High frequency of +1 programmed ribosomal frameshifting in Euplotes octocarinatus

Wang, Ruanlin; Xiong, Jie; Wang, Wei; Miao, Wei; Liang, Aihua

doi:10.1038/srep21139

Cited by 47 publications

(53 citation statements)

References 83 publications

(83 reference statements)

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“…Comparative genome analysis in the present study reveals that E. vannus shares similar patterns of frameshifting and stop codon usage with E. octocarinatus (Figure ). Our analyses are consistent with previous studies demonstrating that euplotids have a large number of genes requiring programmed ribosomal frameshifting (PRF), and this phenomenon is more prevalent in this clade of ciliates than in the viruses, prokaryotes and other eukaryotes where it has been studied (Karamysheva et al, ; Wang et al, ). Previous study reported a putative suppressor tRNA of UAA, which may play an important role in +1 frameshifting in E. octocarinatus (Wang et al, ).…”

Section: Discussionsupporting

confidence: 92%

“…Frameshifting events were detected using a custom Perl script modified from the protocol in a previous study (Wang et al, ). Transcripts of euplotids were compared using blastx to conserved protein sequences of other ciliates (E‐value cutoff = 1e‐5), and frame changes between adjacent blastx hits were identified.…”

Section: Methodsmentioning

confidence: 99%

“…However, conflicting models suggest a variety of mechanisms for genome rearrangement within the investigated ciliates (Chen et al, ; Feng et al, ; Maurer‐Alcalá, Knight, & Katz, ), Second, the nuclear genetic code in ciliates is diversified and flexible as standard stop codons are often reassigned to amino acids; even stranger, in some ciliates all three standard stop codons can either code for amino acid or terminate translation in a context‐dependent manner (Swart, Serra, Petroni, & Nowacki, ). More relevant for the current study, euplotid ciliates exhibit widespread programmed ribosomal frameshifting (PRF) at stop codons, 60‐fold higher than other organisms, for instance, human, mouse, flies, Caenorhabditis elegans , yeast and Escherichia coli (Wang, Xiong, Wang, Miao, & Liang, ). Stop codons are not sufficient for translation termination in euplotids and frameshifting is sequence context‐dependent (Lobanov et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors

Chen

Jiang

Gao

et al. 2019

Molecular Ecology Resources

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As a model organism for studies of cell and environmental biology, the free‐living and cosmopolitan ciliate Euplotes vannus shows intriguing features like dual genome architecture (i.e., separate germline and somatic nuclei in each cell/organism), “gene‐sized” chromosomes, stop codon reassignment, programmed ribosomal frameshifting (PRF) and strong resistance to environmental stressors. However, the molecular mechanisms that account for these remarkable traits remain largely unknown. Here we report a combined analysis of de novo assembled high‐quality macronuclear (MAC; i.e., somatic) and partial micronuclear (MIC; i.e., germline) genome sequences for E. vannus, and transcriptome profiling data under varying conditions. The results demonstrate that: (a) the MAC genome contains more than 25,000 complete “gene‐sized” nanochromosomes (~85 Mb haploid genome size) with the N50 ~2.7 kb; (b) although there is a high frequency of frameshifting at stop codons UAA and UAG, we did not observe impaired transcript abundance as a result of PRF in this species as has been reported for other euplotids; (c) the sequence motif 5′‐TA‐3′ is conserved at nearly all internally‐eliminated sequence (IES) boundaries in the MIC genome, and chromosome breakage sites (CBSs) are duplicated and retained in the MAC genome; (d) by profiling the weighted correlation network of genes in the MAC under different environmental stressors, including nutrient scarcity, extreme temperature, salinity and the presence of ammonia, we identified gene clusters that respond to these external physical or chemical stimulations, and (e) we observed a dramatic increase in HSP70 gene transcription under salinity and chemical stresses but surprisingly, not under temperature changes; we link this temperature‐resistance to the evolved loss of temperature stress‐sensitive elements in regulatory regions. Together with the genome resources generated in this study, which are available online at Euplotes vannus Genome Database (http://evan.ciliate.org), these data provide molecular evidence for understanding the unique biology of highly adaptable microorganisms.

