Family: Fusariviridae

 

Sotaro Chiba, Nobuhiro Suzuki, Leonardo Velasco, María A. Ayllón, Shin-Yi Lee-Marzano, Liying Sun, Sead Sabanadzovic, and Massimo Turina

The citation for this ICTV Report chapter is the summary to be published as Chiba et al., (2024):

ICTV Virus Taxonomy Profile: Fusariviridae 2024, Journal of General Virology, (in press)

Corresponding author: Massimo Turina (massimo.turina@ipsp.cnr.it)
Edited by: Sead Sabanadzovic and Evelien Adriaenssens
Posted: March 2024

Summary

Fusariviridae is a family of mono-segmented, positive-sense RNA viruses with a genome size of 5.9–10.7 kb (Table 1 Fusarividae). The family Fusarividae includes 34 species, grouped in the three genera Alphafusarivirus, Betafusarivirus and Gammafusarivirus. In the vast majority of cases, genomic RNAs are bicistronic, with some exceptions where up to four predicted ORFs are present. In the bicistronic fusarivirids, the 5′-proximal ORF codes for a single protein with both RNA-directed RNA polymerase (RdRP) and RNA helicase (Hel) domains; little is known about the protein encoded by the second ORF. The 3′-terminus of the genomic RNA is generally polyadenylated. Fusarivirids do not appear to form virions; during their replication cycle they accumulate intracellularly an abundance of the replicative form of dsRNA.

Table 1 Fusariviridae. Characteristics of members of the family Fusariviridae

CharacteristicDescription
ExampleFusarium graminearum dsRNA mycovirus 1 (AY533037), species Alphafusarivirus fusarii, genus Alphafusarivirus
VirionThought to be capsidless since no virions can be purified on a sucrose density gradient
Genome5.9–10.7 kb mono-segmented positive-sense RNA
ReplicationUnknown
TranslationExpression of Fusarium graminearum dsRNA mycovirus-1 downstream ORFs is from subgenomic RNAs. No evidence for such molecules in Rosellinia necatrix fusarivirus 1
Host rangeExperimentally confirmed hosts are members of the kingdom Fungi and in one case a confirmed stramenopiles oomycetes host. Additional members of two species have been associated with peronosporaceaen stramenopiles from a metatranscriptomic sample.
TaxonomyRealm Riboviria, kingdom Orthornavirae, phylum Pisuviricota, class Duploviricetes, order Durnavirales: 3 genera and 34 species

Virion

Morphology

No true virions are associated with fusarivirids. No infectious form has been identified yet.

Nucleic acid

The members of this family characterized so far have positive-sense RNA genomes of 5.9 kb to 10.7 kb

Genome organization and replication

Viruses belonging to the family have very diverse genome organizations varying from monocistronic (Lentinula edodes fusarivirus 1) (Liu et al., 2023) or bicistronic (Rosellinia necatrix fusarivirus 1) (Zhang et al., 2014) to more complex genome organizations with 3 (Pleospora tiphycola fusarivirus 1) (Nerva et al., 2016) or 4 ORFs (Rhizoctonia solani fusarivirus 1) (Picarelli et al., 2019) (Figure 1 Fusariviridae). In all genomes, the largest ORF codes for a single protein with both RNA-directed RNA polymerase (RdRP) and RNA helicase (Hel) domains. The second ORF encodes a conserved protein with unknown function, although it contains a motif from a structural maintenance of chromosomes (SMC) protein (PDB entry code: 6YUF) (Gao et al., 2021, Sahin et al., 2021). Accessory ORFs are often genus-specific or have no detectable similarity with those of any other viruses. In the largest quadricistronic fusarivirids a second helicase domain is present in the protein encoded by ORF1, and this helicase is more similar to those of potyvirids and hypovirids, suggesting possible horizontal gene transfer between these viruses (Abdoulaye et al., 2022).

Expression of ORFs2–4 of Fusarium graminearum dsRNA mycovirus 1 (FgV1) is likely to occur through the production of subgenomic RNAs (Kwon et al., 2007).

Fusariviridae genome
Figure 1 Fusariviridae. Genome organisation of representative fusariviruses. RdRP, RNA-directed RNA polymerase domain, Hel, Helicase domain, SMC, structural maintenance of chromosomes domain.

Biology

Fusarivirids infect ascomycetes and basidiomycetes in the kingdom Fungi. Pythium ultimum RNA virus 1 infects the stramenopiles oomycetes Globisporangium ultimum (Fukunishi et al., 2021).

