Circular RNAs: relics of precellular evolution?

Abstract

The demonstration of enzymatic capabilities of certain RNAs, in addition to their well-known template properties, has led to the recognition that RNAs are the only biological macromolecules that can function both as genotype and phenotype, hence raising the possibility of Darwinian selection and precellular evolution at the RNA level in the absence of DNA or protein. Recent models of such precellular RNA systems are patterned after the properties of intron-derived ribozymes. On the basis of a phylogenetic analysis and known properties of certain small plant pathogenic RNAs (viroids and viroid-like satellite RNAs), I suggest that these plant RNAs are more plausible candidates than introns as "living fossils" of a precellular RNA world. Their small size and circularity would have enhanced probability of their survival in error-prone, primitive self-replicating RNA systems and assured complete replication without the need for initiation or termination signals. All of these RNAs possess efficient mechanisms for the precise cleavage of monomers from oligomeric replication intermediates. Some (most viroids) require a host factor, but others (viroid-like satellite RNAs and one viroid) function as self-cleaving RNA enzymes far smaller and simpler than those derived from introns. The question is raised whether introns could have evolved from viroids or viroid-like satellite RNAs rather than vice versa, as has been widely speculated.