Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses

Mata, Carlos P.; Luque, Daniel; Gómez-Blanco, J.; Rodrı́guez, Javier M.; González, José M.; Suzuki, Nobuhiro; Ghabrial, Said A.; Carrascosa, José L.; Trus, Benes L.; Castón, José R.

doi:10.1371/journal.ppat.1006755

Cited by 27 publications

(39 citation statements)

References 63 publications

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“…All dsRNA viruses in this branch share a unique virion organization and encode homologous CPs. In particular, the specialized icosahedral capsids of these viruses, involved in transcription and replication of the dsRNA genome inside cells, are constructed from 60 homo-or heterodimers of CP subunits organized on an unusual T=1 (also known as pseudo-7=2) lattice (69, 91). The only exception are the chrysoviruses which encode large CPs corresponding to the CP dimers of other dsRNA viruses and form genuine T=1 capsids (92).…”

Section: Resultsmentioning

confidence: 99%

Origins and Evolution of the Global RNA Virome

Dolja¹,

Wolf

Kazlauskas³

et al. 2018

Preprint

118

197

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Viruses with RNA genomes dominate the eukaryotic virome, reaching enormous diversity in animals and plants. The recent advances of metaviromics prompted us to perform a detailed phylogenomic reconstruction of the evolution of the dramatically expanded global RNA virome. The only universal gene among RNA viruses is the RNA-dependent RNA polymerase (RdRp). We developed an iterative computational procedure that alternates the RdRp phylogenetic tree construction with refinement of the underlying multiple sequence alignments. The resulting tree encompasses 4,617 RNA virus RdRps and consists of 5 major branches, 2 of which include positive-sense RNA viruses, 1 is a mix of positive-sense (+) RNA and double-stranded (ds) RNA viruses, and 2 consist of dsRNA and negative-sense (−) RNA viruses, respectively. This tree topology implies that dsRNA viruses evolved from +RNA viruses on at least two independent occasions, whereas -RNA viruses evolved from dsRNA viruses. Reconstruction of RNA virus evolution using the RdRp tree as the scaffold suggests that the last common ancestors of the major branches of +RNA viruses encoded only the RdRp and a single jelly-roll capsid protein. Subsequent evolution involved independent capture of additional genes, particularly, those encoding distinct RNA helicases, enabling replication of larger RNA genomes and facilitating virus genome expression and virus-host interactions. Phylogenomic analysis reveals extensive gene module exchange among diverse viruses and horizontal virus transfer between distantly related hosts. Although the network of evolutionary relationships within the RNA virome is bound to further expand, the present results call for a thorough reevaluation of the RNA virus taxonomy.IMPORTANCEThe majority of the diverse viruses infecting eukaryotes have RNA genomes, including numerous human, animal, and plant pathogens. Recent advances of metagenomics have led to the discovery of many new groups of RNA viruses in a wide range of hosts. These findings enable a far more complete reconstruction of the evolution of RNA viruses than what was attainable previously. This reconstruction reveals the relationships between different Baltimore Classes of viruses and indicates extensive transfer of viruses between distantly related hosts, such as plants and animals. These results call for a major revision of the existing taxonomy of RNA viruses.

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Section: Resultsmentioning

confidence: 99%

Origins and Evolution of the Global RNA Virome

Dolja¹,

Wolf

Kazlauskas³

et al. 2018

Preprint

118

197

View full text Add to dashboard Cite

show abstract

“…All dsRNA viruses in this branch share a unique virion organization and encode homologous CPs. In particular, the specialized icosahedral capsids of these viruses, involved in transcription and replication of the dsRNA genome inside cells, are constructed from 60 homo-or heterodimers of CP subunits organized on an unusual Tϭ1 (also known as pseudo-Tϭ2) lattice (69,91). The only exceptions are the chrysoviruses, which encode large CPs corresponding to the CP dimers of other dsRNA viruses and form genuine Tϭ1 capsids (92).…”

