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Short and long term efficacy and prevalence of Cryphonectria parasitica hypovirulent strains released as biocontrol agents of chestnut blight

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Abstract

Chestnut blight, Cryphonectria parasitica (Murrill) Barr, was reported in Portugal in 1989. The disease rapidly spread within the chestnut region of the Trás-os-Montes (the Northeast of Portugal). Eradication and mechanical/burning exclusion failed to control the disease and natural hypovirulence is still absent or of very low incidence. The introduction of human-assisted therapeutic hypovirulence is therefore required to control the disease. We presente here the efficacy of field applications (short and long term) of a locally characterized hypovirulent strain (CHV1-RBB111), by the punch method in two chestnut orchards (Valpaços and Vinhais). The Valpaços disease incidence was 68% (65 out of 96 trees) and in Vinhais it was 46% (78 out of 169 trees). In both locations, diversity of vegetative incompatibility (vc type) was low and largely dominated (> 85%) by a single vc type (EU11). In Valpaços, all cankers of the orchard were treated (63 cankers) and in Vinhais 31 trees (cankers) were treated. One year after application, field efficacy was very high with 93.8% of healed cankers in Valpaços and 90.3% in Vinhais, these values increased to 100% and 93.5% (respectively) after four years. The persistence of the introduced CHV1-RBB 111 strain was high and present in almost all treated cankers and it was dominant both inwards and on the application site revealing an endophytic behavior. The non-C. parasitica microfungi were abundant with 14 different species. Biscogniauxia mediterranea (De Not.) Kuntze was the most abundant in both orchards. Treatment with the introduced hypovirulent strain (CHV1-RBB111) was found to be effective in controlling chestnut blight with regeneration of cortical tissues and recovery of treated trees.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abreu, C. (1992). A hipovirulência como forma de luta natural contra o cancro do castanheiro. Revista das Ciências Agrárias, 15(1–2), 167–169.

    Google Scholar 

  • Akilli, S., Katircioðlu, Y. Z., & Maden, S. (2009). Chestnut blight cankers in black sea region of Turkey. Acta Horticulturae, 815, 247–252.

    Article  Google Scholar 

  • Akıllı, S., Ulubaş Serçe, Ç. U., Katircioǧlu, Y. Z., Maden, S., & Rigling, D. (2013). Characterization of hypovirulent isolates of the chestnut blight fungus, Cryphonectria parasitica from the Marmara and Black Sea regions of Turkey. European Journal of Plant Pathology, 135(2), 323–334.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 

  • Bragança, H., Simões, S., Onofre, N., Tenreiro, R., & Rigling, D. (2007). Cryphonectria parasitica in Portugal: diversity of vegetative compatibility types, mating types, and occurrence of hypovirulence. Forest Pathology, 37, 391–402.

    Article  Google Scholar 

  • Bryner, S. F., Rigling, D., & Brunner, P. C. (2012). Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus. Ecology and Evolution, 2, 32927–33241.

    Article  Google Scholar 

  • Câmara, M. S. (1929). Micotes aliquot novi allique in mycoflora lusitaneae ignoti. Revista Agronómica, 17, 7.

    Google Scholar 

  • Chira, D., Bolea, V., Chira, F., Mantale, C., Tăut, I., Şimonca, V., et al. (2017). Biological control of Cryphonectria parasitica in Romanian protected sweet chestnut forests. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 45(2), 632–638.

    Article  Google Scholar 

  • Curković-Perica, M., Ježić, M., Karin, V., Idžojtić, M., Sotirovski, K., Risteski, M. et al. (2017). Biological control of chestnut blight: (In)stable infection of the chestnut blight fungus by Cryphonectria hypovirus 1. In: 7th Congress of European Microbiologists, Valencia, Spain 9-13 July 2017.

  • Diamandis, S. (2018). Management of Chestnut blight in Greece using hypovirulence and silvicultural interventions. Forests, 9, 492.

    Article  Google Scholar 

  • Double, M. L., Kolp, M. R., Jarosz, A. M., Davelos Baines, A., Fulbright, D. W., & MacDonald, W. L. (2014). Fungi associated with hypovirulent cankers of differing ages on American chestnut. Acta Horticulturae, 1043, 57–65.

    Article  Google Scholar 

  • EC 1107/2009. Regulation (EC) No 1107/2009 of the European Parliament and of the council of 21 October 2009.

