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A global analysis of Caenorhabditis elegans operons

Nature volume 417, pages 851–854 (2002)Cite this article

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.

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Figure 1: SL2/poly(A)+ ratios of 17,817 C. elegans genes.
Figure 2: Chromosomal distribution of operons.
Figure 3: Operon intercistronic distances.

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Acknowledgements

We thank J. Spieth, J. Kent, A. Zahler and L. Stein for help with navigation of the C. elegans databases, Y. Kohara for cDNA data, M. Huang for discussions, I. Shah for statistical advice, D. Guiliano and M. Blaxter for communication of unpublished results, and P. MacMorris for advice on the manuscript. This work was supported by the NIH (T.B., C.D.L. and S.K.K.).

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Genetics, University of Colorado School of Medicine, Box B121, 4200 E. 9th Avenue, Colorado, 80262, Denver, USA

    Thomas Blumenthal & Donald Evans

  2. Institute of Behavioral Genetics, Box 447, University of Colorado, Boulder, Colorado, 80309, USA

    Christopher D. Link

  3. The Sanger Centre, Wellcome Trust Genome Campus, CB10 1SA, Hinxton, Cambridge, UK

    Alessandro Guffanti & Daniel Lawson

  4. Gene Network Laboratory, National Institute of Genetics, Mishima, 411, Japan

    Jean Thierry-Mieg & Danielle Thierry-Mieg

  5. National Center for Biotechnology Information, Bethesda, Maryland, USA

    Jean Thierry-Mieg & Danielle Thierry-Mieg

  6. Department of Molecular Sciences and Technologies, Pfizer Global Research & Development—Ann Arbor, 2800 Plymouth Road, Michigan, 48105, Ann Arbor, USA

    Wei Lu Chiu

  7. Departments of Developmental Biology and Genetics, Stanford University Medical Center, 279 Campus Drive, Stanford, California, 94305, USA

    Kyle Duke, Moni Kiraly & Stuart K. Kim

Authors
  1. Thomas Blumenthal
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Corresponding author

Correspondence to Thomas Blumenthal.

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The authors declare that they have no competing financial interests.

Supplementary information

Table 1 (HTM 102 KB)

Genes with SL2-containing cDNA Clones

Table 2 (HTM 512 KB)

List of operons found from the SL2 DNA microarray experiments and predicted by gene structure. Underline denotes cDNA clones containing SL2, bold or red denote genes supported by microarray data

Table 3 (HTM 2 KB)

Co-expression of related genes in the same operon

Table 4 (HTM 3 KB)

Frequencies of having two genes with the same annotation in the same operon

Table 5. Results from DNA microarrays on SL2 enrichment

Tab-delimited format (TXT 1.196 MB)

Comma-delimited format (TXT 1.196 MB)

MS Excel file (XLS 3.306 MB)

  • ORFNAME: unique identifier of the gene

  • SUID: unique Stanford gene identification

  • Expt1

  • Expt2

  • Expt3

  • Expt4

  • Expt5

  • Log(SL2/polyA): average of the log2 of the SL2/polyA ratio

  • STD: standard deviation

  • # exp: number of datapoints used

  • confidence: confidence level from t-test

Table 6 (HTM 77 KB)

List of gene pairs on which the gene spacing was determined

Full data for the DNA microarrays are available at the Stanford Microarray Database (http://genome-www4.stanford.edu/MicroArray/SMD/).

Details for Table 2 (HTM 20 KB)

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Blumenthal, T., Evans, D., Link, C. et al. A global analysis of Caenorhabditis elegans operons. Nature 417, 851–854 (2002). https://doi.org/10.1038/nature00831

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