Skip to main content
SpringerLink
Log in

Existence of different physiological forms within genetically diverse strains of Ampelomyces quisqualis

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

Powdery mildew fungi are parasitized by strains of the genetically distinct Ampelomyces quisqualis. To investigate whether differences in the phylogeny and other cultural, morphological and physiological characteristics of these different strains are related to differences in their geographic origins or the host species from which they were isolated, several A. quisqualis strains isolated from different species of Erysiphaceae collected in different countries and possessing different ITS rDNA sequences were selected and characterized. The results revealed some significant variation among the selected strains, which provides evidence for the existence of different physiological forms within the A. quisqualis species. Two groups that display differential growth on artificial media were identified. These groups also differ in the morphology of their mycelium, but not in the morphology of their pycnidia and conidia. Temperature greatly affected the in vitro growth of the A. quisqualis strains and growth rate was closely correlated to colony color. Differences in the conidial germination of distinct strains were observed during the recognition phase of the parasitic relationship. The germination of each of the investigated strains was greatly stimulated by all of the examined powdery mildew species and not only by the conidia of their original hosts. An Italian strain isolated from grapevine in the Trentino Alto-Adige region was identified as the strain that germinates the most quickly in the presence of powdery mildew conidia. Phylogenetic analysis revealed that these A. quisqualis strains can be classified into five different genetic groups, which generally correlate with the fungal host of origin and morphological and growth characteristics.

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

  • Angeli, D., Pellegrini, E., Micheli, S., Ress, D., Maurhofer, M., Pertot, I., et al. (2009a). Molecular characterization of Ampelomyces spp. strains from different hosts and geographic origins and evaluation of their potential to control powdery mildew of cucumber. IOBC/WPRS Bulletin, 43, 40–44.

    Google Scholar 

  • Angeli, D., Pellegrini, E., & Pertot, I. (2009b). Occurrence of Erysiphe necator chasmothecia and their natural parasitization by Ampelomyces quisqualis. Phytopathology, 99, 704–710.

    Article  Google Scholar 

  • Bélanger, R. R., & Labbé, C. (2002). Control of powdery mildews without chemicals: prophylactic and biological alternatives for horticultural crops. In R. R. Bélanger, W. R. Bushnell, A. J. Dik, & T. L. W. Carver (Eds.), The powdery mildews: a comprehensive treatise (pp. 256–267). St. Paul, MN, USA: APS Press.

    Google Scholar 

  • Belsare, S. W., Moniz, L., & Deo, V. B. (1980). The hyperparasite Ampelomyces quisqualis Ces. from Maharashtra State, India. Biovigyanam, 6, 173–176.

    Google Scholar 

  • Falk, S. P., Gadoury, D. M., Cortesi, P., Pearson, R. C., & Seem, R. C. (1995a). Parasitism of Uncinula necator cleistothecia by the mycoparasite Ampelomyces quisqualis. Phytopathology, 85, 794–800.

    Article  Google Scholar 

  • Falk, S. P., Gadoury, D. M., Pearson, R. C., & Seem, R. C. (1995b). Partial control of grape powdery mildew by the mycoparasite Ampelomyces quisqualis. Plant Disease, 79, 483–490.

    Article  Google Scholar 

  • Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113–118.

    Article  PubMed  CAS  Google Scholar 

  • Gu, Y. H., & Ko, W. H. (1997). Water agarose medium for studying factors affecting germination of conidia of Ampelomyces quisqualis. Mycological Research, 101, 422–424.

    Article  Google Scholar 

  • Hashioka, Y., & Nakai, Y. (1980). Ultrastructure of pycnidial development and mycoparasitism of Ampelomyces quisqualis parasitic on Erysiphales. Transactions of the Mycological Society of Japan, 21, 329–338.

    Google Scholar 

  • Jarvis, W. R., & Slingsby, K. (1997). The control of powdery mildew of greenhouse cucumber by water spray and Ampelomyces quisqualis. Plant Disease Reporter, 61, 728–730.

