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Using molecular markers to assess the establishment and spread of a mycovirus applied as a biological control agent against chestnut blight

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Abstract

Chestnut blight, caused by the invasive fungus Cryphonectria parasitica, is one of the few tree diseases in Europe for which biological control is possible. The fungus may be infected by a mycovirus that reduces its virulence and sporulation capacity. In this study, we used molecular markers to assess the establishment and dissemination of the Cryphonectria hypovirus (CHV1) after its release as a biological control agent. The study was conducted in two chestnut stands in northern Switzerland. In both stands, viruses were repeatedly introduced by conducting classical canker treatments. Sequence analysis of viral isolates revealed the presence of the released viruses in the majority of the treated cankers, confirming that therapeutic canker treatment is mostly effective. Analysis of the dissemination of the released viruses gave contradictory results. In both stands, more than 50 % of the sampled untreated cankers were found to be virus-infected. In one stand, all viral isolates from those cankers originated from the released viruses, which evidently had spontaneously spread in the local C. parasitica population. In the other stand, the released virus was outcompeted by a naturally occurring virus, which was dominant in untreated cankers. Our study emphasizes the usefulness of molecular markers to track biological control agents and to evaluate the success of their application.

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References

  • Allemann C, Hoegger P, Heiniger U, Rigling D (1999) Genetic variation of Cryphonectria hypoviruses (CHV1) in Europe, assessed using restriction fragment length polymorphism (RFLP) markers. Mol Ecol 8:843–854

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Bryner SF, Rigling D (2011) Temperature-dependent genotype-by-genotype interaction between a pathogenic fungus and its hyperparasitic virus. Am Nat 177:65–74

    Article  PubMed  Google Scholar 

  • Bryner SF, Sotirovski K, Akilli S, Risteski M, Perlerou C, Rigling D (2013) Informative value of canker morphology on the presence or absence of virus infection in chestnut blight cankers. For Pathol 43:496–504

    Google Scholar 

  • Castello JD, Leopold DJ, Smallidge PJ (1995) Pathogens, patterns, and processes in forest ecosystems. Bioscience 45:16–24

    Article  Google Scholar 

  • Choi GH, Nuss DL (1992) Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science 257:800–803

    Article  CAS  PubMed  Google Scholar 

  • Cortesi P, Milgroom MG (1998) Genetics of vegetative incompatibility in Cryphonectria parasitica. Appl Environ Microbiol 64:2988–2994

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cortesi P, McCulloch CE, Song H, Lin H, Milgroom MG (2001) Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics 159:107–118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469

    Article  Google Scholar 

  • Dutech C, Barres B, Bridier J, Robin C, Milgroom MG, Ravigne V (2012) The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen. Mol Ecol 21:3931–3946

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edmonds RL (2013) General strategies of forest disease management. In: Gonthier P, Nicolotti G (eds) Infectious Forest Diseases. CAB International, Wallingford, pp 29–49

    Chapter  Google Scholar 

  • Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194

    Article  CAS  PubMed  Google Scholar 

  • Gobbin D, Hoegger PJ, Heiniger U, Rigling D (2003) Sequence variation and evolution of Cryphonectria hypovirus 1 (CHV-1) in Europe. Virus Res 97:39–46

    Article  CAS  PubMed  Google Scholar 

  • Gonthier P, Thor M (2013) Annosus Root and Butt Rots. In: Gonthier P, Nicolotti G (eds) Infectious forest diseases. CAB International, Wallingford, pp 128–158

    Chapter  Google Scholar 

  • Grente J (1965) Les formes hypovirulentes d’Endothia parasitica et les espoirs de lutte contre le chancre du châtaignier. C R de l’Acad d’Agric de Fr 51:1033–1037

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Heiniger U, Rigling D (1994) Biological control of chestnut blight in Europe. Annu Rev Phytopathol 32:581–599

    Article  Google Scholar 

  • Heiniger U, Rigling D (2009) Application of the Cryphonectria hypovirus (CHV-1) to control the chestnut blight, experience from Switzerland. Acta Hortic 815:233–245

    Article  Google Scholar 

  • Hoegger PJ, Rigling D, Holdenrieder O, Heiniger U (2000) Genetic structure of newly established populations of Cryphonectria parasitica. Mycol Res 104:1108–1116

    Article  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: a critical analysis. Annu Rev Phytopathol 42:311–338

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Pal KK, McSpadden Gardener B (2006) Biological control of plant pathogens. Plant Health Instr. doi:10.1094/PHI-A-2006-1117-02

    Google Scholar 

  • Papazova-Anakieva I, Sotirovski K, Cortesi P, Milgroom MG (2008) Horizontal transmission of hypoviruses between vegetative compatibility types of Cryphonectria parasitica in Macedonia. Eur J Plant Pathol 120:35–42

    Article  Google Scholar 

  • Pautasso M, Schlegel M, Holdenrieder O (2015) Forest health in a changing world. Microbial Ecol 69:826–842

    Article  Google Scholar 

  • Peever TL, Liu YC, Cortesi P, Milgroom MG (2000) Variation in tolerance and virulence in the chestnut blight fungus-hypovirus interaction. Appl Environ Microbiol 66:4863–4869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters FS, Bußkamp J, Prospero S, Rigling D, Metzler B (2014) Genetic diversification of the chestnut blight fungus Cryphonectria parasitica and its associated hypovirus in Germany. Fungal Biol 118:193–210

    Article  PubMed  Google Scholar 

  • Prospero S, Rigling D (2012) Invasion genetics of the chestnut blight fungus Cryphonectria parasitica in Switzerland. Phytopathology 102:73–82

    Article  CAS  PubMed  Google Scholar 

  • Prospero S, Rigling D (2013) Chestnut Blight. In: Gonthier P, Nicolotti G (eds) Infectious forest diseases. CAB International, Wallingford, pp 318–339

    Chapter  Google Scholar 

  • Prospero S, Conedera M, Heiniger U, Rigling D (2006) Saprophytic activity and sporulation of Cryphonectria parasitica on dead chestnut wood in forests with naturally established hypovirulence. Phytopathology 96:1337–1344

    Article  CAS  PubMed  Google Scholar 

  • Robin C, Lanz S, Soutrenon A, Rigling D (2010) Dominance of natural over released biological control agents of the chestnut blight fungus Cryphonectria parasitica in south-eastern France is associated with fitness-related traits. Biol Control 53:55–61

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Sarah Bryner, Andrea Dürmüller, Aline Frank and Esther Jung for the help in the field and in the laboratory, to Curtis Gautschi for English revision of the manuscript, and to the two anonymous reviewers for valuable comments on the manuscript.

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Correspondence to Simone Prospero.

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Handling Editor: Francisco Cazorla.

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Prospero, S., Rigling, D. Using molecular markers to assess the establishment and spread of a mycovirus applied as a biological control agent against chestnut blight. BioControl 61, 313–323 (2016). https://doi.org/10.1007/s10526-015-9713-0

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  • DOI: https://doi.org/10.1007/s10526-015-9713-0

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