Virus Research 195 (2015) 119–123

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Heterobasidion wood decay fungi host diverse and globally distributed viruses related to Helicobasidium mompa partitivirus V70 M. Kashif ∗ , R. Hyder, D. De Vega Perez 1 , J. Hantula, E.J. Vainio Finnish Forest Research Institute, Vantaa Research Unit, PO Box 18, 01301 Vantaa, Finland

a r t i c l e

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Article history: Received 4 July 2014 Received in revised form 5 September 2014 Accepted 6 September 2014 Available online 16 September 2014 Keywords: Partitiviridae Heterobasidion annosum H. parviporum H. irregulare Interspecies transmission Co-infection

a b s t r a c t Viruses of the Partitiviridae family occur at a relatively low frequency in the fungal genus Heterobasidion, but show high genetic diversity. Here, we describe four novel partitivirus species that infect three Heterobasidion species that are pathogens of conifers: H. annosum, H. parviporum and H. irregulare. We show that these viruses, designated Heterobasidion partitivirus 12 (HetPV12), HetPV13, HetPV14 and HetPV15, form a phylogenetically distinct clade together with the previously described Heterobasidion partitivirus 3 (HetPV3) found in the H. insulare species complex and Helicobasidium mompa partitivirus V70, both members of the genus Alphapartitivirus. Closely related strains of HetPV13 (over 97% polymerase identity at the nucleotide level) occur in H. annosum and H. parviporum, suggesting recent transmission of this virus species between the two fungal host species. Moreover, the occurrence of nearly identical HetPV13 strains in Finland and Poland (ca 1400 km apart) indicates that the dispersal capacity of Heterobasidion partitiviruses is high. Viruses related to HetPV3 have a global distribution but only ca 2.7% overall prevalence among isolates of Heterobasidion. In three cases, these HetPV3-related viruses co-infected their hosts with distantly related partitiviruses or Heterobasidion RNA virus 6. © 2014 Elsevier B.V. All rights reserved.

Fungal viruses (mycoviruses) are hosted by a wide range of fungal taxa, including Chytridiomycota, Zygomycota, Ascomycota and Basidiomycota (Ghabrial, 2013; Ghabrial and Suzuki, 2009; Pearson et al., 2009). These mycoviruses typically form chronic but benign infections, although some mycoviruses can mediate adverse or beneficial changes in their host fungi (Ahn and Lee, 2001; Anagnostakis and Day, 1979; Ghabrial and Suzuki, 2009; MacDonald and Fulbright, 1991; Márquez et al., 2007). Fungal viruses with double-stranded RNA (dsRNA) genomes have been classified by the International Committee on Taxonomy of Viruses (ICTV; into seven families: Chrysoviridae, Partitiviridae, Reoviridae, Endornaviridae, Megabirnaviridae, Totiviridae, and Quadriviridae. The fungal genus Heterobasidion includes some of the most destructive conifer pathogens in the boreal forest region (Niemelä and Korhonen, 1998; Ostrosina and Garbelotto, 2010; Woodward et al., 1998). This genus includes two species clusters: Heterobasidion annosum (Fr.) Bref. sensu lato and Heterobasidion insulare

∗ Corresponding author. Tel.: +358 40 8012250; fax: +358 29 532 2103. E-mail addresses:, (M. Kashif). 1 Present address: The James Hutton Institute, Invergowrie, Dundee DD2 5DA, Scotland, UK. 0168-1702/© 2014 Elsevier B.V. All rights reserved.