A Fusarium graminearum gene product, hexagonal peroxisome (Hex1) protein, was identified as necessary for efficient FgV1 replication and symptom induction (Son et al., 2013). Hex1 is a major component of the Woronin body, a peroxisome-derived organelle that prevents the extension of wound-induced damage to neighboring cells. The involvement of Hex1 was also investigated on Neurospora crassa fusarivirus 1 (NcFV1) replication in N. crassa, and no discernible effect was observed, suggesting that the involvement of Hex1 in fusarivirus replication is specific to the pathosystem F. graminearum-FgV1 (Honda et al., 2020).

A comparison of colony morphology between virus-free and virus-infected isogenic strains grown on nutrition-rich (PDA) and -poor (Vogel's) media suggests that infections of Rosellinia necatrix with RnFV1 is asymptomatic. Results were confirmed with a virulence assay that showed no significant difference between these fungal strains on apple rootstocks (Zhang et al., 2014). Lack of symptoms was also observed by transmission of the virus to two independent virus-free Sclerotinia sclerotiorum strains and one infected with Sclerotinia sclerotiorum fusarivirus 1 (SsFV1) (Liu et al., 2015). In the case of FgV1 strain SD4 (FgV1-SD4), isogenic virus-infected and virus-free strains demonstrated a role for the virus in hypovirulence by eliminating deoxynivalenol synthesis in F. graminearum (Paudel et al., 2022).

Penicillium aurantiogriseum fusari-like virus 1 (PaFV1) has been transfected into plant protoplasts but without evidence of replication in that heterologous system (Nerva et al., 2017).

Derivation of names

Fusariviridae: from the host of the first virus characterized of this family (Fusarium graminearum).

Genus demarcation criteria

Members of different genera belong to monophyletic clades in phylogenetic trees derived from an alignment of the protein that includes the RdRP domain (Figure 2 Fusariviridae).

Fusarivirdae phylogeny
Figure 2 Fusariviridae. Phylogenetic analysis of fusarivirus RdRP protein sequences. Numbers at nodes indicated percentage bootstrap support. Representative sequences of the family Hypoviridae are used as outgroup.

Species demarcation criteria

Viruses belonging to the same species are >80% identical in the full-length sequence of the protein that includes an RdRP domain.

Relationships within the family

Three major monophyletic groups, corresponding to the three genera in the family, can be identified by phylogenetic analysis of the complete sequence of the protein that includes the RdRP domain (Figure 2 Fusariviridae).

Relationships with other taxa

Deduced amino acid sequences of the RdRP and Hel domains of viruses in the family Fusariviridae place them as a distinct clade close to viruses in the family Hypoviridae (Kwon et al., 2007, Zhang et al., 2014). However, fusarivirids have a different genome organization and relative position of the RdRP and Hel domains. Furthermore, some groups of viruses that putatively code for a coat protein have been detected in metatranscriptomic studies and are basal to members of the family Hypoviridae in phylogenetic analyses. The largest of such groups (identified as f.066) is populated with fusarivirids suggesting that a coat protein could have been present in the ancestors of fusarivirds (Neri et al., 2022).

Virus nameAccession numberVirus abbreviation
Alternaria solani fusarivirus 1MW544173AsFV1
Botryosphaeria dothidea fusarivirus 2MW863557BdFV2
Botrytis cinerea fusarivirus 8OK558541BcFV8
Botrytis cinerea fusarivirus 9OK558542BcFV9
Corynespora cassiicola fusarivirus 1OL456888CcFV1
Erysiphe necator associated fusarivirus 1MN558695EnFV1
Fusarium fusarivirus 1OP729394#FuFV1
Fusarium pseudograminearum fusarivirus 1OP100308FpsFV1
Gaeumannomyces tritici fusarivirus 1MK279501GtFV1
Morchella esculenta fusarivirus 1MW965472MeFV1
Morchella esculenta fusarivirus 2MW965473MeFV2
Monilinia fructicola fusarivirus 1ON038402MfFV1
Monilinia fructicola fusarivirus 2ON038403MfFV2
Morchella importuna fusarivirus 1MK279502MiFV1
Nigrospora oryzae fusarivirus 1KU980909NoFV1
Nigrospora sphaerica fusarivirus 1MT774523NsFV1
Rhizoctonia solani fusarivirus 4MZ636366RsFV4
Rhizoctonia solani fusarivirus 5MW713065RsFV5
Rhizoctonia solani fusarivirus 6MW149059RsFV6
Setosphaeria turcica fusarivirus 1MW489564StFV1

Virus names and virus abbreviations are not official ICTV designations. 

# Sequence available October 2024, (Gao et al., 2023)