Skip to main content
SpringerLink
Log in

Virus Community Dynamics in the Conifer Pathogenic Fungus Heterobasidion parviporum Following an Artificial Introduction of a Partitivirus

  • Fungal Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Viruses infecting the conifer pathogenic fungus Heterobasidion annosum sensu lato are intracellular and spread via anastomosis contacts. In the laboratory, these viruses transmit readily even between somatically incompatible isolates, but their dispersal capacity in natural conditions has not been previously studied. We introduced a mycovirus to a heavily diseased forest site by inoculating Norway spruce stumps with heartrot decay using a mycelial suspension of Heterobasidion parviporum strain RT3.49C hosting the partitivirus strain HetRV4-pa1. The Heterobasidion population at the sample plot was screened for mycoviruses prior to and after the inoculation. Based on sequence analysis, the resident H. parviporum strains harbored six different strains of the virus species Heterobasidion RNA virus 6 (HetRV6) and one strain of HetRV4 prior to the inoculation. After three growth seasons, the inoculated H. parviporum host strain was not detected, but the introduced virus had infected two resident H. parviporum genets. The presence of a preexisting HetRV6 infection did not hinder spread of the introduced partitivirus but resulted in coinfections instead. The resident HetRV6 virus population seemed to be highly stable during the incubation period, while the single indigenous HetRV4 infection was not detected after the inoculation. In laboratory infection experiments, the introduced virus could be transmitted successfully into all of the resident H. parviporum genets. This study shows for the first time transmission of a Heterobasidion virus between somatically incompatible hosts in natural conditions.

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

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. Niemelä T, Korhonen K (1998) Taxonomy of the genus Heterobasidion. In: Woodward S, Stenlid J, Karjalainen R, Hüttermann A (eds) Heterobasidion annosum: biology, ecology, impact and control. CAB International, Wallingford, pp 27–41

    Google Scholar 

  2. Dai Y-C, Vainio EJ, Hantula J, Niemelä T, Korhonen K (2003) Investigations on Heterobasidion annosum s.lat. in central and eastern Asia with the aid of mating tests and DNA fingerprinting. For Path 33:269–286

    Article  Google Scholar 

  3. Woodward S, Stenlid J, Karjalainen R, Hüttermann A (1998) Heterobasidion annosum: biology, ecology, impact and control. CAB International, Wallingford

    Google Scholar 

  4. Otrosina WJ, Garbelotto M (2010) Heterobasidion occidentale sp. nov. and Heterobasidion irregulare nom. nov.: a disposition of North American Heterobasidion biological species. Fungal Biol 114:16–25

    Article  PubMed  Google Scholar 

  5. Piri T (2003) Silvicultural control of Heterobasidion root rot in Norway spruce forests in southern Finland: regeneration and vitality fertilization of infected stands. Dissertation, University of Helsinki

  6. Ihrmark K (2001) Double-stranded RNA elements in the root rot fungus Heterobasidion annosum. Dissertation, Swedish University of Agricultural Sciences

  7. Vainio EJ, Hakanpää J, Dai Y-C, Hansen E, Hantula J (2011) Species of Heterobasidion host a diverse pool of partitiviruses with global distribution and interspecies transmission. Fungal Biol 115:1234–1243

    Article  PubMed  CAS  Google Scholar 

  8. Ihrmark K, Johannesson H, Stenström E, Stenlid J (2002) Transmission of double-stranded RNA in Heterobasidion annosum. Fungal Genet Biol 36:147–154

    Article  PubMed  CAS  Google Scholar 

  9. Vainio EJ, Korhonen K, Tuomivirta TT, Hantula J (2010) A novel putative partitivirus of the saprotrophic fungus Heterobasidion ecrustosum infects pathogenic species of the Heterobasidion annosum complex. Fungal Biol 114:955–965

    Article  PubMed  CAS  Google Scholar 

  10. Ihrmark K, Stenström E, Stenlid J (2004) Double-stranded RNA transmission through basidiospores of Heterobasidion annosum. Mycol Res 108:149–153

    Article  PubMed  CAS  Google Scholar 

  11. Vainio EJ, Hyder R, Aday G, Hansen E, Piri T, Doğmuş-Lehtijärvi T, Lehtijärvi A, Korhonen K, Hantula J (2012) Population structure of a novel putative mycovirus infecting the conifer root-rot fungus Heterobasidon annosum sensu lato. Virology 422:366–376

    Article  PubMed  CAS  Google Scholar 

  12. Vainio EJ, Keriö S, Hantula J (2011) Description of a new putative virus infecting the conifer pathogenic fungus Heterobasidion parviporum with resemblance to Heterobasidion annsoum P-type partitivirus. Arch Virol 156:79–86

    Article  PubMed  CAS  Google Scholar 

  13. Deng F, Xu R, Boland GJ (2003) Hypovirulence-associated double-stranded RNA from Sclerotinia homoeocarpa is conspecific with Ophiostoma novo-ulmi mitovirus 3a-Ld. Phytopathology 93:1407–1414