  • Feau, N., Dutech, C., Brusini, J., Rigling, D., & Robin, C. (2014). Multiple introductions and recombination in Cryphonectria hypovirus 1: perspective for a sustainable biological control of chestnut blight. Evolutionary Applications, 7, 580–596.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gobbin, D., Hoegger, P. J., Heiniger, U., & Rigling, D. (2003). Sequences variation and evolution of Cryphonectria parasitica (CHV-1) in Europe. Virus Research, 97, 39–46.

    Article  CAS  PubMed  Google Scholar 

  • González, A. J., & Estefanía, T. (2020). Strains of Neopestalotiopsis sp. are in vitro antagonists of Cryphonectria parasitica. Biological Control, 143, 104187.

    Article  Google Scholar 

  • Gouveia, E., Coelho, V., & Monteiro, M. L. (2010). Potential of local Hypovirulent strains of Cryphonectria parasitica for biological control of chestnut blight. Acta Horticulturae, 866, 443–448.

    Article  CAS  Google Scholar 

  • Gouveia, E., Pereira, E., Araújo, A., Coelho, V., Castro, J., Bragança, H., & Martins, L. (2016). Cancro do Castanheiro em Trás-os-Montes (Portugal): Incidência atual e estudo da estrutura populacional de Cryphonectria parasitica para a introdução da luta biológica por hipovirulência. Gaia Scientia, 10(2), 75–83.

    Article  Google Scholar 

  • Gouveia, E., Torrent, I.I. & Coelho, V. (2017). Diversidade de microfungos presentes nos ramos e troncos de castanheiro infectados por Cryphonectria parasitica. 8° Congresso Florestal Nacional. Viana do Castelo, 11-14 October 2017, pp. 193.

  • Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3), 307–321.

    Article  CAS  PubMed  Google Scholar 

  • Heiniger, U., & Rigling, D. (1994). Biological control of chestnut blight in Europe. Annual Review of Phytopathology, 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 Horticulturae, 815, 233–245.

    Article  Google Scholar 

  • Henriques, J., Nóbrega, F., Sousa, E., & Lima, A. (2014). Diversity of Biscogniauxia mediterranea within single Stromata on Cork Oak. The Journal of Mycology, 2014, 324349.

    Google Scholar 

  • Henriques, J., Nóbrega, F., Sousa, E., & Lima, A. (2015). Morphological and genetic diversity of Biscogniauxia mediterranea associated to Quercus suber in the Mediterranean Basin. Revista de Ciências Agrárias, 38(2), 166–175.

    Google Scholar 

  • Hoegger, P. J., Heiniger, U., Holdenrieder, O., & Rigling, D. (2003). Differential transfer and dissemination of hypovirus and nuclear and mitochondrial genomes of a hypovirus-infected Cryphonectria parasitica strain after introduction into a natural population. Applied and Environmental Microbiology, 69, 3767–3771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homs, G., Rodríguez, J., Rigling, D. & Colinas, C. (2001). Caracterización de la población de Cryphonectria parasitica y detección de cepas hipovirulentas en 3 subpoblaciones de Cataluña. Montes para la sociedad del nuevo milenio. III Congreso Forestal Español. Granada, Spain.

  • Huerta-Cepas, J., Serra, F., & Bork, P. (2016). ETE 3: Reconstruction, analysis, and visualization of Phylogenomic data. Molecular Biology and Evolution, 33(6), 1635–1638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeger, M., Bragard, C., Chatzivassiliou, E., Dehnen-Schmutz, K., Gilioli, G., Jaques Miret, J.A., MacLeod, A., Navajas Navarro, M., Niere, B., Parnell, S., Potting, R., Rafoss, T., Urek, G., Van Bruggen, A., Van der Werf, W., West, J., Winter, S., Maresi, G., Prospero, S., Vettraino, A.M., Vloutoglou, I., Pautasso, M. & Rossi, V. (2016). Scientific opinion on the risk assessment and reduction options for Cryphonectria parasitica in the EU. EFSA Journal, 14(12), 4641, 54 pp.

  • Ježić, M., Kolp, M., Prospero, S., Sotirovski, K., Double, M., Rigling, D., Risteski, M., Karin-Kujundžić, V., Idžojtić, M., Poljak, I., & Ćurković-Perica, M. (2019). Diversity of Cryphonectria parasitica in callused chestnut blight cankers on European and American chestnut. Forest Pathology, 49, e12566.

    Article  Google Scholar 

  • Kolp, M. (2018). Fungal community succession and interactions in chestnut blight cankers on American chestnut trees in Michigan and Wisconsin. PhD thesis. Michigan State University, East Lansing, Michigan.

