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Global analysis of Caenorhabditis elegans operons

ABSTRACT: Caenorhabditis elegans and its relatives are unique among animals, possibly even among eukaryotes, in having operons. In these regulated multigene transcription units, a polycistronic pre-mRNA is processed to monocistronic mRNAs by 3' end formation and trans-splicing utilizing a special snRNP, the SL2 snRNP, for downstream mRNAs1. Previously, the correlation between downstream location in an operon and SL2 trans-splicing has been strong, but anecdotal. Although only 28 operons have been reported previously, the complete sequence of the genome reveals numerous gene clusters. To determine how many represent operons, we probed full-genome microarrays for SL2-containing mRNAs. We found significant enrichment for about 1200 genes including most of a group of several hundred genes represented by cDNAs that contain SL2 sequence. Analysis of their genomic arrangements indicates that >90% are downstream genes, falling in 790 distinct operons. We conclude that the genome contains at least 1000 operons, 2- 8 genes in length, that contain ~15% of C. elegans genes. Most of the operons have not been reported previously, and numerous examples of co-transcription of genes encoding functionally related proteins are evident. Inspection of the operon list should reveal heretofore unknown functional relationships. Set of arrays organized by shared biological context, such as organism, tumors types, processes, etc. Keywords: Logical Set

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE2975 | GEO | 2005/07/22

SECONDARY ACCESSION(S): PRJNA91921

REPOSITORIES: GEO

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Global analysis of Caenorhabditis elegans operons

Project description:Caenorhabditis elegans and its relatives are unique among animals, possibly even among eukaryotes, in having operons. In these regulated multigene transcription units, a polycistronic pre-mRNA is processed to monocistronic mRNAs by 3' end formation and trans-splicing utilizing a special snRNP, the SL2 snRNP, for downstream mRNAs1. Previously, the correlation between downstream location in an operon and SL2 trans-splicing has been strong, but anecdotal. Although only 28 operons have been reported previously, the complete sequence of the genome reveals numerous gene clusters. To determine how many represent operons, we probed full-genome microarrays for SL2-containing mRNAs. We found significant enrichment for about 1200 genes including most of a group of several hundred genes represented by cDNAs that contain SL2 sequence. Analysis of their genomic arrangements indicates that >90% are downstream genes, falling in 790 distinct operons. We conclude that the genome contains at least 1000 operons, 2- 8 genes in length, that contain ~15% of C. elegans genes. Most of the operons have not been reported previously, and numerous examples of co-transcription of genes encoding functionally related proteins are evident. Inspection of the operon list should reveal heretofore unknown functional relationships. Set of arrays organized by shared biological context, such as organism, tumors types, processes, etc. Keywords: Logical Set Computed

2005-07-22 | E-GEOD-2975 | biostudies-arrayexpress

Transcription profiling of C. elegans operons

Project description:Caenorhabditis elegans and its relatives are unique among animals, possibly even among eukaryotes, in having operons1. In these regulated multigene transcription units, a polycistronic pre-mRNA is processed to monocistronic mRNAs by 3' end formation and trans-splicing utilizing a special snRNP, the SL2 snRNP2, for downstream mRNAs1. Previously, the correlation between downstream location in an operon and SL2 trans-splicing has been strong, but anecdotal3. Although only 28 operons have been reported previously, the complete sequence of the genome reveals numerous gene clusters4. To determine how many represent operons, we probed full-genome microarrays for SL2-containing mRNAs. We found significant enrichment for about 1200 genes including most of a group of several hundred genes represented by cDNAs that contain SL2 sequence. Analysis of their genomic arrangements indicates that >90% are downstream genes, falling in 790 distinct operons. We conclude that the genome contains at least 1000 operons, 2- 8 genes in length, that contain ~15% of C. elegans genes. Most of the operons have not been reported previously, and numerous examples of co-transcription of genes encoding functionally related proteins are evident. Inspection of the operon list should reveal heretofore unknown functional relationships.

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RNA polymerase II CTD S2P is dispensable during embryogenesis but regulates the developmental diapause in C. elegans [ChIP-seq]

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Project description:Genes clustered into polycistronic operons was thought a characteristic of bacteria and many other species. More than half protein-coding genes are organized in polycistronic operons composed of two or more than ten genes in bacterial genomes. Although the structure of operons have been studied precisely, how the member genes within operon maintain their stoichiometry expression is remain unknown. Using a highly accurate label-free absolute quantification method DIA (data-independent acquisition), we present a global analysis of Escherichia coli proteome, quantified 1607 proteins, including 59.1% of the known polycistronic operons. We found shorter operons tend to be more tightly controlled than longer operons, and those operons for metabolic pathways are less controlled for stoichiometry balance than those operons for protein complexes. Our results thus reveal the two-level regulation mode involving transcription and translation of operons would balance the stoichiometry expression of genes in polycistronic operons in different time-scale.