    Article  PubMed  CAS  Google Scholar 

  14. Huang S, Ghabrial SA (1996) Organization and expression of the double-stranded RNA genome of Helminthosporium victoriae 190S virus, a totivirus infecting a plant pathogenic filamentous fungus. Proc Natl Acad Sci USA 93:12541–12546

    Article  PubMed  CAS  Google Scholar 

  15. Lakshman DK, Jian J, Tavantzis M (1998) A double-stranded RNA element from a hypovirulent strain of Rhizoctonia solani occurs in DNA form and is genetically related to the pentafunctional AROM protein of the shikimate pathway. Proc Natl Acad Sci USA 95:6425–6429

    Article  PubMed  CAS  Google Scholar 

  16. Preisig O, Moleleki N, Smit WA, Wingfield BD, Wingfield MJ (2000) A novel RNA mycovirus in a hypovirulent isolate of the plant pathogen Diaporthe ambigua. J Gen Virol 81:3107–3114

    PubMed  CAS  Google Scholar 

  17. Yu X, Li B, Fu Y, Jiang D, Ghabrial SA, Li G, Peng Y, Xie J, Cheng J, Huang J, Yi X (2010) A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci USA 107:8387–8392

    Article  PubMed  CAS  Google Scholar 

  18. Anagnostakis S, Day P (1979) Hypovirulence conversion in Endothia parasitica. Phytopathology 69:1226–1229

    Article  CAS  Google Scholar 

  19. Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384

    Article  PubMed  CAS  Google Scholar 

  20. Rogers HJ, Buck KW, Brasier CM (1986) Transmission of double-stranded RNA and a disease factor in Ophiostoma ulmi. Plant Pathol 35:227–287

    Article  Google Scholar 

  21. Coenen A, Kevei F, Hoekstra RF (1997) Factors affecting the spread of double-stranded RNA viruses in Aspergillus nidulans. Genet Res 69:1–10

    Article  PubMed  CAS  Google Scholar 

  22. Liu Y-C, Milgroom MG (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 

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

    Article  PubMed  CAS  Google Scholar 

  24. Harris RF, Sommers LE (1968) Plate-dilution frequency technique for assay of microbial ecology. Appl Microbiol 16:330–334

    PubMed  CAS  Google Scholar 

  25. Stenlid J (1985) Population structure of Heterobasidion annosum as determined by somatic incompatibility, sexual incompatibility, and isoenzyme patterns. Can J Bot 63:2268–2273

    Article  CAS  Google Scholar 

  26. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

  27. Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858

    Article  CAS  Google Scholar 

  28. Tuomivirta T, Hantula J (2003) Two unrelated double-stranded RNA molecule patterns in Gremmeniella abietina type A code for putative viruses of the families Totiviridae and Partitiviridae. Arch Virol 148:2293–2305

    Article  PubMed  CAS  Google Scholar 

  29. Müller MM, Kantola R, Kitunen V (1994) Combining sterol and fatty acid profiles for the characterization of fungi. Mycol Res 98:593–603

    Article  Google Scholar 

  30. Vainio E, Korhonen K, Hantula J (1998) Genetic variation in Phlebiopsis gigantea as detected with random amplified microsatellite (RAMS) markers. Mycol Res 102:187–192

    Article  Google Scholar 

  31. Bendz-Hellgren M, Brandtberg P-O, Johansson M, Swedjemark G, Stenlid J (1999) Growth rate of Heterobasidion annosum in Picea abies established on forest land and arable land. Scand J For Res 14:402–407

    Article  Google Scholar 

  32. Carbone I, Liu Y-C, Hillman BI, Milgroom MG (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 

  33. Ikeda K-I, Nakamura H, Arakawa M, Matsumoto N (2004) Diversity and vertical transmission of double-stranded RNA elements in root rot pathogens of trees, Helicobasidium mompa and Rosellinia necatrix. Mycol Res 108:626–634

    Article  PubMed  CAS  Google Scholar 

  34. Domingo E, Escarmís C, Sevilla N, Moya A, Elena SF, Quer J, Novella IS, Holland JJ (1996) Basic concepts in RNA virus evolution. FASEB J 10:859–864

    PubMed  CAS  Google Scholar 

  35. 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  PubMed  CAS  Google Scholar 

  36. Ikeda K-I, Nakamura H, Arakawa M, Koiwa T, Matsumoto N (2005) Dynamics of double-stranded RNA segments in a Helicobasidium mompa clone from a tulip tree plantation. FEMS Microbiol Ecol 51:293–301

    Article  PubMed  CAS  Google Scholar 

  37. Arakawa M, Nakamura H, Uetake Y, Matsumoto N (2002) Presence and distribution of double-stranded RNA elements in the white root rot fungus Rosellinia necatrix. Mycoscience 43:21–26

