Pseudomonas fluorescens and Burkholderia cepacia. In summary, our results show that ABC transporters from M. graminicola play a role in protection against toxic compounds of natural and artificial origin.

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Acknowledgments

Dr. G.H.J. Kema and Dr. C. Waalwijk are acknowledged for discussions within the Wageningen Mycosphaerella group. We thank Prof. Dr. P.J.G. De Wit for critically reading the manuscript, Dr. T. Hohn (Syngenta) for the generous gift of diacetoxyscirpenol, Dr. J. Raaymakers for providing P. fluorescens Pf5 and B. cepacia B37W, and H. Schoonbeek for help and discussions on the bacterial bioassay. L-H. Zwiers was financially supported by Syngenta, Switzerland, I. Stergiopoulos by the Training and Mobility of Researchers (TMR) Programme (Marie Curie Research Grants) of the European Commission (Contract No. ERBFMBICT983558), and M.M.C. Gielkens and S.D. Goodall by the EU-BIOTECH 2 programme (Reference No. BIO4CT960352)

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Author notes

  1. M. M. C. Gielkens

    Present address: National Institute for Public Health and the Environment, P.O. Box 1, 3720 BA, Bilthoven, The Netherlands

  2. S. D. Goodall

    Present address: Galton Laboratory, Department of Biology, University College London, Wolfson House, 4 Stephenson Way, London, NW12 HE, UK

Authors and Affiliations

  1. Laboratory of Phytopathology, Department of Plant Sciences, Wageningen University, P.O. Box 8025, 6700 EE, Wageningen, The Netherlands

    L.-H. Zwiers, I. Stergiopoulos, M. M. C. Gielkens, S. D. Goodall & M. A. De Waard

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  1. L.-H. Zwiers
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Correspondence to M. A. De Waard.

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Communicated by C. A. M. J. J. van den Hondel

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Zwiers, LH., Stergiopoulos, I., Gielkens, M.M.C. et al. ABC transporters of the wheat pathogen Mycosphaerella graminicola function as protectants against biotic and xenobiotic toxic compounds. Mol Gen Genomics 269, 499–507 (2003). https://doi.org/10.1007/s00438-003-0855-x

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