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Origin and evolution of papillomavirus (onco)genes and genomes.

ABSTRACT: Papillomaviruses (PVs) are ancient viruses infecting vertebrates, from fishes to mammals. Although the genomes of PVs are small and show conserved synteny, PVs display large genotypic diversity and ample variation in the phenotypic presentation of the infection. Most PV genomes contain two small early genes E6 and E7. In a bunch of closely related human papillomaviruses (HPVs), the E6 and E7 proteins provide the viruses with oncogenic potential. The recent discoveries of PVs without E6 and E7 in different fish species place a new root on the PV tree, and suggest that ancestral PVs consisted of the minimal PV backbone E1-E2-L2-L1. Bayesian phylogenetic analyses date the most recent common ancestor of the PV backbone to 424 million years ago (Ma). Common ancestry tests on extant E6 and E7 genes indicate that they share a common ancestor dating back to at least 184 Ma. In AlphaPVs infecting Old World monkeys and apes, the appearance of the E5 oncogene 53-58 Ma concurred with (i) a significant increase in substitution rate, (ii) a basal radiation and (iii) key gain of functions in E6 and E7. This series of events was instrumental to construct the extant phenotype of oncogenic HPVs. Our results assemble the current knowledge on PV diversity and present an ancient evolutionary timeline punctuated by evolutionary innovations in the history of this successful viral family. This article is part of the theme issue 'Silent cancer agents: multi-disciplinary modelling of human DNA oncoviruses'.

SUBMITTER: Willemsen A

PROVIDER: S-EPMC6501903 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Origin and evolution of papillomavirus (onco)genes and genomes.

Willemsen Anouk A Bravo Ignacio G IG

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20190501 1773

Papillomaviruses (PVs) are ancient viruses infecting vertebrates, from fishes to mammals. Although the genomes of PVs are small and show conserved synteny, PVs display large genotypic diversity and ample variation in the phenotypic presentation of the infection. Most PV genomes contain two small early genes E6 and E7. In a bunch of closely related human papillomaviruses (HPVs), the E6 and E7 proteins provide the viruses with oncogenic potential. The recent discoveries of PVs without E6 and E7 in ...[more]

PMID: 30955499

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Project description:BackgroundSpecies of Bryopsidales form ecologically important components of seaweed communities worldwide. These siphonous macroalgae are composed of a single giant tubular cell containing millions of nuclei and chloroplasts, and harbor diverse bacterial communities. Little is known about the diversity of chloroplast genomes (cpDNAs) in this group, and about the possible consequences of intracellular bacteria on genome composition of the host. We present the complete cpDNAs of Bryopsis plumosa and Tydemania expeditiones, as well as a re-annotated cpDNA of B. hypnoides, which was shown to contain a higher number of genes than originally published. Chloroplast genomic data were also used to evaluate phylogenetic hypotheses in the Chlorophyta, such as monophyly of the Ulvophyceae (the class in which the order Bryopsidales is currently classified).ResultsBoth DNAs are circular and lack a large inverted repeat. The cpDNA of B. plumosa is 106,859 bp long and contains 115 unique genes. A 13 kb region was identified with several freestanding open reading frames (ORFs) of putative bacterial origin, including a large ORF (>8 kb) closely related to bacterial rhs-family genes. The cpDNA of T. expeditiones is 105,200 bp long and contains 125 unique genes. As in B. plumosa, several regions were identified with ORFs of possible bacterial origin, including genes involved in mobile functions (transposases, integrases, phage/plasmid DNA primases), and ORFs showing close similarity with bacterial DNA methyltransferases. The cpDNA of B. hypnoides differs from that of B. plumosa mainly in the presence of long intergenic spacers, and a large tRNA region. Chloroplast phylogenomic analyses were largely inconclusive with respect to monophyly of the Ulvophyceae, and the relationship of the Bryopsidales within the Chlorophyta.ConclusionsThe cpDNAs of B. plumosa and T. expeditiones are amongst the smallest and most gene dense chloroplast genomes in the core Chlorophyta. The presence of bacterial genes, including genes typically found in mobile elements, suggest that these have been acquired through horizontal gene transfer, which may have been facilitated by the occurrence of obligate intracellular bacteria in these siphonous algae.

Dataset Information

Origin and evolution of papillomavirus (onco)genes and genomes.

Publications

Origin and evolution of papillomavirus (onco)genes and genomes.

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