U3 snoRNA genes are multi-copy and frequently linked to U5 snRNA genes in Euglena gracilis§

Charette, J. Michael; Gray, Michael W.

doi:10.1186/1471-2164-10-528

Cited by 7 publications

(11 citation statements)

References 92 publications

(133 reference statements)

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“…It was previously observed that Euglena snoRNA species frequently consist of sequence-related isoforms (Charette and Gray 2009;Russell et al 2006) and therefore we are likely underestimating the frequency of tandem clustered arrangements. Those species whose closest gene copies (isoforms) contain the greatest sequence divergence in primer binding regions may not be efficiently amplified.…”

Section: Resultsmentioning

confidence: 85%

“…The overall organization of the Euglena U14 and modification-guide snoRNA genes is significantly different from that of the U3 snoRNA genes identified in this organism (Charette and Gray 2009). There is no indication of polycistronic U3 transcripts and those genes most closely linked to U3, including both tRNAs and U5 snRNA, are encoded in the opposite transcriptional orientation (Charette and Gray 2009).…”

Section: Discussionmentioning

confidence: 85%

“…Total E. gracilis genomic DNA was extracted using the method described in (Charette and Gray 2009), with the following modifications: (1) the cell pellet from the 1.4 L culture was re-suspended in 25 mL of room temperature extraction wash buffer and (2) after the high molecular weight DNA was spooled out of solution, it was dissolved in 10 mL of TE, 1 mL of 3 M sodium acetate was added, and a phenol-cresol extraction was repeated 4 times. The resulting purified DNA was treated with 480 U of RNase A (NEB) and incubated at 37°C for 3 h, followed by phenolic extraction and ethanol precipitation.…”

Section: Isolation Of Euglena Gracilis Genomic Dna and Total Rnamentioning

confidence: 99%

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Clustered organization, polycistronic transcription, and evolution of modification-guide snoRNA genes in Euglena gracilis

Moore

Russell

2011

Mol Genet Genomics

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Previous studies have shown that the eukaryotic microbe Euglena gracilis contains an unusually large assortment of small nucleolar RNAs (snoRNAs) and ribosomal RNA (rRNA) modification sites. However, little is known about the evolutionary mechanisms contributing to this situation. In this study, we have examined the organization and evolution of snoRNA genes in Euglena with the additional objective of determining how these properties relate to the rRNA modification pattern in this protist. We have identified and extensively characterized a clustered pattern of genes encoding previously biochemically isolated snoRNA sequences in E. gracilis. We show that polycistronic transcription is a prevalent snoRNA gene expression strategy in this organism. Further, we have identified 121 new snoRNA coding regions through sequence analysis of these clusters. We have identified an E. gracilis U14 snoRNA homolog clustered with modification-guide snoRNA genes. The U14 snoRNAs in other eukaryotic organisms examined to date typically contain both a modification and a processing domain. E. gracilis U14 lacks the modification domain but retains the processing domain. Our analysis of U14 structure and evolution in Euglena and other eukaryotes allows us to propose a model for its evolution and suggest its processing role may be its more important function, explaining its conservation in many eukaryotes. The preponderance of apparent small and larger-scale duplication events in the genomic regions we have characterized in Euglena provides a mechanism for the generation of the unusually diverse collection and abundance of snoRNAs and modified rRNA sites. Our findings provide the framework for more extensive whole genome analysis to elucidate whether these snoRNA gene clusters are spread across multiple chromosomes and/or form dense "arrays" at a limited number of chromosomal loci.

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Section: Resultsmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 85%

Section: Isolation Of Euglena Gracilis Genomic Dna and Total Rnamentioning

confidence: 99%

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Clustered organization, polycistronic transcription, and evolution of modification-guide snoRNA genes in Euglena gracilis

Moore

Russell

2011

Mol Genet Genomics

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“…Not all E. gracilis snoRNAs are expressed polycistronically as the U3 snoRNA, a snoRNA that functions in pre-rRNA processing steps (i.e. specifying rRNA cleavage sites instead of targeting modification sites) appears to be expressed monocistronically (Greenwood et al 1996;Charette and Gray 2009). Although the U3 snoRNA genes are multi-copy and frequently found associated with either U5 snRNA or tRNA genes, the U3 genes are in the opposite transcriptional orientation to the nearby U5 or tRNA genes (Charette and Gray 2009).…”

Section: Euglena Snornas and Their Expressionmentioning

confidence: 99%

“…specifying rRNA cleavage sites instead of targeting modification sites) appears to be expressed monocistronically (Greenwood et al 1996;Charette and Gray 2009). Although the U3 snoRNA genes are multi-copy and frequently found associated with either U5 snRNA or tRNA genes, the U3 genes are in the opposite transcriptional orientation to the nearby U5 or tRNA genes (Charette and Gray 2009). Unlike U3, two other predicted E. gracilis processing snoRNAs, U14 and the Eg-h1 H/ ACA-like RNA, are instead encoded by closely-spaced tandemly repeated genes like the modification-guide snoRNAs and are likely polycistronically expressed (Moore and Russell 2012).…”