(Murril) Ryvarden sensu lato. The H. annosum s. lat. complex consists of three European species (Heterobasidion parviporum, H. annosum and Heterobasidion abietinum) and two North American species (Heterobasidion irregulare and Heterobasidion occidentale) that have different but overlapping host tree ranges. The Heterobasidion insulare complex mainly consists of saprophytic species, all of which occur in Asia (Dai et al., 2003). Viruses with dsRNA genomes are found in approximately 15–17% of H. annosum s. lat. isolates in Europe and Western Asia (Ihrmark, 2001; Vainio et al., 2011a). These viruses laterally transmit between Heterobasidion strains through anastomosis (Ihrmark et al., 2002; Vainio et al., 2010, 2011a) and vertically via basidiospores and conidia (Ihrmark et al., 2002, 2004). Heterobasidion RNA virus 6 (HetRV6; taxonomically unassigned) is the most common virus species in H. annosum s. lat., and it shares relatively high polymerase sequence identity with the Curvularia thermal tolerance virus (Márquez et al., 2007; Vainio et al., 2012, 2013a). All other Heterobasidion viruses described thus far are members of the Partitiviridae family. Partitiviruses have been detected in all species of the H. annosum s. lat complex and Heterobasidion australe and Heterobasidion ecrustosum of the H. insulare complex (Ihrmark, 2001; Vainio et al., 2010, 2011a,b, 2012, 2013a,b). There are four Heterobasidion partitivirus species included in the latest taxonomy released by ICTV (Nibert et al., 2014). After some recent nomenclature changes, these species are called


M. Kashif et al. / Virus Research 195 (2015) 119–123

Fig. 1. Bayesian analysis based on the complete amino acid sequences of viral RdRp sequences, including Heterobasidion partitiviruses and related taxa. Viruses infecting Heterobasidion species are shown in bold and sequences determined in this study are indicated by star symbols. GenBank accession numbers are shown in parentheses. White clover cryptic virus 1 is the type species of Alphapartitivirus, and Atkinsonella hypoxylon virus is the type species of Betapartitivirus (Pepper cryptic virus 1 was used as an outgroup and is the type species in the genus Deltapartitivirus, whereas Penicillium stoloniferum virus S is the type species in the genus Gammapartitivirus (Nibert et al., 2014). The dendrogram was constructed using gamma among-site rate variation with 1.1 × 106 cycles for the MCMC algorithm, sampling 1 tree per 200 cycles, and discarding 105 samples as burn-in. The scale shows 0.5 substitutions per site, and the numbers at the branch nodes indicate percentage posterior probabilities.

Heterobasidion partitivirus 1 (HetPV1; Vainio et al., 2011a), HetPV2 (Vainio et al., 2011b), HetPV3 (Vainio et al., 2010), and HetPV8 (Vainio et al., 2013a) and encompass two genomic segments encoding genes for a RNA-dependent RNA polymerase (RdRp) of 585-722 amino acids (aa) and a capsid protein (CP) of 510-659 aa. Several partial partitivirus genome sequences further support the view that Heterobasidion partitiviruses are polyphyletic and highly diverse (Ihrmark, 2001; Vainio et al., 2011b, 2014). It should be noted that most Heterobasidion partitiviruses were formerly known as Heterobasidion RNA viruses, but we use the new nomenclature for all of the viruses here. To further understand the diversity of partitiviruses infecting Heterobasidion spp., we focused on viruses related to a previously described species, HetPV3, which has been observed in only a single isolate of an East Asian saprotrophic species (Vainio et al., 2010). Here, we describe the genome sequences (three complete and one partial) of four novel partitivirus species that infect three different conifer pathogenic species of the H. annosum s. lat species complex. We show (Fig. 1) that these viruses are globally distributed but form an independent clade with known partitiviruses, the previously described HetPV3 in the H. insulare species complex and Helicobasidium mompa partitivirus V70 (HmPV-V70; Osaki et al., 2002), which is referred to as the ‘HetPV3-related virus clade’ below.

