Operons Are a Conserved Feature of Nematode Genomes

Jonathan Pettitt, Lucas Philippe, Debjani Sarkar, Christopher Johnston, Henrike Gothe, Diane Massie, Bernadette Connolly, Berndt Muller

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

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. Operons are present in the class Chromadorea, one of the two main nematode classes, but their distribution in the other class, the Enoplea, is not known. We have surveyed the genomes of Trichinella spiralis, Trichuris muris and Romanomermis culicivorax and identified the first putative operons in members of the Enoplea. Consistent with the mechanism of polycistronic RNA resolution in other nematodes, the mRNAs produced by genes downstream of the first gene in the T. spiralis and T. muris operons are trans-spliced to spliced leader RNAs, and we are able to detect polycistronic RNAs derived from these operons. Importantly, a putative intercistronic region from one of these potential enoplean operons confers polycistronic processing activity when expressed as part of a chimeric operon in Caenorhabditis elegans. We find that T. spiralis genes located in operons have an increased likelihood of having operonic C. elegans homologues. However, operon structure in terms of synteny and gene content is not tightly conserved between the two taxa, consistent with models of operon evolution. We have nevertheless identified putative operons conserved between Enoplea and Chromadorea. Our data suggest that operons and 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.
Original languageEnglish
Pages (from-to)1201-1211
Number of pages11
JournalGenetics
Volume197
Issue number4
Early online date1 Jun 2014
DOIs
Publication statusPublished - Aug 2014

Fingerprint

Operon
Genome
Trichinella spiralis
Trans-Splicing
Genes
Caenorhabditis elegans
Mermithoidea
Spliced Leader RNA
RNA
Synteny
Trichuris
Intergenic DNA
RNA Precursors
Multigene Family
Prednisolone
Radiation

Keywords

  • SL trans-splicing
  • nematode genome
  • operons

Cite this

Pettitt, J., Philippe, L., Sarkar, D., Johnston, C., Gothe, H., Massie, D., ... Muller, B. (2014). Operons Are a Conserved Feature of Nematode Genomes. Genetics, 197(4), 1201-1211. https://doi.org/10.1534/genetics.114.162875

Operons Are a Conserved Feature of Nematode Genomes. / Pettitt, Jonathan; Philippe, Lucas; Sarkar, Debjani; Johnston, Christopher; Gothe, Henrike; Massie, Diane; Connolly, Bernadette; Muller, Berndt.

In: Genetics, Vol. 197, No. 4, 08.2014, p. 1201-1211.

Research output: Contribution to journalArticle

Pettitt, J, Philippe, L, Sarkar, D, Johnston, C, Gothe, H, Massie, D, Connolly, B & Muller, B 2014, 'Operons Are a Conserved Feature of Nematode Genomes', Genetics, vol. 197, no. 4, pp. 1201-1211. https://doi.org/10.1534/genetics.114.162875
Pettitt J, Philippe L, Sarkar D, Johnston C, Gothe H, Massie D et al. Operons Are a Conserved Feature of Nematode Genomes. Genetics. 2014 Aug;197(4):1201-1211. https://doi.org/10.1534/genetics.114.162875
Pettitt, Jonathan ; Philippe, Lucas ; Sarkar, Debjani ; Johnston, Christopher ; Gothe, Henrike ; Massie, Diane ; Connolly, Bernadette ; Muller, Berndt. / Operons Are a Conserved Feature of Nematode Genomes. In: Genetics. 2014 ; Vol. 197, No. 4. pp. 1201-1211.
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abstract = "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. Operons are present in the class Chromadorea, one of the two main nematode classes, but their distribution in the other class, the Enoplea, is not known. We have surveyed the genomes of Trichinella spiralis, Trichuris muris and Romanomermis culicivorax and identified the first putative operons in members of the Enoplea. Consistent with the mechanism of polycistronic RNA resolution in other nematodes, the mRNAs produced by genes downstream of the first gene in the T. spiralis and T. muris operons are trans-spliced to spliced leader RNAs, and we are able to detect polycistronic RNAs derived from these operons. Importantly, a putative intercistronic region from one of these potential enoplean operons confers polycistronic processing activity when expressed as part of a chimeric operon in Caenorhabditis elegans. We find that T. spiralis genes located in operons have an increased likelihood of having operonic C. elegans homologues. However, operon structure in terms of synteny and gene content is not tightly conserved between the two taxa, consistent with models of operon evolution. We have nevertheless identified putative operons conserved between Enoplea and Chromadorea. Our data suggest that operons and 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.",
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AU - Pettitt, Jonathan

AU - Philippe, Lucas

AU - Sarkar, Debjani

AU - Johnston, Christopher

AU - Gothe, Henrike

AU - Massie, Diane

AU - Connolly, Bernadette

AU - Muller, Berndt

N1 - We thank Allison Bancroft and Richard Grencis for providing T. muris RNA. The Bristol (N2) C. elegans N2 strain was provided by the Caenorhabditis Genetics Center, which is funded by National Institutes of Health Office of Research Infrastructure Programs (P40 OD010440). This work was funded by a Biotechnology and Biological Sciences Research Council project grant BB/J007137/1.

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N2 - 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. Operons are present in the class Chromadorea, one of the two main nematode classes, but their distribution in the other class, the Enoplea, is not known. We have surveyed the genomes of Trichinella spiralis, Trichuris muris and Romanomermis culicivorax and identified the first putative operons in members of the Enoplea. Consistent with the mechanism of polycistronic RNA resolution in other nematodes, the mRNAs produced by genes downstream of the first gene in the T. spiralis and T. muris operons are trans-spliced to spliced leader RNAs, and we are able to detect polycistronic RNAs derived from these operons. Importantly, a putative intercistronic region from one of these potential enoplean operons confers polycistronic processing activity when expressed as part of a chimeric operon in Caenorhabditis elegans. We find that T. spiralis genes located in operons have an increased likelihood of having operonic C. elegans homologues. However, operon structure in terms of synteny and gene content is not tightly conserved between the two taxa, consistent with models of operon evolution. We have nevertheless identified putative operons conserved between Enoplea and Chromadorea. Our data suggest that operons and 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.

AB - 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. Operons are present in the class Chromadorea, one of the two main nematode classes, but their distribution in the other class, the Enoplea, is not known. We have surveyed the genomes of Trichinella spiralis, Trichuris muris and Romanomermis culicivorax and identified the first putative operons in members of the Enoplea. Consistent with the mechanism of polycistronic RNA resolution in other nematodes, the mRNAs produced by genes downstream of the first gene in the T. spiralis and T. muris operons are trans-spliced to spliced leader RNAs, and we are able to detect polycistronic RNAs derived from these operons. Importantly, a putative intercistronic region from one of these potential enoplean operons confers polycistronic processing activity when expressed as part of a chimeric operon in Caenorhabditis elegans. We find that T. spiralis genes located in operons have an increased likelihood of having operonic C. elegans homologues. However, operon structure in terms of synteny and gene content is not tightly conserved between the two taxa, consistent with models of operon evolution. We have nevertheless identified putative operons conserved between Enoplea and Chromadorea. Our data suggest that operons and 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.

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