1887

Abstract

A non-mycoparasitic restriction enzyme-mediated DNA integration (REMI) mutant of (R2427) contains two tandem plasmid copies integrated towards the 3′ end of an ORF. The predicted polypeptide (845 aa) exhibits high similarity with DNA-helicase proteins from other filamentous fungi and yeasts that play a role in mitochondrial DNA maintenance and repair. Disruption of the DNA helicase gene results in altered morphology, reduced growth rates and a concomitant loss in ability to mycoparasitize sclerotia of . In infection bioassays, R2427 exhibited sparse mycelial growth on the surface of live sclerotia, but no mycelia were detected inside the sclerotia. Conversely, R2427 readily colonized autoclaved sclerotia. Complementation of the mutant with wild-type restored normal mycelial growth and mycoparasitic capability, confirming a functional role in the host–pathogen interaction. The DNA helicase may maintain mitochondrial stability in response to reactive oxygen species, either produced endogenously within the mycoparasite, or exogenously from the sclerotial host.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/017020-0
2008-06-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/6/1628.html?itemId=/content/journal/micro/10.1099/mic.0.2008/017020-0&mimeType=html&fmt=ahah

References

  1. Apel, K. & Hirt, H. ( 2004; ). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55, 373–399.[CrossRef]
    [Google Scholar]
  2. BalhadÉre, P. V., Foster, A. J. & Talbot, N. J. ( 1999; ). Identification of pathogenicity mutants of the rice blast fungus Magnaporthe grisea by insertional mutagenesis. Mol Plant Microbe Interact 12, 129–142.[CrossRef]
    [Google Scholar]
  3. Bessler, J. B., Torres, J. Z. & Zakian, V. A. ( 2001; ). The Pif1p subfamily of helicases: region-specific DNA helicases? Trends Cell Biol 11, 60–65.[CrossRef]
    [Google Scholar]
  4. Boland, G. J. & Hall, R. ( 1994; ). Index of plant hosts of Sclerotinia sclerotiorum. Can J Plant Pathol 16, 93–108.[CrossRef]
    [Google Scholar]
  5. Budge, S. P. & Whipps, J. M. ( 2001; ). Potential for integrated control of Sclerotinia sclerotiorum in glasshouse lettuce using Coniothyrium minitans and reduced fungicide application. Phytopathology 91, 221–227.[CrossRef]
    [Google Scholar]
  6. Budge, S. P., McQuilken, M. P., Fenlon, J. S. & Whipps, J. M. ( 1995; ). Use of Coniothyrium minitans and Gliocladium virens for biological-control of Sclerotinia sclerotiorum in glasshouse lettuce. Biol Control 5, 513–522.[CrossRef]
    [Google Scholar]
  7. Challen, M. P., Kerrigan, R. W. & Callac, P. ( 2003; ). A phylogenetic reconstruction and emendation of Agaricus section Duploannulatae. Mycologia 95, 61–73.[CrossRef]
    [Google Scholar]
  8. Chen, C. & Dickman, M. B. ( 2005; ). Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci U S A 102, 3459–3464.[CrossRef]
    [Google Scholar]
  9. Doudican, N. A., Song, B. W., Shadel, G. S. & Doetsch, P. W. ( 2005; ). Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol Cell Biol 25, 5196–5204.[CrossRef]
    [Google Scholar]
  10. Escande, A. R., Laich, F. S. & Pedraza, M. V. ( 2002; ). Field testing of honeybee-dispersed Trichoderma spp. to manage sunflower head rot (Sclerotinia sclerotiorum). Plant Pathol 51, 346–351.[CrossRef]
    [Google Scholar]
  11. Felsenstein, J. ( 1993; ). phylip (phylogeny inference package), version 3.5c. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.
  12. Foury, F. & Lahaye, A. ( 1987; ). Cloning and sequencing of the Pif gene involved in repair and recombination of yeast mitochondrial-DNA. EMBO J 6, 1441–1449.