  • Kolp, M., Double, M.L., Fulbright, D.W., MacDonald, W.L. & Jarosz, A.M. (2017). Tracking disease and the fungal community structure in chestnut blight cankers on American chestnut in Michigan and Wisconsin. In: 102nd Annual Meeting of the Ecological Society of America, Portland, Oregon 5-11 August 2017.

  • Krstin, L., Katanić, Z., Ježić, M., Poljak, I., Nuskern, L., Matković, I., Idžojtić, M., & Ćurković-Perica, M. (2017). Biological control of chestnut blight in Croatia: An interaction between host sweet chestnut, its pathogen Cryphonectria parasitica and the biocontrol agent Cryphonectria hypovirus 1. Pest Management Science, 73, 582–589.

    Article  CAS  PubMed  Google Scholar 

  • Kunova, A., Pizzatti, C., Cerea, M., Gazzaniga, A., & Cortesi, P. (2016). New formulation and delivery method of Cryphonectria parasitica for biological control of chestnut blight. Journal of Applied Microbiology, 22, 180–187.

    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  CAS  PubMed  Google Scholar 

  • Moura, L., Pereira, G., Costa, S., Martins, M., & Gouveia, E. (2015). Chestnut blight in the Minho region. Population structure and genetic variability of Cryphonectria parasitica. Revista de Ciências Agrárias, 38(2), 238–247.

    Google Scholar 

  • Murolo, S., Concas, J., & Romanazzi, G. (2019). Use of biocontrol agents as potential tools in the management of chestnut blight. Biological Control, 132, 102–109.

    Article  Google Scholar 

  • Pereira, E., Rigling, D., Prospero, S., & Gouveia, E. (2015). Controlo biológico do cancro do castanheiro. Deteção, identificação e caracterização do Hypovirus - CHV1. Revista de Ciências Agrárias, 38(2), 258–263.

    Google Scholar 

  • Potter, B. (2017). Biocontrol potential of endophytes of healthy Castanea dentata for application against Cryphonectria parasitica. Master of Science in Biology. University of Wisconsin-La Crosse, pp. 70.

  • Rigling, D., & Prospero, S. (2018). Cryphonectria parasitica, the causal agent of chestnut blight: invasion history, population biology and disease control. Molecular Pant Pathology, 19(1), 7–20.

    Article  CAS  Google Scholar 

  • Robin, C., & Heiniger, U. (2001). Chestnut blight in Europe: diversity of Cryphonectria parasitica, hypovirulence and biocontrol. Forest Snow and Landscape Research Editorial, 76(3), 361–367.

    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  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. Biological Control, 53, 55–61.

    Article  Google Scholar 

  • Shain, L., & Miller, J. B. (1992). Movement of cytoplasmic hypovirulence agents in chestnut blight cankers. Canadian Journal of Botany, 70, 557–561.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Suzuki, N., Ghabrial, S. A., Kim, K., Pearson, M., Marzano, S. L., Yaegashi, H., et al. (2018). ICTV virus taxonomy profile: Hypoviridae. Journal of General Virology, 99, 615–616.

    Article  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. Innis, D. Gelfand, J. Shinsky, & T. J. White (Eds.), PCR protocols: a guide to methods and applications (pp. 315–322). San Diego: Academic Press.

    Google Scholar 

  • Zamora, P., Martín, A. B., Rigling, D., & Diez, J. J. (2012). Diversity of Cryphonectria parasitica in western Spain and identification of hypovirus-infected isolates. Forest Pathology, 42(5), 412–419.

    Article  Google Scholar 

  • Zamora, P., Martín, A. B., San Martín, R., Martínez-Álvarez, P., & Diez, J. J. (2014). Control of chestnut blight by the use of hypovirulent strains of the fungus Cryphonectria parasitica in northwestern Spain. Biological Control, 79, 58–66.

    Article  Google Scholar 

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Acknowledgments

The authors are grateful to the Project BioChestnut -IPM - Implement effective control strategies against the chestnut and almond diseases under the Programme PDR2020-101-030959 for financial support.

Funding

This study was funded by the Project BioChestnut-IPM (PDR2020–101-030959).

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Correspondence to Eugénia Gouveia.

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Coelho, V., Nunes, L. & Gouveia, E. Short and long term efficacy and prevalence of Cryphonectria parasitica hypovirulent strains released as biocontrol agents of chestnut blight. Eur J Plant Pathol 159, 769–781 (2021). https://doi.org/10.1007/s10658-021-02200-3

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