Section: Evolution Of the 5 Major Branches Of Rna Viruses And Reconstmentioning

confidence: 99%

Origins and Evolution of the Global RNA Virome

Wolf

Kazlauskas

Iranzo

et al. 2018

mBio

432

333

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Viruses with RNA genomes dominate the eukaryotic virome, reaching enormous diversity in animals and plants. The recent advances of metaviromics prompted us to perform a detailed phylogenomic reconstruction of the evolution of the dramatically expanded global RNA virome. The only universal gene among RNA viruses is the gene encoding the RNA-dependent RNA polymerase (RdRp). We developed an iterative computational procedure that alternates the RdRp phylogenetic tree construction with refinement of the underlying multiple-sequence alignments. The resulting tree encompasses 4,617 RNA virus RdRps and consists of 5 major branches; 2 of the branches include positive-sense RNA viruses, 1 is a mix of positive-sense (ϩ) RNA and double-stranded RNA (dsRNA) viruses, and 2 consist of dsRNA and negative-sense (Ϫ) RNA viruses, respectively. This tree topology implies that dsRNA viruses evolved from ϩRNA viruses on at least two independent occasions, whereas ϪRNA viruses evolved from dsRNA viruses. Reconstruction of RNA virus evolution using the RdRp tree as the scaffold suggests that the last common ancestors of the major branches of ϩRNA viruses encoded only the RdRp and a single jelly-roll capsid protein. Subsequent evolution involved independent capture of additional genes, in particular, those encoding distinct RNA helicases, enabling replication of larger RNA genomes and facilitating virus genome expression and virus-host interactions. Phylogenomic analysis reveals extensive gene module exchange among diverse viruses and horizontal virus transfer between distantly related hosts. Although the network of evolutionary relationships within the RNA virome is bound to further expand, the present results call for a thorough reevaluation of the RNA virus taxonomy. IMPORTANCE The majority of the diverse viruses infecting eukaryotes have RNA genomes, including numerous human, animal, and plant pathogens. Recent advances of metagenomics have led to the discovery of many new groups of RNA viruses in a wide range of hosts. These findings enable a far more complete reconstruction of the evolution of RNA viruses than was attainable previously. This reconstruction reveals the relationships between different Baltimore classes of viruses and indicates extensive transfer of viruses between distantly related hosts, such as plants and animals. These results call for a major revision of the existing taxonomy of RNA viruses.

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“…They have also been described for members of the family Cystoviridae —bacteriophages that infect the prokaryote Pseudomonas syringae [ 25 , 26 ]. Members of the Toti- [ 27 , 28 , 29 ], Partiti- [ 30 , 31 ], Megabirna- [ 32 ], Chryso- [ 33 , 34 , 35 ], and Quadriviridae [ 36 , 37 ] families, which infect unicellular and simple eukaryotes, such as fungi, protozoa, but also some plants, also have these capsids. Members of the family Birnaviridae, which infect vertebrates, mollusks, insects, and rotifers, are exceptions, since they lack the T = 1 core of 60 CP dimers [ 38 , 39 ].…”

Section: Introductionmentioning

confidence: 99%

“…To date, 14 T = 1 capsid proteins have been resolved at the atomic level ( Figure 1 ): VP3 of orbivirus bluetongue virus (BTV) [ 4 ], λ1 of reovirus (genus Orthoreovirus ) [ 42 ], P3 of rice dwarf virus (RDV) [ 43 ], VP1 of cytoplasmic polyhedrosis virus (CPV) [ 20 ], VP2 of rotavirus [ 44 ], and VP3 of grass carp reovirus (GCRV) [ 23 ] (these last six viruses are all members of Reoviridae), CP of picobirnavirus (PBV) [ 24 ], ϕ6 P1 [ 45 ] and ϕ8 P1 [ 46 ] of the family Cystoviridae , Gag of the yeast virus ScV-L-A [ 27 ] (family Totiviridae), CP of Penicillium chrysogenum virus (PcV, family Chrysoviridae) [ 47 ], CP of Penicillium stoloniferum virus F (PsV-F, family Partitiviridae) [ 30 ], and the heterodimer P2–P4 of Rosellinia necatrix quadrivirus 1 (RnQV1, family Quadriviridae) [ 37 ]. The amino acid sequences of the above 14 CPs are quite different.…”

Section: Introductionmentioning

confidence: 99%

Capsid Structure of dsRNA Fungal Viruses

Luque

Mata

Suzuki

et al. 2018

Viruses

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Most fungal, double-stranded (ds) RNA viruses lack an extracellular life cycle stage and are transmitted by cytoplasmic interchange. dsRNA mycovirus capsids are based on a 120-subunit T = 1 capsid, with a dimer as the asymmetric unit. These capsids, which remain structurally undisturbed throughout the viral cycle, nevertheless, are dynamic particles involved in the organization of the viral genome and the viral polymerase necessary for RNA synthesis. The atomic structure of the T = 1 capsids of four mycoviruses was resolved: the L-A virus of Saccharomyces cerevisiae (ScV-L-A), Penicillium chrysogenum virus (PcV), Penicillium stoloniferum virus F (PsV-F), and Rosellinia necatrix quadrivirus 1 (RnQV1). These capsids show structural variations of the same framework, with 60 asymmetric or symmetric homodimers for ScV-L-A and PsV-F, respectively, monomers with a duplicated similar domain for PcV, and heterodimers of two different proteins for RnQV1. Mycovirus capsid proteins (CP) share a conserved α-helical domain, although the latter may carry different peptides inserted at preferential hotspots. Insertions in the CP outer surface are likely associated with enzymatic activities. Within the capsid, fungal dsRNA viruses show a low degree of genome compaction compared to reoviruses, and contain one to two copies of the RNA-polymerase complex per virion.

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Acquisition of functions on the outer capsid surface during evolution of double-stranded RNA fungal viruses

Cited by 27 publications

References 63 publications

Origins and Evolution of the Global RNA Virome

Origins and Evolution of the Global RNA Virome

Origins and Evolution of the Global RNA Virome

Capsid Structure of dsRNA Fungal Viruses

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