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Viroids: molecular vestiges of the RNA world

05 June 2009 — 05 June 2009 Centro de Astrobiologia CSIC-INTA

Viroids are unique systems for the study of RNA structure, function and evolution. They are the minimal RNA replicons characterized so far their genome is ten-fold smaller than that the smallest known vius RNA and they can therefore be considered in a certain sense at the frontier of life. Despite being only composed by a single-stranded circular RNA of 246-401 nt not encoding any protein, viroids contain sufficient information to infect some host plants, to manipulate their gene expression for producing a viroid progeny and, as a consequence, to incite in most cases specific diseases. In contrast to viruses, which can be essentially regarded as parasites of the translation machinery of their host, viroids are parasites of their host transcription machinery.

The approximately 30 known viroids are grouped in the families Pospiviroidae, type species Potato spindle tuber viroid (PSTVd), and Avsunviroidae, type species Avocado sunblotch viroid (ASBVd). PSTVd and ASBVd replicate and accumulate in the nucleus and the chloroplast, respectively, and the same presumably occurs with the other members of both families. This classification scheme is supported by other criteria including the presence of hammerhead ribozymes in members of the family Avsunviroidae and of a central conserved region in members of the family Pospiviroidae.

As opposed to plant viruses, which encode proteins that mediate their own replication and movement, viroids depend exclusively on host factors for these purposes. Viroids replicate through an RNA-based rolling circle mechanism with three steps: i) synthesis of longer-than-unit strands catalyzed by a host nuclear or chloroplastic RNA polymerase that reiteratively transcribes the initial circular template, ii) processing to unit-length, which remarkably is mediated by hammerhead ribozymes in the family Avsunviroidae, and iii) and circularization resulting from the action of an RNA ligase or from self-ligation. Among the many pending issues, how viroids redirect the template specificity of certain host DNA-dependent RNA polymerases to transcribe RNA, is one of the most challenging. In addition, viroids must recruit host factors for their intracelular, cell-to-cell and long-distance movement within the plant. There are also pending questions in this context, the most appealing of which is how members of the family Avsunviridae gain access into the chloroplast; because essentially no other RNA has been reported to traffic inside this organelle, the answer to this question may reveal novel transport pathways in plant cells.

Recently, viroid-specific RNAs with the characteristic properties of the small interfering RNAs, the most reliable markers for post-transcriptional gene silencing (PTGS), have been detected in plants infected by members of both families. This indicates that viroids are inducers and targets (and perhaps even suppressors) of PTGS, and that processes of this kind may mediate many aspects of viroid biology including pathogenesis.

Finally, certain viroid properties, prominent among which are their size, circularity and specially the presence of hammerhead ribozymes in members of the family Avsunviroidae, support the idea that viroids may have a very ancient evolutionary origin independent of viruses. Viroid origin would go back to the RNA world postulated to have preceded the present world on Earth based on DNA and proteins.

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