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Section: Discussionsupporting

confidence: 92%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors

Chen

Jiang

Gao

et al. 2019

Molecular Ecology Resources

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“…Previous work suggested that a high frequency of +1 PRF existed in E. octocarinatus 19. A shotgun analysis was applied to investigate the proteome of E. octocarinatus to experimentally verify such high frequency +1 PRF in vivo .…”

Section: Resultsmentioning

confidence: 99%

Large-scale mass spectrometry-based analysis of Euplotes octocarinatus supports the high frequency of +1 programmed ribosomal frameshift

Wang

Zhang

et al. 2016

Sci Rep

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Programmed ribosomal frameshifting (PRF) is commonly used to express many viral and some cellular genes. We conducted a genome-wide investigation of +1 PRF in ciliate Euplotes octocarinatus through genome and transcriptome sequencing and our results demonstrated that approximately 11.4% of genes require +1 PRF to produce complete gene products. While nucleic acid-based evidence for candidate genes with +1 PRF is strong, only very limited information is available at protein levels to date. In this study, E. octocarinatus was subjected to large-scale mass spectrometry-based analysis to verify the high frequency of +1 PRF and 226 +1 PRF gene products were identified. Based on the amino acid sequences of the peptides spanning the frameshift sites, typical frameshift motif AAA-UAR for +1 PRF in Euplotes was identified. Our data in this study provide very useful insight into the understanding of the molecular mechanism of +1 PRF.

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“…; Wang et al. ,b). An even more convincing reason is the recent demonstration in Condylostoma , Parduczia, and Blastocrithidia , that all three UAA, UAG, and UGA stop codons may act as sense codons, depending on the relative position that they take in the transcript sequence (Alkalaeva and Mikhailova ; Heaphy et al.…”

Section: Discussionmentioning

confidence: 99%

The Sub‐Chromosomic Macronuclear Pheromone Genes of the Ciliate Euplotes raikovi: Comparative Structural Analysis and Insights into the Mechanism of Expression

Ricci

Candelori

Brandi

et al. 2018

J Eukaryotic Microbiology

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In Euplotes raikovi, we have determined the full-length sequences of a family of macronuclear genes that are the transcriptionally active versions of codominant alleles inherited at the mating-type (mat) locus of the micronuclear genome, and encode cell type-distinctive signaling pheromones. These genes include a 225-231-bp coding region flanked by a conserved 544-bp 5'-leader region and a more variable 3'-trailer region. Two transcription initiation start sites and two polyadenylation sites associated with nonconventional signals cooperate with a splicing phenomenon of a 326-bp intron residing in the 5'-leader region in the generation of multiple transcripts from the same gene. In two of them, the synthesis of functional products depends on the reassignment to a sense codon, or readthrough of a strictly conserved leaky UAG stop codon. That this reassignment may take place is suggested by the position this codon occupies in the transcripts, close to the transcript extremity and far from the poly(A) tail. In such a case, one product is a 69-amino acid protein in search of function and the second product is a 126-amino acid protein that represents a membrane-bound pheromone isoform candidate to function as a cell type-specific binding site (receptor) of the soluble pheromones.

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High frequency of +1 programmed ribosomal frameshifting in Euplotes octocarinatus

Cited by 47 publications

References 83 publications

Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors

Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors

Large-scale mass spectrometry-based analysis of Euplotes octocarinatus supports the high frequency of +1 programmed ribosomal frameshift

The Sub‐Chromosomic Macronuclear Pheromone Genes of the Ciliate Euplotes raikovi: Comparative Structural Analysis and Insights into the Mechanism of Expression

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