Skip to main content
Log in

Distribution of Viruses Inhabiting Heterobasidion annosum in a Pine-Dominated Forest Plot in Southern Finland

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

An Erratum to this article was published on 18 September 2017

This article has been updated

Abstract

We investigated the diversity and spatial distribution of viruses infecting strains of the root rot fungus Heterobasidion annosum collected from pine stumps at a heavily infected forest site. Four different partitiviruses were detected in 14 H. annosum isolates at the study site, constituting approximately 29% of all Heterobasidion isolates investigated (N = 48). Two of the viruses detected were new partitiviruses designated here as Heterobasidion partitivirus 16 (HetPV16) and HetPV20, and two were previously known partitiviruses: HetPV7 and HetPV13. The two new partitiviruses found, HetPV16-an1 and HetPV20-an1, shared ~70% RdRp nucleotide sequence identity with the alphapartitivirus Rosellinia necatrix partitivirus 2, and less than 40% identity with known viruses of Heterobasidion spp. HetPV7-an1 was closely similar to HetPV7-pa1 isolated earlier from Heterobasidion parviporum, supporting the view of conspecific virus pools in different Heterobasidion species. Three fungal isolates were found to be co-infected with two different partitivirus strains (HetPV7-an1 and HetPV13-an2 or HetPV16-an1 and HetPV20-an1). Different isolates representing each host clone had variable virus compositions, and virus strains occurring in more than one host clone showed minor sequence variations between clones.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Change history

  • 18 September 2017

    An erratum to this article has been published.

References

  1. Pearson MN, Beever RE, Boine B, Arthur K (2009) Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10:115–128

  2. Ghabrial SA (2013) Advances in virus research, Vol. 86: Mycoviruses. Elsevier, San Diego

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

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

  5. MacDonald W, Fulbright D (1991) Biological control of chestnut blight: use and limitations of transmissible hypovirulence. Plant Dis 75:656–661

  6. Zhou T, Boland GJ (1997) Hypovirulence and double-stranded RNA in Sclerotinia homeocarpa. Phytopathology 87:147–153

  7. 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

  8. 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. PNAS 107:8387–8392

  9. Doherty M, Coutts RHA, Brasier CM, Buck KW (2006) Sequence of RNA-dependent RNA polymerase genes provides evidence for three more distinct mitoviruses in Ophiostoma novo-ulmi isolate Ld. Virus Genes 33:41–44

  10. Castro M, Kramer K, Valdivia L, Ortiz S, Castillo A (2003) A new double-stranded RNA mycovirus confers hypovirulence-associated traits Botrytis cinerea. FEMS Microbiol Lett 228:87–91

  11. Wu MD, Zhang L, Li GQ, Jiang DH, Hou MS, Huang HC (2007) Hypovirulence and double-stranded RNA in Botrytis cinerea. Phytopathology 97:1590–1599

  12. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515

  13. Woodward S, Stenlid J, Karjalainen R, Hütterman A (1998) Heterobasidion annosum—biology, ecology, impact and control. CAB International, Wallingford,

    Google Scholar 

  14. Korhonen K, Capretti P, Karjalainen R, Stenlid J (1998) Distribution of Heterobasidion annosum intersterility groups in Europe. In: Woodward S, Stenlid J, Karjalainen R, Hüttermann A (eds) Heterobasidion annosum—biology, ecology, impact and control. CAB International, Wallingford, pp. 93–104

    Google Scholar 

  15. Redfern DB, Stenlid J (1998) Spore dispersal and infection. In: Woodward S, Stenlid J, Karjalainen R, Hüttermann A (eds) Heterobasidion annosum—biology, ecology, impact and control. CAB International, Wallingford, pp. 105–124

    Google Scholar 

  16. Garbelotto M, Gonthier P (2013) Biology, epidemiology, and control of Heterobasidion species worldwide. Annu Rev Phytopathol 51:39–59

  17. Vainio EJ, Hantula J (2016) Taxonomy, biogeography and importance of Heterobasidion viruses. Virus Res 219:2–10

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

  19. Ihrmark K, Zheng J, Stenström E, Stenlid J (2001) Presence of double-stranded RNA in Heterobasidion annosum. For Pathol 31:387–394

  20. 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

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

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

  23. Vainio EJ, Piri T, Hantula J (2013) Virus community dynamics in the conifer pathogenic fungus Heterobasidion parviporum following an artificial introduction of a partitivirus. Microb Ecol 65:28–38

  24. Vainio EJ, Capretti P, Motta E, Hantula J (2013) Molecular characterization of HetRV8-ir1, a partitivirus of the invasive conifer pathogenic fungus H. irregulare. Arch Virol 158:1613–1615

