Phylogeny of viroids, viroidlike satellite RNAs, and the viroidlike domain of hepatitis delta virus RNA.

Abstract

We report a phylogenetic study of viroids, some plant satellite RNAs, and the viroidlike domain of human hepatitis 8 virus RNA. Our results support a monophyletic origin of these RNAs and are consistent with the hypothesis that they may be "living fossils" of a precellular RNA world. Moreover, the viroidlike domain of human hepatitis 8 virus RNA appears closely related to the viroidlike satellite RNAs of plants, with which it shares some structural and functional properties. On the basis of our phylogenetic analysis, we propose a taxonomic classification of these RNAs.assumed an intracellular mode of existence sometime after the evolution of cellular organisms.Implicit in this proposal is the possibility that all viroids and viroidlike RNAs may have been derived from a common ancestor. To obtain evidence for or against this proposition, we have conducted a phylogenetic analysis of these small pathogenic RNAs and report here that our results are consistent with a monophyletic origin of viroids and viroidlike satellite RNAs, as well as possibly of the viroidlike domain of HDV RNA.Viroids, subviral pathogens of higher plants, are small (246-375 nucleotide residues), unencapsidated, single-stranded, circular RNAs characterized by highly base-paired, rodlike secondary structures (1). Viroids do not code for any proteins, yet they replicate autonomously (without the assistance of helper viruses) in susceptible cells. Viroidlike satellite RNAs resemble viroids, but they are found within the capsids of specific helper viruses required for their replication (2). Human hepatitis 8 virus (HDV) RNA is a circular RNA requiring hepatitis B virus as a helper virus for packaging and transmission (3). HDV RNA contains a region, termed the viroidlike domain, with significant similarities with viroid and viroidlike satellite RNAs (4). Viroids, viroidlike satellite RNAs, and HDV RNA appear to replicate via oligomeric RNA intermediates by some type of rolling-circle mechanism (2-6).Several hypotheses have been advanced to explain the evolution of viroids. It has been suggested, for example, that viroids may have originated from retroviruses or transposable elements by deletion of interior sequences (7), that they may represent escaped introns (8, 9), or that they have evolved comparatively recently from hypothetical "antenna" or "signal" RNAs, which eukaryotic cells are assumed to interchange (10).With the demonstration that certain RNAs have catalytic properties (11,12), the idea that RNA preceded DNA as a carrier of genetic information has gained support. Most recent models for self-replicating precellular RNAs assume the existence of primitive RNA enzymes with properties that are derived from extant self-splicing introns (13,14). Because one viroid, all known viroidlike satellite RNAs, and the viroidlike domain of HDV RNA are self-cleaving (3, 15, 16), it is equally plausible to consider these RNAs as relics of the RNA world, thus leading to an alternative hypothesis for the evolution of viroids and viroidlike satellite R...

Nucleotide sequence and structural features of the Group III citrus viroids

“…Among the different viroid families or subgroups represented in the citrus viroids (Elena et al, 1991), the percentage similarity values indicate the closest relationship between the CVd-III viroids and CVd-Ib, a reported member of the ASSVd group (Ashulin et al, 1991). The percentage similarity between ASSVd and CVd-IlIa (56"8 %) or CVd-IIIb (57-4 %) supports this relationship.…”

Current status of viroid taxonomy

“…As shown in Figure 4, a monophyletic origin of viroids can be assumed at the genus and family levels, as proposed before [12]. Moreover, the apparently monophyletic origin of viroids and several groups of ribozyme-containing satellite RNAs [13] is an important part of the argument for their possible origin in the ''RNA world'' [9], but the choice of appropriate phylogenetic approaches for these analyses are a matter of some controversy (e.g., [12,39]). …”

“…3) in both polarity strands, which allow selfcleavage of the oligomeric RNAs intermediates generated through a rolling-circle replication mechanism. Due to their obvious biological implications, CCR and hammerhead ribozymes have long been considered of taxonomic relevance [13,21]. In fact, nowadays, two characteristicsthe presence/absence of either a CCR or hammerhead ribozymes -divide viroids into two families.…”

“…In the case of viroids, although the 32 recognized species and eight genera were established using either the arbitrarilyselected value of \90% sequence identity [21] or the previous ICTV definition of virus (and viroid) species, they essentially meet the new requirement for monophyletic origin ( Fig. 4; see also [12,13,51]). Therefore, the new criteria adopted for defining virus species can be certainly applied to viroids, thus preserving Section 3.32 of the International Code of Virus Classification and Nomenclature.…”

“…Table 1 shows the most recent taxonomy of viroids published in the 9th ICTV Report [51]. This scheme is a direct descendant of the first formal proposal for viroid classification advanced by Elena et al [13]. Following official adoption, this taxonomic scheme first appeared in the 6th ICTV Report [15], in which several viroid species were listed.…”