Promoter Motifs in NCLDVs: An Evolutionary Perspective

Oliveira, Graziele Pereira; Andrade, Aron José Pazin de; Rodrigues, Rodrigo Araújo Lima; Arantes, Thalita Souza; Boratto, Paulo Victor de Miranda; Silva, Ludmila Karen dos Santos; Dornas, Fábio P.; Trindade, Giliane de Souza; Drumond, Betânia Paiva; Scola, Bernard La; Kroon, Erna Geessien; Abrahão, Jônatas Santos

doi:10.3390/v9010016

Cited by 20 publications

(27 citation statements)

References 134 publications

(195 reference statements)

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“…In view of the high coverage of RNA sequence reads mapped to the viral genome in this work, it is possible that the intergenic regions are shorter than anticipated, as observed in phycodnaviruses, another member group of the NCLDVs (Blanc et al, 2014). The temporal expression profile observed for Marseillevirus T19, with genes divided into early, intermediate and late categories, was similar to that observed for other giant DNA viruses (Oliveira et al, 2017a). This profile was validated by RT-qPCR data, a more sensitive technique compared to highthroughput sequencing.…”

Section: Discussionsupporting

confidence: 65%

Analysis of a Marseillevirus Transcriptome Reveals Temporal Gene Expression Profile and Host Transcriptional Shift

et al. 2020

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Marseilleviruses comprise a family of large double-stranded DNA viruses belonging to the proposed order "Megavirales." These viruses have a circular genome of ∼370 kbp, coding hundreds of genes. Over a half of their genes are associated with AT-rich putative promoter motifs, which have been demonstrated to be important for gene regulation. However, the transcriptional profile of Marseilleviruses is currently unknown. Here we used RNA sequencing technology to get a general transcriptional profile of Marseilleviruses. Eight million 75-bp-long nucleotide sequences were robustly mapped to all 457 genes initially predicted for Marseillevirus isolate T19, the prototype strain of the family, and we were able to assemble 359 viral contigs using a genomeguided approach with stringent parameters. These reads were differentially mapped to the genes according to the replicative cycle time point from which they were obtained. Cluster analysis indicated the existence of three main temporal categories of gene expression, early, intermediate and late, which were validated by quantitative reverse transcription polymerase chain reaction assays targeting several genes. Genes belonging to different functional groups exhibited distinct expression levels throughout the infection cycle. We observed that the previously predicted promoter motif, AAATATTT, as well as new predicted motifs, were not specifically related to any of the temporal or functional classes of genes, suggesting that other components are involved in temporally regulating virus transcription. Moreover, the host transcription machinery is heavily altered, and many genes are down regulated, including those related to translation process. This study provides an overview of the transcriptional landscape of Marseilleviruses.

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Section: Discussionsupporting

confidence: 65%

Analysis of a Marseillevirus Transcriptome Reveals Temporal Gene Expression Profile and Host Transcriptional Shift

et al. 2020

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“…5). We were able to detect the previously identified late consensus sequences TATA box-like motif (TAATTAAA) and ATTTGATCTT in two late genes, namely, ORF22 (RNase III) and ORF41 (MCP), respectively (18,19). The TATA box like motif is located 16 bp before the ATG start codon, and the ATTTGATCTT consensus sequence is 28 bp before the ORF start codon.…”

Section: In Vivo Expression Of Sfav Genesmentioning

confidence: 86%

Transcriptome Analysis of the Spodoptera frugiperda AscovirusIn VivoProvides Insights into How Its Apoptosis Inhibitors and Caspase Promote Increased Synthesis of Viral Vesicles and Virion Progeny