    Article  CAS  Google Scholar 

  38. Hoegger PJ, 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. Appl Environ Microbiol 69:3767–3771

    Article  PubMed  CAS  Google Scholar 

  39. Yaegashi H, Sawahata T, Ito T, Kanematsu S (2010) A novel colony-print immunoassay reveals differential patterns of distribution and horizontal transmission of four unrelated mycoviruses in Rosellinia necatrix. Virology 409:2280–2289

    Google Scholar 

  40. Ghabrial SA, Soldevila AI, Havens WM (2002) Molecular genetics of the viruses infecting the plant pathogenic fungus Helminthosporium victoriae. In: Tavantzis S (ed) Molecular biology of double-stranded RNA: concepts and applications in agriculture, forestry and medicine. CRC Press, Boca Raton, pp 213–236

    Google Scholar 

  41. Tuomivirta TT, Hantula J (2005) Three unrelated viruses occur in a single isolate of Gremmeniella abietina var. abietina type A. Virus Res 110:31–39

    Article  PubMed  CAS  Google Scholar 

  42. Hong Y, Dover SL, Cole TE, Brasier CM, Buck KW (1999) Multiple mitochondrial viruses in an isolate of the Dutch Elm disease fungus Ophiostoma novo-ulmi. Virology 258:118–127

    Article  PubMed  CAS  Google Scholar 

  43. Osaki H, Nomura K, Matsumoto N, Ohtsu Y (2004) Characterization of double-stranded RNA elements in the violet root rot fungus Helicobasidium mompa. Mycol Res 108:635–640

    Article  PubMed  CAS  Google Scholar 

  44. Peever TL, Liu Y-C, Milgroom MG (1997) Diversity of hypoviruses and other double-stranded RNAs in Cryphonectria parasitica in North America. Phytopathology 87:1026–1033

    Article  PubMed  CAS  Google Scholar 

  45. Preisig O, Wingfield BD, Wingfield MJ (1998) Coinfection of a fungal pathogen by two distinct double-stranded RNA viruses. Virology 252:399–406

    Article  PubMed  CAS  Google Scholar 

  46. Park Y, James D, Punja ZK (2005) Co-infection by two distinct totivirus-like double-stranded RNA elements in Chalara elegans (Thielaviopsis basicola). Virus Res 109:71–85

    Article  PubMed  CAS  Google Scholar 

  47. Vartiamäki H, Maijala P, Uotila A, Hantula J (2008) Characterization of growth and enzyme production of Chondrostereum purpureum isolates and correlation of these characteristics with their capability to prevent sprouting of birch in field. Biol Control 47:46–54

    Article  Google Scholar 

  48. Hansen EM, Stenlid J, Johansson M (1993) Somatic incompatibility and nuclear reassortment in Heterobasidion annosum. Mycol Res 97:1223–1228

    Article  Google Scholar 

  49. Johannesson H, Stenlid J (2004) Nuclear reassortment between vegetative mycelia in natural populations of the basidiomycete Heterobasidion annosum. Fungal Genet Biol 41:563–570

    Article  PubMed  Google Scholar 

  50. Liu Y-C, Double ML, MacDonald WL, Milgroom MG (2002) Persistence of Cryphonectria hypoviruses after their release for biological control of chestnut blight in West Virginia forests. For Path 32:345–356

    Article  Google Scholar 

  51. Griffin GJ, Robbins N, Hogan EP, Farias-Santopietro G (2004) Nucleotide sequence identification of Cryphonectria hypovirus 1 infecting Cryphonectria parasitica on grafted American chestnut trees 12–18 years after inoculation with a hypovirulent strain mixture. For Path 34:33–46

    Article  Google Scholar 

  52. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the Academy of Finland (projects 122565 and 251193) and the Finnish Forest Research Institute. We thank Ms. Marja-Leena Santanen, Ms. Sonja Sarsila, Mr. Juha Lehtonen, and Ms. Christina Östman for their skillful technical assistance in the laboratory. Mr. Ari Rajala, Mr. Jonne Hakanpää, and Dr. Henna Vartiamäki are gratefully acknowledged for assisting in the design and implementation of the stump inoculation experiment. Harri, Saana, Veikko, and Pihla Vainio are cordially thanked for conducting the measurements at the study plot.

Author information

Authors and Affiliations

  1. Vantaa Research Unit, Finnish Forest Research Institute, PO Box 18, 01301, Vantaa, Finland

    Eeva J. Vainio, Tuula Piri & Jarkko Hantula

Authors
  1. Eeva J. Vainio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tuula Piri
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jarkko Hantula
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eeva J. Vainio.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vainio, E.J., Piri, T. & Hantula, J. Virus Community Dynamics in the Conifer Pathogenic Fungus Heterobasidion parviporum Following an Artificial Introduction of a Partitivirus. Microb Ecol 65, 28–38 (2013). https://doi.org/10.1007/s00248-012-0118-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0118-7

Keywords

Search

Navigation