Section: Euglena Snornas and Their Expressionmentioning

confidence: 99%

Euglena Transcript Processing

McWatters

Russell

2017

Advances in Experimental Medicine and Biology

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RNA transcript processing is an important stage in the gene expression pathway of all organisms and is subject to various mechanisms of control that influence the final levels of gene products. RNA processing involves events such as nuclease-mediated cleavage, removal of intervening sequences referred to as introns and modifications to RNA structure (nucleoside modification and editing). In Euglena, RNA transcript processing was initially examined in chloroplasts because of historical interest in the secondary endosymbiotic origin of this organelle in this organism. More recent efforts to examine mitochondrial genome structure and RNA maturation have been stimulated by the discovery of unusual processing pathways in other Euglenozoans such as kinetoplastids and diplonemids. Eukaryotes containing large genomes are now known to typically contain large collections of introns and regulatory RNAs involved in RNA processing events, and Euglena gracilis in particular has a relatively large genome for a protist. Studies examining the structure of nuclear genes and the mechanisms involved in nuclear RNA processing have revealed that indeed Euglena contains large numbers of introns in the limited set of genes so far examined and also possesses large numbers of specific classes of regulatory and processing RNAs, such as small nucleolar RNAs (snoRNAs). Most interestingly, these studies have also revealed that Euglena possesses novel processing pathways generating highly fragmented cytosolic ribosomal RNAs and subunits and non-conventional intron classes removed by unknown splicing mechanisms. This unexpected diversity in RNA processing pathways emphasizes the importance of identifying the components involved in these processing mechanisms and their evolutionary emergence in Euglena species.

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The small subunit processome in ribosome biogenesis—progress and prospects

2010

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The small subunit (SSU) processome is a 2.2 MDa ribonucleoprotein complex involved in the processing, assembly and maturation of the SSU of eukaryotic ribosomes. The identities of many of the factors involved in SSU biogenesis have been elucidated over the past 40 years. However, as our understanding increases, so do the number of questions about the nature of this complicated process. Cataloguing the components is the first step towards understanding the molecular workings of a system. This review will focus on how identifying components of ribosome biogenesis has led to the knowledge of how these factors, protein and RNA alike, associate with one another into sub-complexes, with a concentration on the small ribosomal subunit. We will also explore how this knowledge of sub-complex assembly has informed our understanding of the workings of the ribosome synthesis system as a whole. KeywordsSSU processome; U3 snoRNA; Utp; ribosomal SSU; RNA processing; RNA chaperoneThe process of making a single ribosome is a herculean task, and is one of the most metabolically expensive activities of a cell. In vigorously growing yeast cells, it requires the activity of all three RNA polymerases, accounting for 70% of total transcription, 90% of pre-mRNA splicing and more than 25% of translation.1 In Saccharomyces cerevisiae, nearly 7000 nucleotides of pre-rRNA must be accurately transcribed, cleaved, folded, chemically modified by 71 snoRNPs directing either 2′-O-methylation or pseudouridylation, and assembled with 78 ribosomal proteins (r-proteins) to form one mature ribosome. Despite the immensity of this task, about 2000 new ribosomes are produced each minute in yeast (~7500 subunits per minute in HeLa cells), leading to the presence of ~200 000 ribosomes in each cell (~10 million in each HeLa cell).1 , 2Because of its central importance, defects in ribosome biogenesis can have detrimental effects on cellular metabolism and vitality. Interestingly, a number of diseases have been found to be associated with defects in ribosome synthesis pathways. Several recent reviews contain details on the particular ribosomopathies known to date.3 , 4 In addition, ribosome biogenesis is a key component of the cell cycle where it regulates cell size and growth,5 -7 and is thus up-regulated in cancer.8 Despite this critical linkage, ribosome biogenesis is + To whom correspondence should be addressed. susan.baserga@yale.edu. * These two authors contributed equally NIH Public Access Author ManuscriptWiley Interdiscip Rev RNA. Author manuscript; available in PMC 2012 January 1. Published in final edited form as:Wiley Interdiscip Rev RNA. 2011 January ; 2(1): 1-21. doi:10.1002/wrna.57. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript understudied and its role in cancer is underappreciated. In addition, new evidence suggests that ribosome biogenesis proteins play critical roles in stem-cell differentiation in Drosophila.9 Furthermore, ribosome synthesis may also be a mechanism through which HIV modulates host respo...

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U3 snoRNA genes are multi-copy and frequently linked to U5 snRNA genes in Euglena gracilis§

Cited by 7 publications

References 92 publications

Clustered organization, polycistronic transcription, and evolution of modification-guide snoRNA genes in Euglena gracilis

Clustered organization, polycistronic transcription, and evolution of modification-guide snoRNA genes in Euglena gracilis

Euglena Transcript Processing

The small subunit processome in ribosome biogenesis—progress and prospects

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