The isolates used in this study originated from Europe and North America (Table 1). Three of the virus-positive isolates were detected during an earlier study (Vainio et al., 2011a). The four remaining strains were found during the examination of 80 isolates of H. annosum and 41 isolates of H. parviporum from Finland and 5 isolates of H. irregulare from North America (Vainio, Hyder, Poimala and Hamberg, unpublished; Table S1). The total number of Heterobasidion strains included in the analysis is 400. CF11 cellulose affinity chromatography was used to extract viral dsRNA from the Heterobasidion isolates as previously described (Morris and Dodds, 1979; Tuomivirta et al., 2002; Vainio et al., 2010), and the dsRNAs were visualized by agarose gel electrophoresis (Fig. S1). For cloning and sequence analysis, dsRNA bands were extracted and purified from the gel using the RNaid Kit (Bio 101; CA, USA). The single primer amplification technique (Lambden et al., 1992) was used with some modifications (Tuomivirta and Hantula, 2003; Vainio et al., 2011a) to determine dsRNA sequences from H. annosum 94221, 94233 and S45-8, H. irregulare 57002, and H. parviporum 95122. After adapter ligation, reverse transcription (RT), RT-PCR and cloning were performed as previously described (Vainio et al., 2011a). The cloned inserts were sequenced at Macrogen Inc., South Korea ( Missing sequence regions, insufficiently covered sequence positions

M. Kashif et al. / Virus Research 195 (2015) 119–123


Table 1 Viral strains described in this study, sequence characteristics and collection data. Virus strain Host isolate GenBank accession Host species Host tree Location

HetPV12-an1 94221 KF963175 KF963176 H. annosum Pinus sylvestris Poland, Wielun

HetPV13-an1 94233 KF963177 KF963178 H. annosum Pinus sylvestris Poland, Krucz

HetPV13-an2 S45-8 KF963179 KF963180 H. annosum Pinus sylvestris Finland, Läyliäinen

HetPV13-an3 05003 KF963181 KF963182 H. annosum Pinus sylvestris Finland, Siuntio

HetPV13-pa1 1R41 KF963183 KF963184 H. parviporum Picea abies Finland, Ruotsinkylä

HetPV14-ir1 57002 KF963185 NAa H. irregulare Pinus elliottii USA, Georgia, Cochrane

Collector (s)

P. Lakomy

P. Lakomy

J.S. Boyce Jr.

1994 1884e 1806e

1994 1873e 1776e

2004 1034f 839f

1957 1886e NAa

1995 1882e 1791e


585 aa (1758 bp) 520 aa (1563 bp) 68.72 56.99 72 bp 97 bp 54 bp 146 bp 25 bp 25 bp 90.3% 24.8% UGA UAG 47.50 51.83

581 aa (1746 bp) 509 aa (1530 bp) 68.3 55.88 78 bp 88 bp 49 bp 158 bp 19 bp 38 bpc 81% 21.7% UAA UGA 47.84 51.24

581 aa (1746 bp) 509 aa (1530 bp) 68.27 55.82 78 bp 88 bp 48 bp 157 bp 18 bp 37 bp 86.1% 23.1% UAA UGA 47.60 51.15

H. Schneider, K. Lipponen 2005 1045f 1108f (PS) 329 (990 bp) 269 (808 bp) NDb ND ND ND ND ND ND ND ND ND ND ND ND ND

T. Piri


T. Piri, H. Nuorteva 2006 1872e 1775e

HetPV15-pa1 95122 KF963186 KF963187 H. parviporum Picea abies Russia, Sverdlovsk, Pervouralsk K. Korhonen et al.