    [Google Scholar]
  13. Georgiou, C. D., Tairis, N. & Polycratis, A. ( 2001; ). Production of beta-carotene by Sclerotinia sclerotiorum and its role in sclerotium differentiation. Mycol Res 105, 1110–1115.[CrossRef]
    [Google Scholar]
  14. Gerlagh, M., Whipps, J. M., Budge, S. P. & Goossen van de Geijn, H. M. ( 1996; ). Efficiency of isolates of Coniothyrium minitans as mycoparasites of Sclerotinia sclerotiorum, Sclerotium cepivorum and Botrytis cinerea on tomato stem pieces. Eur J Plant Pathol 102, 787–793.[CrossRef]
    [Google Scholar]
  15. Giczey, G., Kerenyi, Z., Fulop, L. & Hornok, L. ( 2001; ). Expression of cmg1, an exo-beta-1,3-glucanase gene from Coniothyrium minitans, increases during sclerotial parasitism. Appl Environ Microbiol 67, 865–871.[CrossRef]
    [Google Scholar]
  16. Harmsen, M. C., Schuren, F. H. J., Moukha, S. M., van Zuilen, C. M., Punt, P. J. & Wessels, J. G. H. ( 1992; ). Sequence analysis of the glyceraldehyde-3-phosphate dehydrogenase genes from the basidiomycetes Schizophyllum commune, Phanerochaete chrysosporium and Agaricus bisporus. Curr Genet 22, 447–454.[CrossRef]
    [Google Scholar]
  17. Huang, H. C. & Hoes, J. A. ( 1976; ). Penetration and infection of Sclerotinia sclerotiorum by Coniothyrium minitans. Can J Bot 54, 406–410.[CrossRef]
    [Google Scholar]
  18. Huang, H. C. & Kokko, E. G. ( 1987; ). Ultrastructure of hyperparasitism of Coniothyrium minitans on sclerotia of Sclerotinia sclerotiorum. Can J Bot 65, 2483–2489.[CrossRef]
    [Google Scholar]
  19. Huang, H. C., Bremer, E., Hynes, R. K. & Erickson, R. S. ( 2000; ). Foliar application of fungal biocontrol agents for the control of white mold of dry bean caused by Sclerotinia sclerotiorum. Biol Control 18, 270–276.[CrossRef]
    [Google Scholar]
  20. Ivessa, A. S., Zhou, J. Q. & Zakian, V. A. ( 2000; ). The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100, 479–489.[CrossRef]
    [Google Scholar]
  21. Jones, D. & Watson, D. ( 1969; ). Parasitism and lysis by soil fungi of Sclerotinia sclerotiorum (Lib.) de Bary, a phytopathogenic fungus. Nature 224, 287–288.[CrossRef]
    [Google Scholar]
  22. Jones, D., Gordon, A. H. & Bacon, J. S. D. ( 1974; ). Co-operative action by endo- and exo-β-(1→3)-glucanases from parasitic fungi in degradation of cell-wall glucans of Sclerotinia sclerotiorum (Lib) Bary. Biochem J 140, 47–55.
    [Google Scholar]
  23. Jones, E., Carpenter, M., Fong, D., Goldstein, A., Thrush, A., Crowhurst, R. & Stewart, A. ( 1999; ). Co-transformation of the sclerotial mycoparasite Coniothyrium minitans with hygromycin B resistance and beta-glucuronidase markers. Mycol Res 103, 929–937.[CrossRef]
    [Google Scholar]
  24. Kahmann, R. & Basse, C. ( 1999; ). REMI (Restriction Enzyme Mediated Integration) and its impact on the isolation of pathogenicity genes in fungi attacking plants. Eur J Plant Pathol 105, 221–229.[CrossRef]
    [Google Scholar]
  25. Li, G. Q., Huang, H. C. & Acharya, S. N. ( 2003; ). Importance of pollen and senescent petals in the suppression of alfalfa blossom blight (Sclerotinia sclerotiorum) by Coniothyrium minitans. Biocontrol Sci Technol 13, 495–505.[CrossRef]
    [Google Scholar]
  26. Muthumeenakshi, S., Sreenivasaprasad, S., Rogers, C. W., Challen, M. P. & Whipps, J. M. ( 2007; ). Analysis of cDNA transcripts from Coniothyrium minitans reveals a diverse array of genes involved in key processes during sclerotial mycoparasitism. Fungal Genet Biol 44, 1262–1284.[CrossRef]
    [Google Scholar]
  27. Nicholas, K. B., Nicholas, H. B. J. & Deerfield, D. W. ( 1997; ). GeneDoc: analysis and visualization of genetic variation. EMBNEWS 4, 14
    [Google Scholar]
  28. O'Rourke, T. W., Doudican, N. A., Mackereth, M. D., Doetsch, P. W. & Shadel, G. S. ( 2002; ). Mitochondrial dysfunction due to oxidative mitochondrial DNA damage is reduced through cooperative actions of diverse proteins. Mol Cell Biol 22, 4086–4093.[CrossRef]
    [Google Scholar]
  29. Punt, P. J., Oliver, R. P., Dingemanse, M. A., Pouwels, P. H. & van den Hondel, C. A. M. J. J. ( 1987; ). Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56, 117–124.[CrossRef]
    [Google Scholar]
  30. Rogers, C. W. ( 2004; ). Molecular approaches towards the identification of pathogenicity genes in the mycoparasite Coniothyrium minitans. PhD thesis, University of Birmingham, 245pp.