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Project description:More than half of the protein-coding genes in bacteria are organized in polycistronic operons composed of two or more genes. Whether the operon organization maintains the stoichiometric expression of the genes within an operon remain under debate. In this study, we performed a label-free data-independent acquisition hyper reaction monitoring mass-spectrometry (HRM-MS) experiment to quantify the Escherichia coli proteome in exponential phase and quantified 93.6% of the cytosolic proteins, covering 67.9% and 56.0% of the translating polycistronic operons in BW25113 and MG1655 strains, respectively. We found the shorter operons tend to be more tightly controlled for stoichiometry than longer operons, and those operons for metabolic pathways are less controlled for stoichiometry compared with operons for protein complexes, illustrating the multifaceted nature of the operon-wise regulation: the operon-wise unified transcriptional level and gene-specific translational level. This multi-level regulation benefits the host by optimizing the efficiency of the productivity of metabolic pathways and maintenance of different types of protein complexes.

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XRN2 Autoregulation and Control of Polycistronic Gene Expression in Caenorhabditis elegans

Project description:XRN2 is a conserved 5’-->3’ exoribonuclease that complexes with XTB-domain containing proteins. Thus, in Caenorhabditis elegans (C. elegans), the XTBD-protein PAXT-1 stabilizes XRN2 to retain its activity. XRN2 activity is also promoted by 3'(2'),5'-bisphosphate nucleotidase 1 (BPNT1) through its hydrolysis of 3’-phosphoadenosine-5'-bisphosphate (PAP), an endogenous XRN inhibitor. Here, we find through unbiased screening that loss of bpnt-1 function suppresses lethality caused by paxt-1 deletion. This unexpected finding is explained by XRN2 autoregulation, which occurs through repression of a cryptic promoter activity and destabilization of the xrn-2 transcript. Autoregulation appears to be triggered at different thresholds of XRN2 inactivation, such that more robust XRN2 perturbation, by elimination of both PAXT-1 and BPNT1, is less detrimental to worm viability than absence of PAXT-1 alone. Like more than 15% of C. elegans genes, xrn-2 occurs in an operon, and we identify additional operons under its control, consistent with a broader function of XRN2 in polycistronic gene regulation. Regulation occurs through intercistronic regions that link genes in an operon, but similar mechanisms may allow XRN2 to operate on monocistronic genes in organisms lacking operons.

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XRN2 Autoregulation and Control of Polycistronic Gene Expression in Caenorhabditis elegans

Project description:XRN2 is a conserved 5â??-->3â?? exoribonuclease that complexes with XTB-domain containing proteins. Thus, in Caenorhabditis elegans (C. elegans), the XTBD-protein PAXT-1 stabilizes XRN2 to retain its activity. XRN2 activity is also promoted by 3'(2'),5'-bisphosphate nucleotidase 1 (BPNT1) through its hydrolysis of 3â??-phosphoadenosine-5'-bisphosphate (PAP), an endogenous XRN inhibitor. Here, we find through unbiased screening that loss of bpnt-1 function suppresses lethality caused by paxt-1 deletion. This unexpected finding is explained by XRN2 autoregulation, which occurs through repression of a cryptic promoter activity and destabilization of the xrn-2 transcript. Autoregulation appears to be triggered at different thresholds of XRN2 inactivation, such that more robust XRN2 perturbation, by elimination of both PAXT-1 and BPNT1, is less detrimental to worm viability than absence of PAXT-1 alone. Like more than 15% of C. elegans genes, xrn-2 occurs in an operon, and we identify additional operons under its control, consistent with a broader function of XRN2 in polycistronic gene regulation. Regulation occurs through intercistronic regions that link genes in an operon, but similar mechanisms may allow XRN2 to operate on monocistronic genes in organisms lacking operons. Wild-type C. elegans worms were subjected to mock or xrn-2 RNAi from L1 to L4 stage at 20Â°C. Total RNA was extracted from the worms, and polyadenylated RNA was analyzed.

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