318 aa (957 bp) 217 aa (656 bp) ND ND ND ND ND ND ND ND ND ND ND ND ND ND

583 aa (1752 bp)

581 aa (1746 bp) 512 aa (1539 bp) 68.42 56.44 78 bp 102 bp 58 bp 150 bp 23 bp 40 bp 89.7% 27.9% UGA UAG 46.8 50.08

Collection year Length (bp)

ORF (aa) M (kDA) 3 UTR 5 UTR poly(A) at 3 UTR sequence identity RdRp/CP UTRd Stop codon GC-content% a b c d e f


68.55 NA 78 bp NA 56 bp NA 21 bp NA ND ND UGA NA 42.8 NA

NA = the capsid sequence for virus strain HetPV14-ir1 has not been determined. ND = sequence characteristics were not determined due to partial sequence. poly(A) tail in CP for HetPV13-an1 was not interrupted, all other poly(A) tails were interrupted. Similarity of the conserved terminal sequences (5 and 3 ends) in segments RdRp and CP. complete sequences. partial sequences.

and sequence ends were determined using specific primers (Table S2) as previously described (Vainio et al., 2011a, 2013b). The NCBI OrFinder program ( was used to determine open reading frames for acquired nucleotide sequences (Table 1). The deduced amino acid sequences were analyzed using NCBI Protein Blast to find similar sequences (Table S3). Nucleotide and protein sequence alignments were constructed using Geneious Pro version 6.1.6 (; Biomatters Ltd.) and MAFFT multiple aligner (version 7.017). The RdRp nucleotide sequence alignment was used for dendrogram construction by the MEGA5.1 neighbor-joining clustering algorithm (Tamura et al., 2011). RdRp and CP protein sequence alignments were analyzed by MrBayes in Geneious Pro 5.5.8. Based on model testing with ProtTest (Abascal et al., 2005), the substitution models Blosum and VT were selected for the RdRp and CP protein alignments, respectively. Complete partitivirus genome sequences were determined from isolates 94221, 94233, S45-8 and 95122, and partial sequences were obtained for isolates 57002, 05003 and 1R41. Virus infections in H. annosum 05003 and H. parviporum 1R41 were detected by RTPCR using RdRp consensus primers (HV3ConF1 and HV3ConRe1) designed based on pre-existing sequences of HetPV3-ec1, HetPV13an1, HetPV15-pa1 and the HmPV-V70 (Table S2). A capsid protein segment from isolate 57002 was not found despite several cloning/sequencing attempts. Sequence characteristics and GenBank accession numbers are summarized in Table 1. A BlastP conserved motif search revealed that polymerase genes from all virus species described in this study included conserved domains similar to the protein sub-family cd01699 (E-values ≤ 0.02) or the pfam02123 sub-family (E-values ≤ 9.17−04 ). The locations of conserved RdRp gene sequence motifs 3–8, as determined by

Bruenn (1993), are indicated in Table S4. No conserved motifs were detected in the CP gene sequences. The UTR terminal sequences of the two genome segments from each virus species were highly conserved (81–90.3%) in the 5 UTR and less conserved (21.7–27.9%) in the 3 UTR (Table 1). A high conservation of terminal regions has also been reported for other partitiviruses (Hacker et al., 2006; Lim et al., 2005; Tuomivirta and Hantula, 2003), and these sequence similarities may play an important role in the recognition characteristics of RdRp in virus replication (Buck, 1996). All virus species contained interrupted or noninterrupted poly(A) tails at the 3 ends of their genome segments (Table 1). According to ICTV, the species demarcation criteria for partitiviruses are ≤90% aa-sequence identity in the RdRp and/or ≤80% aa-sequence identity in the CP (Nibert et al., 2014). Accordingly, we identified four distinct putative partitivirus species: Heterobasidion partitivirus 12, 13, 14 and 15. We designated the partitivirus strains with species abbreviations (e.g., HetPV12), followed by a two-letter suffix indicating the host species (an = H. annosum; ir = H. irregulare; pa = H. parviporum) and strain number. The observed viruses occurred in the plant pathogenic species H. annosum, H. parviporum or H. irregulare extending the distribution of the HetPV3-related virus clade to the H. annosum s. lat. species cluster. HetPV12, HetPV14 and HetPV15 were represented by only one strain, whereas there were four conspecific strains of HetPV13 (HetPV13-an1, HetPV13-an2, HetPV13-an3 and HetPV13-pa1) with high sequence identity (97.2–98.3% RdRp and 94.8–97.5% CP identity at the nucleotide (nt) level, Table S5). HetPV12, HetPV13, HetPV14 and HetPV15 shared 52.6–67.6% identity with RdRp and 27.4–28.3% of CP identity based on complete protein sequences. Notably, the CP sequence identity between HetPV12-an1 and the previously described HetPV3-ec1 was considerably higher (73.7%)