  31. Rogers, C. W., Challen, M. P., Green, J. R. & Whipps, J. M. ( 2004; ). Use of REMI and Agrobacterium-mediated transformation to identify pathogenicity mutants of the biocontrol fungus, Coniothyrium minitans. FEMS Microbiol Lett 241, 207–214.[CrossRef]
    [Google Scholar]
  32. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  33. Savoie, J.-M. & Largeteau, M. L. ( 2004; ). Hydrogen peroxide concentrations detected in Agaricus bisporus sporocarps and relation with their susceptibility to the pathogen Verticillium fungicola. FEMS Microbiol Lett 237, 311–315.
    [Google Scholar]
  34. Schulz, V. P. & Zakian, V. A. ( 1994; ). The Saccharomyces Pif1 DNA helicase inhibits telomere elongation and de-novo telomere formation. Cell 76, 145–155.[CrossRef]
    [Google Scholar]
  35. Schuren, F. H. J. & Wessels, J. G. H. ( 1994; ). Highly efficient transformation of the homobasidiomycete Schizophyllum commune to phleomycin resistance. Curr Genet 26, 179–183.[CrossRef]
    [Google Scholar]
  36. Schuren, F. H. J. & Wessels, J. G. H. ( 1998; ). Expression of heterologous genes in Schizophyllum commune is often hampered by the formation of truncated transcripts. Curr Genet 33, 151–156.[CrossRef]
    [Google Scholar]
  37. Seong, K., Hou, Z. M., Tracy, M., Kistler, H. C. & Xu, J. R. ( 2005; ). Random insertional mutagenesis identifies genes associated with virulence in the wheat scab fungus Fusarium graminearum. Phytopathology 95, 744–750.[CrossRef]
    [Google Scholar]
  38. Son, D. O., Satsu, H. & Shimizu, M. ( 2005; ). Histidine inhibits oxidative stress- and TNF-alpha-induced interleukin-8 secretion in intestinal epithelial cells. FEBS Lett 579, 4671–4677.[CrossRef]
    [Google Scholar]
  39. Whipps, J. M. & Gerlagh, M. ( 1992; ). Biology of Coniothyrium minitans and its potential for use in disease biocontrol. Mycol Res 96, 897–907.[CrossRef]
    [Google Scholar]
  40. Willetts, H. J. & Wong, J. A. L. ( 1980; ). The biology of Sclerotinia sclerotiorum, S. trifoliorum, and S. minor with emphasis on specific nomenclature. Bot Rev 46, 101–165.[CrossRef]
    [Google Scholar]
  41. Yakes, F. M. & Van Houten, B. ( 1997; ). Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 94, 514–519.[CrossRef]
    [Google Scholar]
  42. Zhang, D. H., Zhou, B., Huang, Y., Xu, L. X. & Zhou, J. Q. ( 2006; ). The human Pif1 helicase, a potential Escherichia coli RecD homologue, inhibits telomerase activity. Nucleic Acids Res 34, 1393–1404.[CrossRef]
    [Google Scholar]
  43. Zhou, J. Q., Monson, E. K., Teng, S. C., Schulz, V. P. & Zakian, V. A. ( 2000; ). Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 289, 771–774.[CrossRef]
    [Google Scholar]
  44. Zhou, J.-Q., Qi, H., Schulz, V. P., Mateyak, M. K., Monson, E. K. & Zakian, V. A. ( 2002; ). Schizosaccharomyces pombe pfh1+ encodes an essential 5′ to 3′ DNA helicase that is a member of the PIF1 subfamily of DNA helicases. Mol Biol Cell 13, 2180–2191.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/017020-0
Loading
/content/journal/micro/10.1099/mic.0.2008/017020-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error