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Operons are a conserved feature of nematode genomes.

Pettitt J, Philippe L, Sarkar D, Johnston C, Gothe HJ, Massie D, Connolly B, Müller B - Genetics (2014)

Bottom Line: The organization of genes into operons, clusters of genes that are co-transcribed to produce polycistronic pre-mRNAs, is a trait found in a wide range of eukaryotic groups, including multiple animal phyla.We have nevertheless identified putative operons conserved between Enoplea and Chromadorea.Our data suggest that operons and "spliced leader" (SL) trans-splicing predate the radiation of the nematode phylum, an inference which is supported by the phylogenetic profile of proteins known to be involved in nematode SL trans-splicing.

View Article: PubMed Central - PubMed

Affiliation: School of Medical Sciences, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, United Kingdom j.pettitt@abdn.ac.uk.

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Evidence for the existence of an enoplean operon. (A) Schematic showing the genomic organization of zgpa-1, dif-1, and aph-1 in selected nematodes mapped onto their phylogenetic relationships. Arrows represent genes, and the gray lines represent the intercistronic regions (ICRs). Numbers above the ICRs represent the distances, in base pairs, between the stop and start codons of the upstream and downstream genes, respectively. The C. elegans operon numbers are given where appropriate. Fractions below the T. spiralis and T. muris genes represent the proportion of cDNAs derived from those genes that begins with a spliced leader sequence (see also Table S2). In C. elegans, the three genes are part of different operons. * indicates the distance between genes on chromosome IV. (B) Detecting polycistronic RNAs derived from the zgpa-1∼dif-1∼aph-1 operon in enoplean nematodes. The exon–intron structures of the amplicons used to identify polycistronic RNAs are shown, with exons represented by boxes (shaded to identify the genes from which they are derived using the same color coding that was used in A. The intercistronic regions are represented by cream-colored boxes. The positions of the SL trans-spliced 3′ splice sites are indicated. The length of each cDNA is indicated.
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fig1: Evidence for the existence of an enoplean operon. (A) Schematic showing the genomic organization of zgpa-1, dif-1, and aph-1 in selected nematodes mapped onto their phylogenetic relationships. Arrows represent genes, and the gray lines represent the intercistronic regions (ICRs). Numbers above the ICRs represent the distances, in base pairs, between the stop and start codons of the upstream and downstream genes, respectively. The C. elegans operon numbers are given where appropriate. Fractions below the T. spiralis and T. muris genes represent the proportion of cDNAs derived from those genes that begins with a spliced leader sequence (see also Table S2). In C. elegans, the three genes are part of different operons. * indicates the distance between genes on chromosome IV. (B) Detecting polycistronic RNAs derived from the zgpa-1∼dif-1∼aph-1 operon in enoplean nematodes. The exon–intron structures of the amplicons used to identify polycistronic RNAs are shown, with exons represented by boxes (shaded to identify the genes from which they are derived using the same color coding that was used in A. The intercistronic regions are represented by cream-colored boxes. The positions of the SL trans-spliced 3′ splice sites are indicated. The length of each cDNA is indicated.

Mentions: As part of the analysis of the transcriptome of the free-living enoplean, Prionchulus punctatus, we identified an EST corresponding to an SL trans-spliced mRNA. Sequence similarity searches using this sequence identified a single predicted T. spiralis gene, Tsp_06075. However, subsequent sequence analysis of Tsp_06075 showed that it corresponds to an erroneous gene prediction, which conflates three genes that are the orthologs of the C. elegans genes zgpa-1 (C33H5.17), dif-1, and aph-1, respectively. That Tsp_06075 is actually three separate genes was confirmed by sequence analysis of 5′ RACE products. It seems likely that the unusually short intergenic regions that exist between these three T. spiralis genes caused the gene annotation error (Figure 1). Such short intergenic distances are characteristic of nematode genes that are arranged into operons (Blumenthal et al. 2002; Guiliano and Blaxter 2006; Ghedin et al. 2007), and we thus decided to investigate the possibility that Tsp-zgpa-1, Tsp-dif-1, and Tsp-aph-1 constitute an operon. In parallel, we also analyzed the homologs of these three genes in the closely related enoplean, T. muris, which show the same syntenic arrangement, although the intergenic distance between Tmu-dif-1 and Tmu-aph-1 is much larger than expected for an ICR. The three C. elegans homologs although organized into operons, are not found in the same operon. However, in a close relative of C. elegans, Pristionchus pacificus, zgpa-1 and dif-1 could potentially constitute a single operon, but again the intergenic space between the two genes is also relatively large compared to the average size of ICRs in C. elegans operons.


Operons are a conserved feature of nematode genomes.