Zaghloul

Hice

Arensburger

et al. 2017

J Virol

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Ascoviruses are ds DNA viruses that attack caterpillars and differ from all other viruses by inducing nuclear lysis followed by cleavage of host cells into numerous anucleate vesicles in which virus replication continues as these grow in the blood. Ascoviruses are also unusual in that most encode apoptosis inhibitors and caspase or caspase-like proteins. A robust cell line to study the novel molecular biology of ascovirus replication is lacking. Therefore, we used strand-specific RNA-Seq to study transcription in third instars of infected with the Spodoptera frugiperda ascovirus, a member of the type species, (SfAV-1a), sampling transcripts at different time points after infection. We targeted transcription of two types of SfAV-1a genes; first, 44 core genes that occur in several ascovirus species, and second, 26 genes predicted to have metabolic functions likely involved in synthesizing viral vesicle membranes. Gene cluster analysis showed differences in temporal expression of SfAV-1a genes, enabling their assignment to three temporal classes; early, late and very late. Inhibitors of apoptosis (IAP-like proteins; ORF016, ORF025 and ORF074) were expressed early, whereas its caspase (ORF073) was expressed very late, which correlated with apoptotic events leading to viral vesicle formation. Expression analysis revealed that a Diedel gene homolog (ORF121), the only known "virokine," was highly expressed, implying this ascovirus protein helps evade innate host immunity. Lastly, single-nucleotide resolution of RNA-Seq data revealed 15 bicistronic and tricistronic messages along the genome, an unusual occurrence for large ds DNA viruses. Unlike all other DNA viruses, ascoviruses code for an executioner caspase, apparently involved in a novel cytopathology in which viral replication induces nuclear lysis followed by cell cleavage yielding numerous large anucleate viral vesicles that continue to produce virions. Our transcriptome analysis of genome expression by the Spodoptera frugiperda ascovirus shows that inhibitors of apoptosis are expressed first enabling viral replication to proceed, after which the SfAV-1a caspase is synthesized, leading to viral vesicle synthesis and subsequent extensive production of progeny virions. Moreover, we detected numerous bicistronic and tricistronic mRNA messages in the ascovirus transcriptome, implying ascoviruses use other non-canonical translational mechanisms such as Internal Ribosome Entry Site (IRES). These results provide the first insights into the molecular biology of a unique coordinated gene expression pattern in which cell architecture is markedly modified, more than in any other known eukaryotic virus, to promote viral reproduction and transmission.

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“…Some studies have described putative A/T-rich promoter sequences for nucleocytoplasmic large DNA viruses (NCLDV) from different families (15)(16)(17)(18)(19)(20)(21). In 2005, the mimivirus promoter sequence was identified.…”

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confidence: 99%

The Investigation of Promoter Sequences of Marseilleviruses Highlights a Remarkable Abundance of the AAATATTT Motif in Intergenic Regions

Oliveira

Lima

Arantes

et al. 2017

J Virol

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Viruses display a wide range of genomic profiles and, consequently, a variety of gene expression strategies. Specific sequences associated with transcriptional processes have been described in viruses, and putative promoter motifs have been elucidated for some nucleocytoplasmic large DNA viruses (NCLDV). Among NCLDV, the is a well-recognized family because of its genomic mosaicism. The marseilleviruses have an ability to incorporate foreign genes, especially from sympatric organisms inhabiting, its main known host. Here, we identified for the first time an eight-nucleotide A/T-rich promoter sequence (AAATATTT) associated with 55% of marseillevirus genes that is conserved in all marseilleviruses lineages, a higher level of conservation than that of any giant virus described to date. We instigated our prediction about the promoter motif by biological assays and by evaluating how single mutations in this octamer can impact gene expression. The investigation of sequences that regulate the expression of genes relative to lateral transfer revealed that the promoter motifs do not appear to be incorporated by marseilleviruses from donor organisms. Indeed, analyses of the intergenic regions that regulate lateral gene transfer-related genes have revealed an independent origin of the marseillevirus intergenic regions that does not match gene-donor organisms. About 50% of AAATATTT motifs spread throughout intergenic regions of the marseilleviruses are present as multiple copies. We believe that such multiple motifs are associated with increased expression of a given gene or are related to incorporation of foreign genes into the mosaic genome of marseilleviruses. The marseilleviruses draw attention because of the peculiar features of their genomes; however, little is known about their gene expression patterns or the factors that regulate those expression patterns. The limited published research on the expression patterns of the marseilleviruses and their unique genomes has led us to study the promoter motif sequences in the intergenic regions of the marseilleviruses. This work is the first to analyze promoter sequences in the genomes of the marseilleviruses. We also suggest a strong capacity to acquire foreign genes and to express those genes mediated by multiple copies of the promoter motifs available in intergenic regions. These findings contribute to an understanding of genomic expansion and plasticity observed in these giant viruses.

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Promoter Motifs in NCLDVs: An Evolutionary Perspective

Cited by 20 publications

References 134 publications

Analysis of a Marseillevirus Transcriptome Reveals Temporal Gene Expression Profile and Host Transcriptional Shift

Analysis of a Marseillevirus Transcriptome Reveals Temporal Gene Expression Profile and Host Transcriptional Shift

Transcriptome Analysis of the Spodoptera frugiperda AscovirusIn VivoProvides Insights into How Its Apoptosis Inhibitors and Caspase Promote Increased Synthesis of Viral Vesicles and Virion Progeny

The Investigation of Promoter Sequences of Marseilleviruses Highlights a Remarkable Abundance of the AAATATTT Motif in Intergenic Regions

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