    Google Scholar 

  • Kiss, L. (1997). Genetic diversity in Ampelomyces isolates, hyperparasites of powdery mildew fungi, inferred from RFLP analysis of the rDNA ITS region. Mycological Research, 101, 1073–1080.

    Article  CAS  Google Scholar 

  • Kiss, L. (1998). Natural occurrence of Ampelomyces intracellular mycoparasites in mycelia of powdery mildew fungi. The New Phytologist, 140, 709–714.

    Article  Google Scholar 

  • Kiss, L. (2003). A review of fungal antagonists of powdery mildews and their potential as biocontrol agents. Pest Management Science, 59, 475–483.

    Article  PubMed  CAS  Google Scholar 

  • Kiss, L., & Nakasone, K. K. (1998). Ribosomal DNA internal transcribed spacer sequences do not support the species status of Ampelomyces quisqualis, a hyperparasite of powdery mildew fungi. Current Genetics, 33, 362–367.

    Article  PubMed  CAS  Google Scholar 

  • Kiss, L., Pintye, A., Kovacs, G. M., Jankovics, T., Fontaine, M. C., Harvey, N., et al. (2011). Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi. Molecular Ecology, 20, 1492–1507.

    Article  PubMed  Google Scholar 

  • Kiss, L., Pintye, A., Zséli, G., Jankovics, T., Szentivànyi, O., Hafez, Y. M., et al. (2009). Microcyclic conidiogenesis in powdery mildews and its association with intracellular parasitism by Ampelomyces. European Journal of Plant Pathology, 126, 445–451.

    Article  Google Scholar 

  • Kiss, L., Russell, J. C., Szentivanyi, O., Xu, X., & Jeffries, P. (2004). Biology and biocontrol potential of Ampelomyces mycoparasites, natural antagonist of powdery mildew fungi. Biocontrol Science and Technology, 14, 635–651.

    Article  Google Scholar 

  • Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). ClustalW2 and ClustalX version 2. Bioinformatics, 23, 2947–2948.

    Article  PubMed  CAS  Google Scholar 

  • Liang, C., Yang, J., Kovacs, G. M., Szentivanyi, O., Li, B., Xu, X. M., et al. (2007). Genetic diversity of Ampelomyces mycoparasite isolated from different powdery mildew species in China inferred from analyses of rDNA ITS sequences. Fungal Diversity, 24, 225–240.

    Google Scholar 

  • Mhaskar, D. N. (1974). Mycoparasite—Ampelomyces in artificial culture I. Morphology and cultural behaviour. Mycopathologia et Mycologia applicata, 52, 55–64.

    Article  Google Scholar 

  • Mhaskar, D. N., & Rao, V. G. (1974). The mycoparasite Ampelomyces quisqualis Ces. in artificial culture. II. Effect of environmental factors. Phytopathologia Mediterranea, 13, 147–154.

    Google Scholar 

  • Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. New York, NY: Oxford University Press.

    Google Scholar 

  • Page, R. D. M. (1996). Tree View: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12, 357–358.

    PubMed  CAS  Google Scholar 

  • Park, M. J., Choi, Y. J., Hong, S. B., & Shin, H. D. (2010). Genetic variability and mycohost association of Ampelomyces quisqualis isolates inferred from phylogenetic analyses of ITS rDNA and actin gene sequences. Fungal Biology, 114, 235–247.

    Article  PubMed  CAS  Google Scholar 

  • Paulitz, T. C., & Bèlanger, R. R. (2001). Biological control in greenhouse systems. Annual Review of Phytopathology, 39, 103–133.

    Article  PubMed  CAS  Google Scholar 

  • Philipp, W. D., & Cruger, G. (1979). Parasitismus von Ampelomyces quisqualis auf echten mehltaupilzen an gurken und anderen gemusearten. Zeitchrift fur Pflkanzenkrankheiten und Pflanzenschutz, 86, 129–142.

    Google Scholar 

  • Rankovic, B. (1997). Hyperparasites of the genus Ampelomyces on powdery mildew fungi in Serbia. Mycopathologia, 139, 157–164.

