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A global analysis of Caenorhabditis elegans operons

Author

Listed:
  • Thomas Blumenthal

    (University of Colorado School of Medicine)

  • Donald Evans

    (University of Colorado School of Medicine)

  • Christopher D. Link

    (Institute of Behavioral Genetics, Box 447, University of Colorado)

  • Alessandro Guffanti

    (The Sanger Centre, Wellcome Trust Genome Campus)

  • Daniel Lawson

    (The Sanger Centre, Wellcome Trust Genome Campus)

  • Jean Thierry-Mieg

    (National Institute of Genetics
    National Center for Biotechnology Information)

  • Danielle Thierry-Mieg

    (National Institute of Genetics
    National Center for Biotechnology Information)

  • Wei Lu Chiu

    (Pfizer Global Research & Development—Ann Arbor)

  • Kyle Duke

    (Stanford University Medical Center)

  • Moni Kiraly

    (Stanford University Medical Center)

  • Stuart K. Kim

    (Stanford University Medical Center)

Abstract

The nematode worm Caenorhabditis elegans and its relatives are unique among animals in having operons1. Operons are regulated multigene transcription units, in which polycistronic pre-messenger RNA (pre-mRNA coding for multiple peptides) is processed to monocistronic mRNAs. This occurs by 3′ end formation and trans-splicing using the specialized SL2 small nuclear ribonucleoprotein particle2 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, the complete sequence of the C. elegans genome reveals numerous gene clusters4. To determine how many of these clusters represent operons, we probed full-genome microarrays for SL2-containing mRNAs. We found significant enrichment for about 1,200 genes, including most of a group of several hundred genes represented by complementary DNAs that contain SL2 sequence. Analysis of their genomic arrangements indicates that >90% are downstream genes, falling in 790 distinct operons. Our evidence indicates that the genome contains at least 1,000 operons, 2–8 genes long, that contain about 15% of all C. elegans genes. Numerous examples of co-transcription of genes encoding functionally related proteins are evident. Inspection of the operon list should reveal previously unknown functional relationships.

Suggested Citation

  • Thomas Blumenthal & Donald Evans & Christopher D. Link & Alessandro Guffanti & Daniel Lawson & Jean Thierry-Mieg & Danielle Thierry-Mieg & Wei Lu Chiu & Kyle Duke & Moni Kiraly & Stuart K. Kim, 2002. "A global analysis of Caenorhabditis elegans operons," Nature, Nature, vol. 417(6891), pages 851-854, June.
    • Handle: RePEc:nat:nature:v:417:y:2002:i:6891:d:10.1038_nature00831
    DOI: 10.1038/nature00831
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    Cited by:

    1. Florian Bernard & Delphine Dargère & Oded Rechavi & Denis Dupuy, 2023. "Quantitative analysis of C. elegans transcripts by Nanopore direct-cDNA sequencing reveals terminal hairpins in non trans-spliced mRNAs," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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