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Abstract
BackgroundCatalytic RNAs, or ribozymes, are regarded as fossils of a prebiotic RNA world that have remained in the genomes of modern organisms. The simplest ribozymes are the small self-cleaving RNAs, like the hammerhead ribozyme, which have been historically considered biological oddities restricted to some RNA pathogens. Recent data, however, indicate that small self-cleaving ribozymes are widespread in genomes, although their functions are still unknown.ResultsWe reveal that hammerhead ribozyme sequences in plant genomes form part of a new family of small non-autonomous retrotransposons with hammerhead ribozymes, referred to as retrozymes. These elements contain two long terminal repeats of approximately 350 bp, each harbouring a hammerhead ribozyme that delimitates a variable region of 600–1000 bp with no coding capacity. Retrozymes are actively transcribed, which gives rise to heterogeneous linear and circular RNAs that accumulate differentially depending on the tissue or developmental stage of the plant. Genomic and transcriptomic retrozyme sequences are highly heterogeneous and share almost no sequence homology among species except the hammerhead ribozyme motif and two small conserved domains typical of Ty3-gypsy long terminal repeat retrotransposons. Moreover, we detected the presence of RNAs of both retrozyme polarities, which suggests events of independent RNA-RNA rolling-circle replication and evolution, similarly to that of infectious circular RNAs like viroids and viral satellite RNAs.ConclusionsOur work reveals that circular RNAs with hammerhead ribozymes are frequently occurring molecules in plant and, most likely, metazoan transcriptomes, which explains the ubiquity of these genomic ribozymes and suggests a feasible source for the emergence of circular RNA plant pathogens.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1002-4) contains supplementary material, which is available to authorized users.
Highlights
Catalytic RNAs, or ribozymes, are regarded as fossils of a prebiotic RNA world that have remained in the genomes of modern organisms
Often contain many small nonautonomous long terminal repeat (LTR)-retrotransposons, like the terminalrepeat retrotransposons in miniature (TRIMs) [32] or the small LTR-retrotransposons (SMARTs) [33], which do not encode any protein and whose mobility depends on autonomous LTR-retrotransposons
In this work, following in silico, in vitro and in vivo approaches, we reveal that genomic hammerhead ribozyme (HHR) in plants are part of an atypical family of non-autonomous LTR-retrotransposons that accumulate in the cell transcriptomes as abundant RNA circles
Summary
Catalytic RNAs, or ribozymes, are regarded as fossils of a prebiotic RNA world that have remained in the genomes of modern organisms. Retrotransposons are the major components of most eukaryotic genomes, especially in the plant kingdom, where long terminal repeat (LTR)retrotransposons can make up more than 70 % of the genome [31] These retroelements encode the protein factors required for their own mobilization. Often contain many small nonautonomous LTR-retrotransposons, like the terminalrepeat retrotransposons in miniature (TRIMs) [32] or the small LTR-retrotransposons (SMARTs) [33], which do not encode any protein and whose mobility depends on autonomous LTR-retrotransposons. All these retrotransposons and other mobile elements remain heavily silenced at the transcriptional level, and they are only expressed under certain conditions. In this work, following in silico, in vitro and in vivo approaches, we reveal that genomic HHRs in plants are part of an atypical family of non-autonomous LTR-retrotransposons that accumulate in the cell transcriptomes as abundant RNA circles
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