    Article  PubMed  CAS  Google Scholar 

  • Shin, H. D., & Kyeung, H. Y. (1994). Isolation of hyperparasitic fungi to control powdery mildews and selection of superior isolates for biocontrol of cucurbit powdery mildew. RDA Journal of Agricoltural Science, 36, 141–151.

    Google Scholar 

  • Speer, E. O. (1978). Beitrag zur morphologie von Ampelomyces quisqualis Ces. Sydowia, 31, 242–246.

    Google Scholar 

  • Staden, R., Beal, K. F., & Bonfield, J. K. (2000). The Staden package, 1998. Methods in Molecular Biology, 132, 115–130.

    PubMed  CAS  Google Scholar 

  • Sullivan, R. F., & White, J. F., Jr. (2000). Phoma glomerata as a mycoparasite of powdery mildew. Applied and Environmental Microbiology, 66, 425–427.

    Article  PubMed  CAS  Google Scholar 

  • Sundheim, L. (1982). Control of cucumber powdery mildew by the hyperparasite Ampelomyces quisqualis and fungicides. Plant Pathology, 31, 209–214.

    Article  Google Scholar 

  • Sundheim, L., & Krekling, T. (1982). Host–parasite relationships of the hyperparasite Ampelomyces quisqualis and its powdery mildew host Sphaerotheca fuliginea. I. Scanning electron microscopy. Phytopathology, 104, 202–210.

    Article  Google Scholar 

  • Sundheim, L., & Tronsmo, A. (1988). Hyperparasites in biological control. Vol. I. In K. G. Mekerji & K. L. Garg (Eds.), Biocontrol of plant diseases (pp. 53–69). Boca Raton, FL, USA: CRC Press.

    Google Scholar 

  • Szentiványi, O., Kiss, L., Russell, J. C., Kovács, G. M., Varga, K., Jankovics, T., et al. (2005). Ampelomyces mycoparasites from apple powdery mildew identified as a distinct group based on single-stranded conformation polymorphism analysis of the rDNA ITS region. Mycological Research, 109, 429–438.

    Article  PubMed  Google Scholar 

  • Sztejnberg, A. (1993). Ampelomyces quisqualis AQ10, CNCM I-807, for biological control of powdery mildew. US patent no. 5190754.

  • Sztejnberg, A., Galper, S., Mazar, S., & Lisker, N. (1989). Ampelomyces quisqualis for biological and integrated control of powdery mildews in Israel. Journal of Phytopathology, 124, 285–295.

    CAS  Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Article  PubMed  CAS  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). San Diego, CA, USA: Academic Press.

    Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Levente Kiss (Plant Protection Institute of the Hungarian Academy of Science, Budapest, Hungary) for valuable comments and suggestions and for providing fungal strains. We are grateful to the following colleagues for their helpful suggestions and assistance with the data analysis: Lorenzo Tosi, Valerio Mazzoni and Alberto Pellegrini. We would also like to thank Susanna Micheli and Denise Ress for their technical support and assistance. This work was supported by the AMPELO project (morphological and genetic analysis) and the ENVIROCHANGE project (effect of temperature), both funded by the Autonomous Province of Trento.

Author information

Authors and Affiliations

  1. Research and Innovation Centre, Fondazione Edmund Mach (FEM), S. Michele all’Adige, 38010, TN, Italy

    Dario Angeli & Ilaria Pertot

  2. Institute of Integrative Biology, Swiss Federal Institute of Technology (ETH), 8092, Zurich, CH, Switzerland

    Monika Maurhofer & Cesare Gessler

Authors
  1. Dario Angeli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika Maurhofer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cesare Gessler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ilaria Pertot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ilaria Pertot.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Angeli, D., Maurhofer, M., Gessler, C. et al. Existence of different physiological forms within genetically diverse strains of Ampelomyces quisqualis . Phytoparasitica 40, 37–51 (2012). https://doi.org/10.1007/s12600-011-0197-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-011-0197-x

Keywords

Search

Navigation