  25. Vainio EJ, Jurvansuu J, Streng J, Rajamäki ML, Hantula J, Valkonen JPT (2015) Diagnosis and discovery of fungal viruses using deep sequencing of small RNAs. J Gen Virol 96:714–725

  26. Kashif M, Hyder R, De Vega PD, Hantula J, Vainio EJ (2015) Heterobasidion wood decay fungi host diverse and globally distributed viruses related to Helicobasidium mompa partitivirus V70. Virus Res 195:119–123

  27. Hyder R, Pennanen T, Hamberg L, Vainio EJ, Piri T, Hantula J (2013) Two viruses of Heterobasidion confer beneficial, cryptic or detrimental effects to their hosts in different situations. Fungal Ecol 6:387–396

  28. Jurvansuu J, Kashif M, Vaario L, Vainio EJ, Hantula J (2014) Partitiviruses of a fungal forest pathogen have species-specific quantities of genome segments and transcripts. Virology 462:25–33

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

  30. Vainio EJ, Pennanen T, Rajala T, Hantula J (2017) Occurence of similar mycoviruses in pathogenic, saprotrophic and mycorrhizal fungi inhabiting the same forest stand. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fix003

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

  32. Melzer MS, Ikeda SS, Boland GJ (2002) Interspecific transmission of double-stranded RNA and Hypovirulence from Sclerotinia sclerotiorum to S. minor. Phytopathology 92:780–784

  33. Liu Y, Linder-Basso D, Hillman B, Kaneko S, Milgroom M (2003) Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Mol Ecol 12:1619–1628

  34. Vainio EJ, Müller MM, Korhonen K, Piri T, Hantula J (2015) Viruses accumulate in aging infection centers of a fungal forest pathogen. ISME J 9:497–507

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

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

  37. 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

  38. Lambden PR, Cooke SJ, Caul EO, Clarke IN (1992) Cloning of noncultivatable human rotavirus by single primer amplification. J Virol 66:1817–1822

  39. Rishbeth J (1951) Observations on the biology of Fomes annosus, with particular reference to east Anglian pine plantations: III. Natural and experimental infection of pines, and some factors affecting severity of the disease. Ann Bot 15:221–246

  40. Gibbs JN (1967) The role of host vigor in the susceptibility of pines to Fomes annosus. Ann Bot 31:803–815

  41. Piri T (2000) Response of compensatory-fertilized Pinus sylvestris to infection by Heterobasidion annosum. Scand J For Res 15:218–224

  42. Chiba S, Lin YH, Kondo H, Kanematsu S, Suzuki N (2013) Effects of defective interfering RNA on symptom induction by, and replication of, a novel partitivirus from a phytopathogenic fungus, Rosellinia necatrix. J Virol 87:2330–2341

  43. Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ, Jiang D, Suzuki N (2014) Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res 188:128–141

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

  45. Drenkhan T, Sibul I, Kasanen R, Vainio EJ (2013) Viruses of Heterobasidion parviporum persist within their fungal host during passage through the alimentary tract of Hylobius abietis. For Pathol 43:317–323

  46. Liu S, Xie J, Cheng J, Li B, Chen T, Fu Y, Li G, Wang M, Jin H, Wan H, Jiang D (2016) Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. PNAS 113(45):12803–12808

  47. Ikeda KI, 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

  48. Yaegashi H, Nakamura H, Sawahata T, Sasaki A, Iwanami Y, Ito T, Kanematsu S (2013) Appearance of mycovirus-like double-stranded RNAs in the white root rot fungus, Rosellinia necatrix, in an apple orchard. FEMS Microbiol Ecol 83:49–62

  49. 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

  50. Kim JW, Choi EY, Lee JI (2005) Genome organization and expression of the Penicillium stoloniferum virus F. Virus Genes 31:175–183

  51. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

Download references

Acknowledgments

We are grateful to Juha Puranen, Marja-Leena Santanen, Ari Rajala, Minna Oksanen, Sonja Sarsila, Päivi Räisänen, and Belen Espinoza for technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rafiqul Hyder.

Ethics declarations

Funding

The study was funded by the Academy of Finland (decision numbers 251193 and 258520).

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

The nucleotide sequence data reported are available in the GenBank databases under the accession numbers: KY859973-KY859980 and KY911256-KY911275.

An erratum to this article is available at https://doi.org/10.1007/s00248-017-1067-y.

Electronic supplementary material

Supplementary Table 1

(PDF 117 kb)

Fig. S1

(PDF 232 kb)

Fig. S2

(PDF 241 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hyder, R., Piri, T., Hantula, J. et al. Distribution of Viruses Inhabiting Heterobasidion annosum in a Pine-Dominated Forest Plot in Southern Finland. Microb Ecol 75, 622–630 (2018). https://doi.org/10.1007/s00248-017-1027-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1027-6

Keywords

Navigation