Capsid‐Less RNA Viruses

Abstract

Capsid‐less RNA viruses comprise an assemblage of diverse virus‐like agents with genomes of variable size that share only the gene encoding the RNA‐dependent RNA polymerase. Although double‐stranded ribonucleic acid (RNA) is the dominant form of virus‐specific RNA isolated from organisms infected by most capsid‐less viruses, these viruses probably have evolved independently from distinct positive‐strand RNA virus ancestors that have lost the ability to form capsids. The loss of capsid caused the loss of virus transmissibility via extracellular routes, limiting these agents to vertical transmission. The capsid‐less RNA viruses include the families Narnaviridae, Hypoviridae, and Endornaviridae as well as several viruses scattered among diverse viral lineages. The majority of the known capsid‐less viruses reproduce in fungi, and the rest in oomycetes and plants. The narnaviruses of the genus Mitovirus replicate within fungal mitochondria and show evolutionary affinity to RNA bacteriophages, suggesting their potential ancient origin from viruses of bacteria that gave rise to mitochondrial endosymbiont of the ancestral eukaryote. In contrast, it seems likely that the fungal hypoviruses and plant/fungal endornaviruses have emerged more recently, via reductive evolution of eukaryotic ancestral viruses of the Picornavirus‐like and Alphavirus‐like superfamilies, respectively.

Key Concepts:

  • Several groups of RNA viruses infecting fungi, plants and protists lack a capsid and replicate in the form of naked RNA.

  • Phylogenomic analysis shows that capsid‐less viruses have evolved on many independent occasions from different groups of typical positive‐strand RNA viruses.

  • The driving force behind the evolution of capsid‐less viruses appears the life style of their hosts such as fungi that hampers infectivity, even for viruses possessing a capsid, and restricts viruses to vertical transmission.

  • Numerous members of a widespread family of capsid‐less viruses, the Narnaviridae, replicate within the host mitochondria and are evolutionarily related to RNA bacteriophage, revealing a direct link between viruses of bacteria and eukaryotes.

Keywords: positive‐strand RNA viruses; double‐stranded RNA viruses; capsid‐less RNA viruses; RNA‐dependent RNA polymerase; mitochondrial viruses; virus evolution

Figure 1.

Genome architecture of naked positive‐strand RNA viruses. Rectangles denote protein‐encoding open reading frames (ORFs); shifted rectangles correspond to distinct ORFs. Coloured areas mark protein domains; identical colours denote homologous domains. Lines attached to rectangles designate terminal noncoding (untranslated) regions of the viral RNA genomes. Abbreviations: OMV‐3a, Ophiostoma mitovirus 3a; CHV‐1, Cryphonectria hypovirus 1; BPEV, Bell pepper endornavirus; GABrV‐XL1, Gremmeniella abietina type BRNAvirus XL1; GRV, Groundnut rosette virus; An, 3′‐terminal, homopolymeric poly(A) tail; GT, glycosyltransferase; Met, methyltransferase; pPro, papain‐like; protease; RdRp, RNA‐dependent RNA polymerase; S1 H, Superfamily 1 helicase; S2 H, Superfamily 2 helicase; MP, movement protein; ORF, open reading frame. Curved arrows denote autocatalytic proteolysis.

Figure 2.

Evolutionary relationships between the RdRp of capsid‐encoding and capsid‐less viruses. The schematic rootless tree is the consensus of several phylogenetic analyses (Koonin et al., ; Rastgou et al., ; Roossinck et al., ). The capsid‐less viruses are rendered in red. Abbreviations: F, Fungi; P, Plants; O, oomycetes.

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Dolja, Valerian V, and Koonin, Eugene V(Jul 2012) Capsid‐Less RNA Viruses. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023269]