Pettitt J, Philippe L, Sarkar D, Johnston C, Gothe HJ, Massie D, Connolly B, Müller B - Genetics (2014)

Evidence for the existence of an enoplean operon. (A) Schematic showing the genomic organization of zgpa-1, dif-1, and aph-1 in selected nematodes mapped onto their phylogenetic relationships. Arrows represent genes, and the gray lines represent the intercistronic regions (ICRs). Numbers above the ICRs represent the distances, in base pairs, between the stop and start codons of the upstream and downstream genes, respectively. The C. elegans operon numbers are given where appropriate. Fractions below the T. spiralis and T. muris genes represent the proportion of cDNAs derived from those genes that begins with a spliced leader sequence (see also Table S2). In C. elegans, the three genes are part of different operons. * indicates the distance between genes on chromosome IV. (B) Detecting polycistronic RNAs derived from the zgpa-1∼dif-1∼aph-1 operon in enoplean nematodes. The exon–intron structures of the amplicons used to identify polycistronic RNAs are shown, with exons represented by boxes (shaded to identify the genes from which they are derived using the same color coding that was used in A. The intercistronic regions are represented by cream-colored boxes. The positions of the SL trans-spliced 3′ splice sites are indicated. The length of each cDNA is indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4125394&req=5

fig1: Evidence for the existence of an enoplean operon. (A) Schematic showing the genomic organization of zgpa-1, dif-1, and aph-1 in selected nematodes mapped onto their phylogenetic relationships. Arrows represent genes, and the gray lines represent the intercistronic regions (ICRs). Numbers above the ICRs represent the distances, in base pairs, between the stop and start codons of the upstream and downstream genes, respectively. The C. elegans operon numbers are given where appropriate. Fractions below the T. spiralis and T. muris genes represent the proportion of cDNAs derived from those genes that begins with a spliced leader sequence (see also Table S2). In C. elegans, the three genes are part of different operons. * indicates the distance between genes on chromosome IV. (B) Detecting polycistronic RNAs derived from the zgpa-1∼dif-1∼aph-1 operon in enoplean nematodes. The exon–intron structures of the amplicons used to identify polycistronic RNAs are shown, with exons represented by boxes (shaded to identify the genes from which they are derived using the same color coding that was used in A. The intercistronic regions are represented by cream-colored boxes. The positions of the SL trans-spliced 3′ splice sites are indicated. The length of each cDNA is indicated.
Mentions: As part of the analysis of the transcriptome of the free-living enoplean, Prionchulus punctatus, we identified an EST corresponding to an SL trans-spliced mRNA. Sequence similarity searches using this sequence identified a single predicted T. spiralis gene, Tsp_06075. However, subsequent sequence analysis of Tsp_06075 showed that it corresponds to an erroneous gene prediction, which conflates three genes that are the orthologs of the C. elegans genes zgpa-1 (C33H5.17), dif-1, and aph-1, respectively. That Tsp_06075 is actually three separate genes was confirmed by sequence analysis of 5′ RACE products. It seems likely that the unusually short intergenic regions that exist between these three T. spiralis genes caused the gene annotation error (Figure 1). Such short intergenic distances are characteristic of nematode genes that are arranged into operons (Blumenthal et al. 2002; Guiliano and Blaxter 2006; Ghedin et al. 2007), and we thus decided to investigate the possibility that Tsp-zgpa-1, Tsp-dif-1, and Tsp-aph-1 constitute an operon. In parallel, we also analyzed the homologs of these three genes in the closely related enoplean, T. muris, which show the same syntenic arrangement, although the intergenic distance between Tmu-dif-1 and Tmu-aph-1 is much larger than expected for an ICR. The three C. elegans homologs although organized into operons, are not found in the same operon. However, in a close relative of C. elegans, Pristionchus pacificus, zgpa-1 and dif-1 could potentially constitute a single operon, but again the intergenic space between the two genes is also relatively large compared to the average size of ICRs in C. elegans operons.

Bottom Line: The organization of genes into operons, clusters of genes that are co-transcribed to produce polycistronic pre-mRNAs, is a trait found in a wide range of eukaryotic groups, including multiple animal phyla.We have nevertheless identified putative operons conserved between Enoplea and Chromadorea.Our data suggest that operons and "spliced leader" (SL) trans-splicing predate the radiation of the nematode phylum, an inference which is supported by the phylogenetic profile of proteins known to be involved in nematode SL trans-splicing.

View Article: PubMed Central - PubMed

Affiliation: School of Medical Sciences, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, United Kingdom j.pettitt@abdn.ac.uk.

Show MeSH
Related in: MedlinePlus