An endogenous bornavirus‐like nucleoprotein in miniopterid bats retains the RNA‐binding properties of the original viral protein

Mukai, Yosuke; Horie, Masayuki; Kojima, Shohei; Kawasaki, Jun; Maeda, Ken; Tomonaga, Keizō

doi:10.1002/1873-3468.14290

Cited by 4 publications

(5 citation statements)

References 53 publications

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“…We previously found miEBLN-1, which is derived from an ancient orthobornaviral N gene and retains the intact ORF, in miniopterid bats (Fig. 2a) and the miEBLN-1 "empty" loci in the genomes of Rhinolophus ferrumequinum and Phyllostomus hastatus [10]. To confirm these results, we reanalyzed the miEBLN-1 empty loci using the current genome datasets.…”

Section: Identification Of N/x/p Transcript-like Ebls In Miniopterid ...mentioning

confidence: 68%

“…We previously identified miEBLN-1, an EBLN derived from an ancient orthobornavirus that retains an intact N ORF in miniopterid bats [10]. The miEBLN-1 locus is present in the genomes of miniopterid bats, specifically in those of Miniopterus natalensis, M. schreibersii , and M. fuliginosus , but is empty (i.e., syntenic loci lacking miEBLN-1) in the genomes of Rhinolophus ferrumequinum and Phyllostomus hastatus .…”

Section: Resultsmentioning

confidence: 99%

“…Genomic DNA was obtained from YubFKT1 (kidney epithelial cell line) [22] in a previous study [10]. miEBLN/X/P-1, miEBLN/X/P-2, miEBLN/X/P-3, and miEBLX/P-4 and corresponding flanking locus in M. fuliginosus were PCR-amplified from the DNA extracted from YubFKT1 using Phusion Hot Start II High-Fidelity PCR Master Mix (Thermo Fisher Scientific).…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

The hidden diversity of ancient bornaviral sequences from X and P genes in vertebrate genomes

Garcia¹,

Mukai

Tomonaga

et al. 2022

Preprint

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Endogenous bornavirus-like elements (EBLs) are heritable sequences derived from bornaviruses in vertebrate genomes, which are strongly suggested to originate from transcripts of ancient bornaviruses. EBLs have been detected by sequence similarity searches, such as tBLASTn, and thus EBLs derived from small and/or rapidly evolving viral genes, such as viral X and P genes, are difficult to be detected. Indeed, no EBLs derived from X and P genes of orthobornaviruses were detected. Thus, although previous studies comprehensively analyzed the presence of EBLs in vertebrate genomes, there may still be undetectable EBLs. In this study, we developed a novel strategy to detect such "hidden" EBLs by focusing on the nature of readthrough transcription of orthobornavirus. We showed a series of evidence supporting that there are EBLs derived from orthobornaviral X and P genes in mammalian genomes. Therefore, this study contributes to a deeper understanding of the evolution of ancient viruses and of virus-host relationships. Further, our data also suggest that endogenous viral elements detected thus far are just the tip of the iceberg, and thus further studies are required to understand ancient viruses more accurately.

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Section: Identification Of N/x/p Transcript-like Ebls In Miniopterid ...mentioning

confidence: 68%

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

The hidden diversity of ancient bornaviral sequences from X and P genes in vertebrate genomes

Garcia¹,

Mukai

Tomonaga

et al. 2022

Preprint

Self Cite

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show abstract

“…However, in vivo experimental evidence for antiviral roles mediated by nrEVE-derived piRNAs against cognate viral replication was only revealed in Aedes aegypti ovaries 21 . In addition to the antiviral roles, functional studies of nrEVEs have mainly focused on coopted EBLNs in mammals [28][29][30][31] , whereas in vivo studies of the cellular functions of domesticated nrEVEs in arthropods are scarce. In this study, although the production of piRNAs was found for the majority of transcribed ToEVEs (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…hsEBLN-2 was shown to be translated and encoded by a mitochondrial protein that is associated with cell viability, demonstrating the potential of co-opted mammalian function originating from ancient bornavirus infection 30 . Moreover, the EBLNs of miniopterid bats have been shown to encode an RNA-binding protein with biochemical properties similar to those of bornaviral nucleoprotein (N), suggesting that EBLNs can maintain the properties of their original genes 31 . In addition to EBLNs, a number of studies have shown that nrEVEs are also transcriptionally active, and several nrEVEs have maintained intact ORFs under strong purifying selection in invertebrates, mostly mosquitoes 7,32 .…”

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confidence: 99%

Co-option of a non-retroviral endogenous viral element in planthoppers

Huang,

Li,

et al. 2023

Nat Commun

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Non-retroviral endogenous viral elements (nrEVEs) are widely dispersed throughout the genomes of eukaryotes. Although nrEVEs are known to be involved in host antiviral immunity, it remains an open question whether they can be domesticated as functional proteins to serve cellular innovations in arthropods. In this study, we found that endogenous toti-like viral elements (ToEVEs) are ubiquitously integrated into the genomes of three planthopper species, with highly variable distributions and polymorphism levels in planthopper populations. Three ToEVEs display exon‒intron structures and active transcription, suggesting that they might have been domesticated by planthoppers. CRISPR/Cas9 experiments revealed that one ToEVE in Nilaparvata lugens, NlToEVE14, has been co-opted by its host and plays essential roles in planthopper development and fecundity. Large-scale analysis of ToEVEs in arthropod genomes indicated that the number of arthropod nrEVEs is currently underestimated and that they may contribute to the functional diversity of arthropod genes.

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The hidden diversity of ancient bornaviral sequences from X and P genes in vertebrate genomes

Garcia¹,

Mukai

Tomonaga

et al. 2023

Virus Evolution

View full text Add to dashboard Cite

Endogenous bornavirus-like elements (EBLs) are heritable sequences derived from bornaviruses in vertebrate genomes that originate from transcripts of ancient bornaviruses. EBLs have been detected using sequence similarity searches such as tBLASTn, whose technical limitations may hinder the detection of EBLs derived from small and/or rapidly evolving viral X and P genes. Indeed, no EBLs derived from the X and P genes of orthobornaviruses have been detected to date in vertebrate genomes. Here, we aimed to develop a novel strategy to detect such “hidden” EBLs. To this aim, we focused on the 1.9 kb read-through transcript of orthobornaviruses, which encodes a well-conserved N gene and small and rapidly evolving X and P genes. We show a series of evidence supporting the existence of EBLs derived from orthobornaviral X and P genes (EBLX/Ps) in mammalian genomes. Furthermore, we found that an EBLX/P is expressed as a fusion transcript with the cellular gene, ZNF451, which potentially encodes the ZNF451/EBLP fusion protein in miniopterid bat cells. This study contributes to a deeper understanding of ancient bornaviruses and co-evolution between bornaviruses and their hosts. Furthermore, our data suggest that endogenous viral elements are more abundant than previously appreciated using BLAST searches alone, and further studies are required to understand ancient viruses more accurately.

show abstract

An endogenous bornavirus‐like nucleoprotein in miniopterid bats retains the RNA‐binding properties of the original viral protein

Cited by 4 publications

References 53 publications

The hidden diversity of ancient bornaviral sequences from X and P genes in vertebrate genomes

The hidden diversity of ancient bornaviral sequences from X and P genes in vertebrate genomes

Co-option of a non-retroviral endogenous viral element in planthoppers

The hidden diversity of ancient bornaviral sequences from X and P genes in vertebrate genomes

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