Widespread Horizontal Gene Transfer from Double-Stranded RNA Viruses to Eukaryotic Nuclear Genomes

Liu, Huiquan; Fù, Yànpíng; Jiāng, Dàohóng; Li, Guoqing; Xiè, Jiǎtāo; Chéng, Jiāsēn; Peng, You-Liang; Ghabrial, Said A.; Yi, Xianhong

doi:10.1128/jvi.00955-10

Cited by 203 publications

(164 citation statements)

References 68 publications

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“…We used virus-specific primers and genomic DNA of the host fungus as a template for PCR to investigate whether endogenization of viral sequences into the host genome was possible (Liu et al, 2010;Chiba et al, 2011, see Supplementary Table S2).…”

Section: Dna Extraction and Microsatellite Markersmentioning

confidence: 99%

Viruses accumulate in aging infection centers of a fungal forest pathogen

Vainio¹,

Müller²,

Korhonen³

et al. 2014

The ISME Journal

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Fungal viruses (mycoviruses) with RNA genomes are believed to lack extracellular infective particles. These viruses are transmitted laterally among fungal strains through mycelial anastomoses or vertically via their infected spores, but little is known regarding their prevalence and patterns of dispersal under natural conditions. Here, we examined, in detail, the spatial and temporal changes in a mycovirus community and its host fungus Heterobasidion parviporum, the most devastating fungal pathogen of conifers in the Boreal forest region. During the 7-year sampling period, viruses accumulated in clonal host individuals as a result of indigenous viruses spreading within and between clones as well as novel strains arriving via airborne spores. Viral community changes produced pockets of heterogeneity within large H. parviporum clones. The appearance of novel viral infections in aging clones indicated that transient cell-to-cell contacts between Heterobasidion strains are likely to occur more frequently than what was inferred from genotypic analyses. Intraspecific variation was low among the three partitivirus species at the study site, whereas the unassigned viral species HetRV6 was highly polymorphic. The accumulation of point mutations during persistent infections resulted in viral diversification, that is, the presence of nearly identical viral sequence variants within single clones. Our results also suggest that co-infections by distantly related viral species are more stable than those between conspecific strains, and mutual exclusion may play a role in determining mycoviral communities.

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Section: Dna Extraction and Microsatellite Markersmentioning

confidence: 99%

Viruses accumulate in aging infection centers of a fungal forest pathogen

Vainio¹,

Müller²,

Korhonen³

et al. 2014

The ISME Journal

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“…Genetic material laterally transferred from nonretroviral viruses to host genomes has been noted for a wide variety of pathogens and hosts (Zhdanov 1975;Belyi et al 2010;Gilbert and Feschotte 2010;Kapoor et al 2010;Katzourakis and Gifford 2010;Liu et al 2010Liu et al , 2011. Several of these gene transfer events can be clearly attributed to retrotransposon activity (Ballinger et al 2012), and in at least one case the gene transfer is associated with viral resistance (Maori et al 2007).…”

Section: Discussionmentioning

confidence: 99%

piRNAs derived from ancient viral processed pseudogenes as transgenerational sequence-specific immune memory in mammals

Parrish

Fujino

Shiromoto

et al. 2015

RNA

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Endogenous bornavirus-like nucleoprotein elements (EBLNs) are sequences within vertebrate genomes derived from reverse transcription and integration of ancient bornaviral nucleoprotein mRNA via the host retrotransposon machinery. While species with EBLNs appear relatively resistant to bornaviral disease, the nature of this association is unclear. We hypothesized that EBLNs could give rise to antiviral interfering RNA in the form of PIWI-interacting RNAs (piRNAs), a class of small RNA known to silence transposons but not exogenous viruses. We found that in both rodents and primates, which acquired their EBLNs independently some 25-40 million years ago, EBLNs are present within piRNA-generating regions of the genome far more often than expected by chance alone (P = 8 × 10 −3 -6 × 10 −8 ). Three of the seven human EBLNs fall within annotated piRNA clusters and two marmoset EBLNs give rise to bona fide piRNAs. In both rats and mice, at least two of the five EBLNs give rise to abundant piRNAs in the male gonad. While no EBLNs are syntenic between rodent and primate, some of the piRNA clusters containing EBLNs are; thus we deduce that EBLNs were integrated into existing piRNA clusters. All true piRNAs derived from EBLNs are antisense relative to the proposed ancient bornaviral nucleoprotein mRNA. These observations are consistent with a role for EBLN-derived piRNA-like RNAs in interfering with ancient bornaviral infection. They raise the hypothesis that retrotransposon-dependent virus-to-host gene flow could engender RNA-mediated, sequence-specific antiviral immune memory in metazoans analogous to the CRISPR/Cas system in prokaryotes.

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“…To investigate the possibility of endogenization of mitoviral sequences into the host genome (Liu et al, 2010;Chiba et al, 2011), we used three different mitovirus primer pairs and total cellular DNA from the host fungus as a template for PCR. The presence of mitochondrial DNA was verified with PCR amplification using the primer pair ML1/ ML2, which is specific for mitochondrial large subunit rDNA (White et al, 1990).…”

Section: Methodsmentioning

confidence: 99%

Diagnosis and discovery of fungal viruses using deep sequencing of small RNAs

Vainio¹,

Jurvansuu²,

Streng

et al. 2015

Journal of General Virology

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Analysis of virus-derived small RNAs with high-throughput sequencing has been successful for detecting novel viruses in plants and invertebrates. However, the applicability of this method has not been demonstrated in fungi, although fungi were among the first organisms reported to utilize RNA silencing. Here, we used virus-infected isolates of the fungal species complex Heterobasidion annosum sensu lato as a model system to test whether mycovirus genome segments can be detected with small RNA deep sequencing. Species of the genus Heterobasidion are some of the most devastating forest pathogens in boreal forests. These fungi cause wood decay and are commonly infected with species of the family Partitiviridae and the unassigned virus species Heterobasidion RNA virus 6. Small RNA deep sequencing allowed the simultaneous detection of all eight double-stranded RNA virus strains known to be present in the tested samples and one putative mitovirus species (family Narnaviridae) with a single-stranded RNA genome, designated here as Heterobasidion mitovirus 1. Prior to this study, no members of the family Narnaviridae had been described as infecting species of Heterobasidion. Quantification of viral double-and single-stranded RNA with quantitative PCR indicated that co-infecting viral species and viruses with segmented genomes can be detected with small RNA deep sequencing despite vast differences in the amount of RNA. This is the first study demonstrating the usefulness of this method for detecting fungal viruses. Moreover, the results suggest that viral genomes are processed into small RNAs by different species of Heterobasidion.

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Widespread Horizontal Gene Transfer from Double-Stranded RNA Viruses to Eukaryotic Nuclear Genomes

Cited by 203 publications

References 68 publications

Viruses accumulate in aging infection centers of a fungal forest pathogen

Viruses accumulate in aging infection centers of a fungal forest pathogen

piRNAs derived from ancient viral processed pseudogenes as transgenerational sequence-specific immune memory in mammals

Diagnosis and discovery of fungal viruses using deep sequencing of small RNAs

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