The wide distribution of endornaviruses, large double-stranded RNA replicons with plasmid-like properties

Fukuhara, Teruyuki; Koga, Ryuichi; Aoki, Nanako; Yuki, C.; Yamamoto, Nobushige; Oyama, Noboru; Udagawa, Tsuyoshi; Horiuchi, Hideki; Miyazaki, Saori; Higashi, Yoshikazu; Takeshita, M; Ikeda, Kenichi; Arakawa, Masao; Matsumoto, Naoyuki; Moriyama, Hiromitsu

doi:10.1007/s00705-005-0688-5

Cited by 73 publications

(65 citation statements)

References 24 publications

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“…Almost all of the 14 000-18 000 nucleotides comprising endornavirus genomes code for a putative polyprotein and exhibit a characteristic nick near the 59 end of the coding strand. Similar putative viruses have been found in the Stramenopila (Phytophthora; Hacker et al, 2005) and in the basidiomycete Helicobasidium mompa (Fukuhara et al, 2005;Osaki et al, 2006), both of which are pathogens of plants.…”

Section: Introductionsupporting

confidence: 64%

A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities

Tuomivirta¹,

Kaitera²,

Hantula³

2009

Journal of General Virology

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A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities Ascospore and mycelial isolates of Gremmeniella abietina type B were found to contain three different dsRNA molecules with approximate lengths of 11, 5 and 3 kb. The 11 kb dsRNA encoded the genome of a putative virus and is named Gremmeniella abietina type B RNA virus XL (GaBRV-XL). GaBRV-XL probably exists in an unencapsulated state. We identified two distinct dsRNAs (10 374 and 10 375 bp) of GaBRV-XL, both of which coded for the same putative polyprotein (3249 amino acids) and contained four regions similar to putative viral methyltransferases, DExH box helicases, viral RNA helicase 1 and RNA-dependent RNA polymerases. While a cysteine-rich region with several CxCC motifs in GaBRV-XL was similar to that of putative endornaviruses, cluster analyses of conserved regions revealed GaBRV-XL to be distinct from a broad range of viral taxa but most closely related to Discula destructiva virus 3. Collectively, these findings suggest that GaBRV-XL represents a novel virus group related to endornaviruses. INTRODUCTIONRecently recognized by the International Committee on Taxonomy of Viruses (ICTVdB Management, 2006), endornaviruses are usually cryptic and non-enveloped plant and fungal dsRNA viruses that spread efficiently through mitotic and meiotic cells but not through grafts (Fukuhara et al., 1995;Moriyama et al., 1999;Wakarchuk & Hamilton, 1990;Pfeiffer, 1998 Fungal viruses of the G. abietina species complex have been studied thoroughly in type A and are known to include putative members of the virus families Narnaviridae, Totiviridae and Partitiviridae, some of which can co-infect a single fungal isolate (Tuomivirta et al., 2002;Tuomivirta & Hantula, 2005).The goals of this study include a survey of dsRNA molecules in G. abietina type B, molecular characterization of the most common dsRNA type and its comparison to representatives of similar viral taxa. METHODSG. abietina type B strains. G. abietina type B strains (see Supplementary Table S1, available in JGV Online) were identified by the random amplified microsatellite (RAMS) technique of Hantula & Müller (1997). Branches from P. sylvestris and Pinus contorta ,2 m in height (,20 years old) with symptoms of scleroderris canker were collected in artificially or naturally regenerated stands between June 1994 and June 1995 in northern Finland. Disease symptoms included death of lateral branches over several internodes, cankers, yellowgreen woody tissues, pycnidia and apothecia. Fungi were isolated either from pycnidia or from infected wood adjacent to apothecia.Nucleic acid isolation and electrophoresis. G. abietina type B isolates were grown at 20 uC on modified orange serum agar covered with a cellophane membrane (Müller et al., 1994). dsRNA isolationThe GenBank/EMBL/DDBJ accession numbers for the complete sequences of the 11 kb dsRNAs of isolates AU58 (GaBRV-XL1) and E46 (GaBRV-XL2) are respectively DQ399289 and DQ399290.Details of ...

