Flores Ricardo, Navarro Beatriz, Serra Pedro, Di Serio Francesco
Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Científicas-Universidad Politécnica de Valencia, Ingeniero Fausto Elio s/n, Valencia 46022, Spain.
Istituto per la Protezione Sostenibile delle Piante, Consiglio Nazionale delle Ricerche, Via Amendola 122/D, Bari 70126, Italy.
Virus Evol. 2022 Jan 15;8(1):veab107. doi: 10.1093/ve/veab107. eCollection 2022.
Viroids are tiny, circular, and noncoding RNAs that are able to replicate and systemically infect plants. The smallest known pathogens, viroids have been proposed to represent survivors from the RNA world that likely preceded the cellular world currently dominating life on the earth. Although the small, circular, and compact nature of viroid genomes, some of which are also endowed with catalytic activity mediated by hammerhead ribozymes, support this proposal, the lack of feasible evolutionary routes and the identification of hammerhead ribozymes in a large number of DNA genomes of organisms along the tree of life have led some to question such a proposal. Here, we reassess the origin and subsequent evolution of viroids by complementing phylogenetic reconstructions with molecular data, including the primary and higher-order structure of the genomic RNAs, their replication, and recombination mechanisms and selected biological information. Features of some viroid-like RNAs found in plants, animals, and possibly fungi are also considered. The resulting evolutionary scenario supports the emergence of protoviroids in the RNA world, mainly as replicative modules, followed by a further increase in genome complexity based on module/domain shuffling and combination and mutation. Such a modular evolutionary scenario would have facilitated the inclusion in the protoviroid genomes of complex RNA structures (or coding sequences, as in the case of hepatitis delta virus and delta-like agents), likely needed for their adaptation from the RNA world to a life based on cells, thus generating the ancestors of current infectious viroids and viroid-like RNAs. Other noninfectious viroid-like RNAs, such as retroviroid-like RNA elements and retrozymes, could also be derived from protoviroids if their reverse transcription and integration into viral or eukaryotic DNA, respectively, are considered as a possible key step in their evolution. Comparison of evidence supporting a general and modular evolutionary model for viroids and viroid-like RNAs with that favoring alternative scenarios provides reasonable reasons to keep alive the hypothesis that these small RNA pathogens may be relics of a precellular world.
类病毒是微小的、环状的非编码RNA，能够进行复制并系统性地感染植物。作为已知最小的病原体，类病毒被认为是RNA世界的幸存者，而RNA世界可能先于当前主宰地球生命的细胞世界出现。尽管类病毒基因组具有小、环状和紧凑的特点，其中一些还具有锤头状核酶介导的催化活性，这支持了上述观点，但缺乏可行的进化途径以及在生命之树上众多生物的DNA基因组中发现锤头状核酶，使得一些人对这一观点提出质疑。在这里，我们通过用分子数据补充系统发育重建来重新评估类病毒的起源及后续进化，这些分子数据包括基因组RNA的一级和高级结构、它们的复制和重组机制以及选定的生物学信息。我们还考虑了在植物、动物以及可能在真菌中发现的一些类病毒样RNA的特征。由此产生的进化情景支持原类病毒在RNA世界中的出现，主要作为复制模块，随后基于模块/结构域的重排、组合和突变，基因组复杂性进一步增加。这样一种模块化的进化情景将有助于将复杂的RNA结构（或编码序列，如丁型肝炎病毒和丁型肝炎样病原体的情况）纳入原类病毒基因组，这些结构可能是它们从RNA世界适应基于细胞的生命所必需的，从而产生了当前感染性类病毒和类病毒样RNA的祖先。如果将它们的逆转录以及分别整合到病毒或真核DNA中视为其进化的一个可能关键步骤，那么其他非感染性类病毒样RNA，如逆转录类病毒样RNA元件和逆转录酶，也可能源自原类病毒。将支持类病毒和类病毒样RNA的一般模块化进化模型的证据与支持其他情景的证据进行比较，为维持这些小RNA病原体可能是前细胞世界遗迹的假说提供了合理依据。
