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Horizontal transmission of hypoviruses between vegetative compatibility types of Cryphonectria parasitica in Macedonia

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Abstract

Biological control of chestnut blight with hypovirulence depends on the successful transmission of hypoviruses between individuals of the chestnut blight fungus, Cryphonectria parasitica. Vegetative incompatibility inhibits horizontal virus transmission, but not completely. In an effort to assess the potential for the spread of hypoviruses in the Republic of Macedonia, we studied the transmission of Cryphonectria hypovirus 1 (CHV-1) among the five observed vegetative compatibility (vc) types of C. parasitica. One fungal isolate of each vc type was infected with CHV-1 and was paired in vitro with isolates of all other vc types for a total of 20 combinations of virus donors and recipients, and 250 replicate trials per combination. Virus transmission was scored after 7 days as successful if the recipient isolate took on an unpigmented culture phenotype typical of virus infection. Transmission occurred at high frequencies between some pairs of vc types, but in <1% of the trials for 10 of the 20 combinations of donors and recipients. Asymmetric transmission was observed between some vc types that had different alleles at vegetative incompatibility loci vic1 or vic7; i.e., transmission occurred at high frequencies in one direction, but very low frequencies between the same pair of isolates in the opposite direction. The expected virus transmission, calculated as the average transmission predicted for any two randomly chosen individuals from a population, was highly negatively correlated to vc type diversity. Results for isolates of C. parasitica from Macedonia were similar to those from Italy, but less transmission was generally observed. Differences in genetic background effects on transmission may vary among different populations even when isolates differ by the same vic alleles.

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Abbreviations

CHV-1:

cryphonectria hypovirus 1

vc type:

vegetative compatibility type

vic :

vegetative incompatibility

References

  • Anagnostakis, S. L. (1982). Biological control of chestnut blight. Science, 215, 466–471.

    Article  PubMed  CAS  Google Scholar 

  • Anagnostakis, S. L. (1983). Conversion to curative morphology in Endothia parasitica and its restriction by vegetative compatibility. Mycologia, 75, 777–780.

    Article  Google Scholar 

  • Anagnostakis, S. L., & Day, P. R. (1979). Hypovirulence conversion in Endothia parasitica. Phytopathology, 69, 1226–1229.

    Article  CAS  Google Scholar 

  • Anagnostakis, S. L., Hau, B., & Kranz, J. (1986). Diversity of vegetative compatibility groups of Cryphonectria parasitica in Connecticut and Europe. Plant Disease, 70, 536–538.

    Google Scholar 

  • Anagnostakis, S. L., & Waggoner, P. E. (1981). Hypovirulence, vegetative incompatibility, and the growth of cankers of chestnut blight. Phytopathology, 71, 1198–1202.

    Google Scholar 

  • Bisiach, M., De Martino, A., Gobbi, E., Intropido, M., & Vegetti, G. (1988). Studies on chestnut blight: Activity report. Rivista di Patologia Vegetale, 24(S.IV), 3–13.

    Google Scholar 

  • Bissegger, M., Rigling, D., & Heiniger, U. (1997). Population structure and disease development of Cryphonectria parasitica in European chestnut forests in the presence of natural hypovirulence. Phytopathology, 87, 50–59.

    Article  PubMed  CAS  Google Scholar 

  • Buck, K. W. (1986). Fungal virology – an overview. In K. W. Buck (Ed.), Fungal virology (pp. 1–84). Boca Raton: CRC Press.

    Google Scholar 

  • Carbone, I., Liu, Y.-C., Hillman, B. I., & Milgroom, M. G. (2004). Recombination and migration of Cryphonectria hypovirus 1 as inferred from gene genealogies and the coalescent. Genetics, 166, 1611–1629.

    Article  PubMed  CAS  Google Scholar 

  • Caten, C. E. (1972). Vegetative incompatibility and cytoplasmic infection in fungi. Journal of General Microbiology, 72, 221–229.

    PubMed  CAS  Google Scholar 

  • Cortesi, P., McCulloch, C. E., Song, H., Lin, H., & Milgroom, M. G. (2001). Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics, 159, 107–118.

    PubMed  CAS  Google Scholar 

  • Cortesi, P., & Milgroom, M. G. (1998). Genetics of vegetative incompatibility in Cryphonectria parasitica. Applied and Environmental Microbiology, 64, 2988–2994.

    PubMed  CAS  Google Scholar 

  • Debets, F., Yang, X., & Griffiths, A. J. G. (1994). Vegetative incompatibility in Neurospora: Its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Current Genetics, 26, 113–119.

    Article  PubMed  CAS  Google Scholar 

  • Double, M. L. (1982). The ability of hypovirulent isolates and mixtures of hypovirulent isolates to control artificially established virulent cankers. In H. C. Smith & W. L. MacDonald (Eds.), USDA Forest service American chestnut cooperators’ meeting (pp. 145–152). Morgantown, WV: West Virginia University Books.

    Google Scholar 

  • Glass, N. L., Jacobson, D. J., & Shiu, P. K. T. (2000). The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annual Review of Genetics, 34, 165–186.

    Article  PubMed  CAS  Google Scholar 

  • Glass, N. L., & Kaneko, I. (2003). Fatal attraction: Nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryotic Cell, 2, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Grente, J., & Berthelay-Sauret, S. (1978). Biological control of chestnut blight in France. In W. L. MacDonald, F. C. Cech, J. Luchok, & C. Smith (Eds.), Proceedings of the American Chestnut Symposium (pp. 30–34). Morgantown, WV: West Virginia University Books.

