Abstract

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.

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