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.
Anagnostakis, S. L. (1983). Conversion to curative morphology in Endothia parasitica and its restriction by vegetative compatibility. Mycologia, 75, 777–780.
Anagnostakis, S. L., & Day, P. R. (1979). Hypovirulence conversion in Endothia parasitica. Phytopathology, 69, 1226–1229.
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.
Anagnostakis, S. L., & Waggoner, P. E. (1981). Hypovirulence, vegetative incompatibility, and the growth of cankers of chestnut blight. Phytopathology, 71, 1198–1202.
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.
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.
Buck, K. W. (1986). Fungal virology – an overview. In K. W. Buck (Ed.), Fungal virology (pp. 1–84). Boca Raton: CRC Press.
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.
Caten, C. E. (1972). Vegetative incompatibility and cytoplasmic infection in fungi. Journal of General Microbiology, 72, 221–229.
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.
Cortesi, P., & Milgroom, M. G. (1998). Genetics of vegetative incompatibility in Cryphonectria parasitica. Applied and Environmental Microbiology, 64, 2988–2994.
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.
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.
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.
Glass, N. L., & Kaneko, I. (2003). Fatal attraction: Nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryotic Cell, 2, 1–8.
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.
Griffin, G. J. (1986). Chestnut blight and its control. Horticultural Review, 8, 291–336.
Hartl, D. L., Dempster, E. R., & Brown, S. W. (1975). Adaptive significance of vegetative incompatibility in Neurospora crassa. Genetics, 81, 553–569.
Heiniger, U., & Rigling, D. (1994). Biological control of chestnut blight in Europe. Annual Review of Phytopathology, 32, 581–599.
Hillman, B. I., & Suzuki, N. (2004). Viruses of the chestnut blight fungus, Cryphonectria parasitica. Advances in Virus Research, 63, 423–472.
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.
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.
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.
MacDonald, W. L., & Fulbright, D. W. (1991). Biological control of chestnut blight: Use and limitations of transmissible hypovirulence. Plant Disease, 75, 656–661.
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.
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.
Milgroom, M. G., & Cortesi, P. (2004). Biological control of chestnut blight with hypovirulence: A critical analysis. Annual Review of Phytopathology, 42, 311–338.
Nuss, D. L. (1992). Biological control of chestnut blight: An example of virus-mediated attenuation of fungal pathogenesis. Microbiological Reviews, 56, 561–576.
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.
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.
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.
Saupe, S. J. (2000). Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiology and Molecular Biology Reviews, 64, 489–502.
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.
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.
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.
Wickner, R. B. (1996). Double-stranded RNA viruses of yeast. Microbiological Reviews, 60, 250–265.
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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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