    Google Scholar 

  • Griffin, G. J. (1986). Chestnut blight and its control. Horticultural Review, 8, 291–336.

    Google Scholar 

  • Hartl, D. L., Dempster, E. R., & Brown, S. W. (1975). Adaptive significance of vegetative incompatibility in Neurospora crassa. Genetics, 81, 553–569.

    PubMed  CAS  Google Scholar 

  • Heiniger, U., & Rigling, D. (1994). Biological control of chestnut blight in Europe. Annual Review of Phytopathology, 32, 581–599.

    Article  Google Scholar 

  • Hillman, B. I., & Suzuki, N. (2004). Viruses of the chestnut blight fungus, Cryphonectria parasitica. Advances in Virus Research, 63, 423–472.

    PubMed  CAS  Google Scholar 

  • Huber, D. H., & Fulbright, D. W. (1996). New vegetative incompatibility loci in Cryphonectria parasitica and their effects upon horizontal transmission of hypoviruses. Phytopathology, 86(Suppl.), S29.

    Google Scholar 

  • Kuhlman, E. G., Bhattacharyya, H., Nash, B. L., Double, M. L., & MacDonald, W. L. (1984). Identifying hypovirulent isolates of Cryphonectria parasitica with broad conversion capacity. Phytopathology, 74, 676–682.

    Google Scholar 

  • Liu, Y.-C., & Milgroom, M. G. (1996). Correlation between hypovirus transmission and the number of vegetative incompatibility (vic) genes different among isolates from a natural population of Cryphonectria parasitica. Phytopathology, 86, 79–86.

    Article  Google Scholar 

  • MacDonald, W. L., & Fulbright, D. W. (1991). Biological control of chestnut blight: Use and limitations of transmissible hypovirulence. Plant Disease, 75, 656–661.

    Article  Google Scholar 

  • Micali, O. C., & Smith, M. L. (2005). Biological concepts of vegetative self and nonself recognition in fungi. In J. Xu (Ed.), Evolutionary genetics of fungi (pp. 63–85). Wymondham, UK: Horizon Bioscience.

    Google Scholar 

  • Milgroom, M. G., & Cortesi, P. (1999). Analysis of population structure of the chestnut blight fungus based on vegetative incompatibility genotypes. Proceedings of the National Academy of Science, USA, 96, 10518–10523.

    Article  CAS  Google Scholar 

  • Milgroom, M. G., & Cortesi, P. (2004). Biological control of chestnut blight with hypovirulence: A critical analysis. Annual Review of Phytopathology, 42, 311–338.

    Article  PubMed  CAS  Google Scholar 

  • Nuss, D. L. (1992). Biological control of chestnut blight: An example of virus-mediated attenuation of fungal pathogenesis. Microbiological Reviews, 56, 561–576.

    PubMed  CAS  Google Scholar 

  • Nuss, D. L., Hillman, B. I., Rigling, D., & Suzuki, N. (2005). Hypoviridae. In C. M. Fauquet (Ed.), Virus taxonomy: VIIIth report of the international committee for the taxonomy of viruses. New York: Academic.

    Google Scholar 

  • Peever, T. L., Liu, Y.-C., Cortesi, P., & Milgroom, M. G. (2000). Variation in tolerance and virulence in the chestnut blight fungus–hypovirus interaction. Applied and Environmental Microbiology, 66, 4863–4869.

    Article  PubMed  CAS  Google Scholar 

  • Robin, C., Anziani, C., & Cortesi, P. (2000). Relationship between biological control, incidence of hypovirulence, and diversity of vegetative compatibility types of Cryphonectria parasitica in France. Phytopathology, 90, 730–737.

    Article  PubMed  CAS  Google Scholar 

  • Saupe, S. J. (2000). Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiology and Molecular Biology Reviews, 64, 489–502.

    Article  PubMed  CAS  Google Scholar 

  • Sotirovski, K., Milgroom, M. G., Rigling, D., & Heiniger, U. (2006). Occurrence of Cryphonectria hypovirus 1 in the chestnut blight fungus in Macedonia. Forest Pathology, 36, 136–143.

    Article  Google Scholar 

  • Sotirovski, K., Papazova-Anakieva, I., Grünwald, N. J., & Milgroom, M. G. (2004). Low diversity of vegetative compatibility types and mating type in Cryphonectria parasitica in the southern Balkans. Plant Pathology, 53, 325–333.

    Article  Google Scholar 

  • Van Alfen, N. K., Jaynes, R. A., Anagnostakis, S. L., & Day, P. R. (1975). Chestnut blight: Biological control by transmissible hypovirulence in Endothia parasitica. Science, 189, 890–891.

    Article  PubMed  Google Scholar 

  • Wickner, R. B. (1996). Double-stranded RNA viruses of yeast. Microbiological Reviews, 60, 250–265.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This research was funded in part by project 40110201 from the Ministry of Education and Science of the Republic of Macedonia to K.S., and grant no. OISE-0350019 from the US National Science Foundation to M.G.M.

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Correspondence to K. Sotirovski.

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Papazova-Anakieva, I., Sotirovski, K., Cortesi, P. et al. Horizontal transmission of hypoviruses between vegetative compatibility types of Cryphonectria parasitica in Macedonia. Eur J Plant Pathol 120, 35–42 (2008). https://doi.org/10.1007/s10658-007-9191-z

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  • DOI: https://doi.org/10.1007/s10658-007-9191-z

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