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Section: Introductionsupporting

confidence: 64%

A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities

Tuomivirta¹,

Kaitera²,

Hantula³

2009

Journal of General Virology

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“…By contrast, in the case of the ourmiaviruses, there is no room for doubt that they really are plant viruses. Conversely, plant endornaviruses that replicate inside mitochondria seem to be derived from typical fungal, capsid-less, virus-like replicons (Fukuhara et al, 2006); essentially, endornaviruses retain the typical replication strategy of fungal RNA replicons even after the transfer to plants. The same fungal character was retained by the plant cryptoviruses (lacking an MP) in the family Partitiviridae (Fauquet et al, 2005;Rong et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin

Rastgou

Habibi

Izadpanah

et al. 2009

Journal of General Virology

118

122

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Ourmia melon virus (OuMV), Epirus cherry virus (EpCV) and Cassava virus C (CsVC) are three species placed in the genus Ourmiavirus. We cloned and sequenced their RNA genomes. The sizes of the three genomic RNAs of OuMV, the type member of the genus, were 2814, 1064 and 974 nt and each had one open reading frame. RNA1 potentially encoded a 97.5 kDa protein carrying the GDD motif typical of RNA-dependent RNA polymerases (RdRps). The putative RdRps of ourmiaviruses are distantly related to known viral RdRps, with the closest similarity and phylogenetic affinity observed with fungal viruses of the genus Narnaviridae. RNA2 encoded a 31.6 kDa protein which, expressed in bacteria as a His-tag fusion protein and in plants through agroinfiltration, reacted specifically with antibodies made against tubular structures found in the cytoplasm. The ORF2 product is significantly similar to movement proteins of the genus Tombusviridae, and phylogenetic analysis supported this evolutionary relationship. The product of OuMV ORF3 is a 23.8 kDa protein. This protein was also expressed in bacteria and plants, and reacted specifically with antisera against the OuMV coat protein. The sequence of the ORF3 protein showed limited but significant similarity to capsid proteins of several plant and animal viruses, although phylogenetic analysis failed to reveal its most likely origin. Taken together, these results indicate that ourmiaviruses comprise a unique group of plant viruses that might have evolved by reassortment of genomic segments of RNA viruses infecting hosts belonging to different eukaryotic kingdoms, in particular, fungi and plants.

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“…An intriguing example is the endornaviruses found in plants, fungi, and protists (Valverde et al 1990;Wakarchuk and Hamilton 1990;Fukuhara et al 2006), which have acquired domains with similar functions from these different hosts (Song et al 2013). Despite their distinct origins, these domains have a strict functional order within the Endornavirus genus (Roossinck et al 2011;Song et al 2013), even though they highly vary as to presence or absence.…”

mentioning

confidence: 99%

Multiple Barriers to the Evolution of Alternative Gene Orders in a Positive-Strand RNA Virus

et al. 2016

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The order in which genes are organized within a genome is generally not conserved between distantly related species. However, within virus orders and families, strong conservation of gene order is observed. The factors that constrain or promote gene-order diversity are largely unknown, although the regulation of gene expression is one important constraint for viruses. Here we investigate why gene order is conserved for a positive-strand RNA virus encoding a single polyprotein in the context of its authentic multicellular host. Initially, we identified the most plausible trajectory by which alternative gene orders could evolve. Subsequently, we studied the accessibility of key steps along this evolutionary trajectory by constructing two virus intermediates: (1) duplication of a gene followed by (2) loss of the ancestral gene. We identified five barriers to the evolution of alternative gene orders. First, the number of viable positions for reordering is limited. Second, the within-host fitness of viruses with gene duplications is low compared to the wild-type virus. Third, after duplication, the ancestral gene copy is always maintained and never the duplicated one. Fourth, viruses with an alternative gene order have even lower fitness than viruses with gene duplications. Fifth, after more than half a year of evolution in isolation, viruses with an alternative gene order are still vastly inferior to the wild-type virus. Our results show that all steps along plausible evolutionary trajectories to alternative gene orders are highly unlikely. Hence, the inaccessibility of these trajectories probably contributes to the conservation of gene order in present-day viruses.

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The wide distribution of endornaviruses, large double-stranded RNA replicons with plasmid-like properties

Cited by 73 publications

References 24 publications

A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities

A novel putative virus of Gremmeniella abietina type B (Ascomycota: Helotiaceae) has a composite genome with endornavirus affinities

Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin

Multiple Barriers to the Evolution of Alternative Gene Orders in a Positive-Strand RNA Virus

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