M. Kashif et al. / Virus Research 195 (2015) 119–123

at the protein level, suggesting a close phylogenetic relationship between these two viral species (Table S5), which were isolated from two different Heterobasidion species clusters and different continents (Europe and Asia). Based on these analyses, it appears as though there is no geographical or phylogenetic differentiation among viruses related to HetPV3, which agrees with the view of Heterobasidion partitiviruses being globally dispersed (Vainio et al., 2011a). Both the Bayesian RdRp and CP dendrograms (Fig. 1 and S2, respectively) and the neighbor-joining dendrogram of the RdRp nucleotide sequences (Fig. S3) confirmed the close association between the conspecific HetPV13 strains and the close resemblance between HetPV12-an1 and HetPV3-ec1. All of the species determined in this study associated with the proposed genus Alphapartitivirus. The genome sizes of HetPV3-related viruses are among the smallest for Partitiviridae and typical for the proposed genus Alphapartitivirus. Only selected species of the genus Alphapartitivirus were included in the CP sequence alignments used for Bayesian clustering (Fig. S2) as lower sequence identity would have prevented reliable phylogenetic inference. The only closely related species observed with BlastP and BlastN was the HmPV-V70 (Osaki et al., 2002), showing 57–67% polymerase identity at the protein level compared with sequences determined in this study (Table S3). It should be noted that Heterobasidion and Helicobasidium are significantly different phylogenetically, and Helicobasidium belongs to order Helicobasidiales, while Heterobasidion is a member of order Russulales. All other available partitivirus sequences, including those from Heterobasidion spp., were more distant (less than 43% of polymerase sequence identity). The CP sequence of HmPV-V70 is undetermined, but those of Heterobasidion partitivirus 1, Chondrostereum purpureum cryptic virus 1, Raphanus sativus cryptic virus 1, Beet cryptic virus 1 and Cherry chlorotic rusty spot associated partitivirus showed identities of 23–28% (aa level) compared with the strains determined in this study (Table S3). The global distribution of partitivirus species appears to extend even among closely related taxonomical clades of these viruses, suggesting that either these lineages are ancient or fungal viruses are more promiscuous in their hosts as commonly thought (Feldman et al., 2012). The latter possibility is supported by the inclusion of HmPV-V70 within the HetPV3-related virus clade. Interspecies virus transmission is considered to be a rare phenomenon among mycoviruses; however, Deng and Boland (2007) reported natural transmission of the betapartitivirus Ceratocystis resinifera virus 1 to Ceratocystis polonica. Recently the partitivirus strain Sclerotinia sclerotiorum partitivirus 1 (SsPV1/WF-1) was found to interspecifically transmitted to Sclerotinia nivalis and Sclerotinia minor (Xiao et al., 2014). In Heterobasidion species, Ihrmark et al. (2002, 2004) showed that certain Heterobasidion partitiviruses transmitted from H. parviporum to H. annosum and H. occidentale via hyphal contacts. Moreover, Vainio et al. (2010) showed that HetPV3 can be similarly transmitted from H. ecrustosum to H. abietinum and H. occidentale. In addition, nearly identical strains of HetPV1 were found in H. parviporum and H. australe within the same region of Bhutan, which suggests natural interspecies transmission (Vainio et al., 2011a). The occurrence of the virus species HetPV13 in H. annosum and H. parviporum suggests recent transmission of this virus between the two fungal species, supporting the view that interspecies transmission is a common phenomenon for viruses infecting Heterobasidion spp. (Vainio et al., 2011b, 2012). Preliminary results also suggest the transfer of HetPV13 from H. annosum to H. parviporum under laboratory conditions (Vainio et al., in preparation). In addition, it is possible that the host range of HetPV13 expands also into other species of Heterobasidion. Moreover, the occurrence of nearly identical HetPV13 strains in Finland and Poland (ca 1400 km apart; Table 1) indicates that the dispersal capacity of these viruses is high, which

agrees with the lack of highly differentiated populations of the host fungus (H. annosum) in Europe (Stenlid et al., 1994). However, the collective infection frequency of the HetPV3-related virus clade in our culture collection was only ca 2.7% (including HetPV3-ec1). During this study, we observed two cases of partitiviruses forming co-infections in a single host isolate. H. annosum S45-8 harbored HetPV13-an2 and the partitivirus strain HetPV7-an1 (Hyder et al., unpublished), and H. irregulare 57002 hosted HetPV14-ir1 and a partitivirus resembling Rosellinia necatrix partitivirus 2 (Chiba et al., 2013). Another Heterobasidion strain, 05003, was co-infected by HetPV13-an3 and a strain of the virus HetRV6 (GenBank accession KF963188) – a condition observed also before (Vainio et al., 2013b). Interestingly, the H. irregulare isolate 57002 containing HetPV14ir1 dates from 1957, suggesting that partitivirus infections may be remarkably stable. Most partitiviruses are considered to form cryptic persistent infections in their host fungi. In the case of Heterobasidion partitiviruses, the effects of HetPV3-ec1 on the growth of different host fungi (H. ecrustosum, H. abietinum and H. occidentale) were temperature dependent, and H. occidentale appeared to be more vulnerable to the effects of HetPV3-ec1 infection than the natural host (Jurvansuu et al., 2014). Moreover, Hyder et al. (2013) demonstrated that HetPV3-ec1 mediates different effects on different Heterobasidion host strains, and it may have beneficial, cryptic or detrimental effects on a single host isolate depending on ecological conditions. Finally, Jurvansuu et al. (2014) showed that the genome segment ratio and transcription regulation of HetPV3 differs from some other Heterobasidion partitiviruses. The ecological role of the new viruses described here remain to be investigated, but based on current knowledge, the HetRV3-related virus clade might be one of the most interesting groups from this point of view. Based on ICTV criteria, previously published Heterobasidion partitiviruses can be classified into two major phylogenetic groups: the virus species HetPV1, HetPV3, HetPV4, HetPV5 and HaV belong to the genus Alphapartitivirus, and HetPV2, HetPV7, HetPVP and HetPV8 are grouped in Betapartitivirus (Fig. 1; Nibert et al., 2014). In this study, phylogenetic analysis revealed a highly supported clade including the newly described virus species together with HetPV3 and HmPV-V70. This study extends our view of HetPV3-related Heterobasidion partitiviruses from one strain observed only in East Asian H. insulare s. lat. to a virus group universally distributed but at low frequency among Heterobasidion species in Europe, East Asia and North America. The diversity of these viruses is considerable and allowed us to group the viruses into five putative species, three of which are described here for the first time with their complete sequence and one with only its RdRp sequence. Acknowledgments We gratefully acknowledge M.-L. Santanen and S. Sarsila for skillful technical assistance. We thank Dr. Leena Hamberg and Dr. Anna Rytkönen for their help with virus screening. This work was supported by the Academy of Finland (decision numbers 122565, 251193, and 258520) and the Finnish Forest Research Institute. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at 2014.09.002. References Abascal, F., Zardoya, R., Posada, D., 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.

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Heterobasidion wood decay fungi host diverse and globally distributed viruses related to Helicobasidium mompa partitivirus V70.

Viruses of the Partitiviridae family occur at a relatively low frequency in the fungal genus Heterobasidion, but show high genetic diversity. Here, we...
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