Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans


Chromosomes are divided into domains of open chromatin, where genes have the potential to be expressed, and domains of closed chromatin, where genes are not expressed1. Classic examples of open chromatin domains include ‘puffs’ on polytene chromosomes in Drosophila and extended loops from lampbrush chromosomes2,3. If multiple genes were typically expressed together from a single open chromatin domain, the position of co-expressed genes along the chromosomes would appear clustered. To investigate whether co-expressed genes are clustered, we examined the chromosomal positions of the genes expressed in muscle of Caenorhabditis elegans at the first larval stage. Here we show that co-expressed genes in C. elegans are clustered in groups of 2–5 along the chromosomes, suggesting that expression from a chromatin domain can extend over several genes. These observations reveal a higher-order organization of the structure of the genome, in which the order of genes along the chromosome is correlated with their expression in specific tissues.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Outline of the mRNA-tagging technique.
Figure 2: Muscle mRNA tagging.
Figure 3: Genes enriched from muscle by mRNA tagging.
Figure 4: Muscle genes are clustered in small groups of 2–5 genes along the chromosomes.


  1. Weintraub, H. Tissue-specific gene expression and chromatin structure. Harvey Lect. 79, 217–244 (1984)

    CAS  Google Scholar 

  2. Beermann, W. Control of differentiation at the chromosomal level. J. Exp. Zool. 157, 49–62 (1964)

    CAS  Article  Google Scholar 

  3. Gall, J. G. & Callan, H. G. H3 Uridine incorporation in lampbrush chromosomes. Proc. Natl Acad. Sci. USA 48, 562–570 (1962)

    ADS  CAS  Article  Google Scholar 

  4. Gorlach, M., Burd, C. G. & Dreyfuss, G. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell Res. 211, 400–407 (1994)

    CAS  Article  Google Scholar 

  5. Okkema, P. G., Harrison, S. W., Plunger, V., Aryana, A. & Fire, A. Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135, 385–404 (1993)

    CAS  Article  Google Scholar 

  6. Jones, A. R., Francis, R. & Schedl, T. GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180, 165–183 (1996)

    CAS  Article  Google Scholar 

  7. Jiang, M. et al. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 98, 218–223 (2001)

    ADS  CAS  Article  Google Scholar 

  8. Stein, L., Sternberg, P., Durbin, R., Thierry-Mieg, J. & Spieth, J. WormBase: network access to the genome and biology of Caenorhabditis elegans. Nucleic Acids Res. 29, 82–86 (2001)

    CAS  Article  Google Scholar 

  9. Fukami-Kobayashi, K., Tomoda, S. & Go, M. Evolutionary clustering and functional similarity of RNA-binding proteins. FEBS Lett. 335, 289–293 (1993)

    CAS  Article  Google Scholar 

  10. Blumenthal, T. Trans-splicing and polycistronic transcription in Caenorhabditis elegans. Trends Genet. 11, 132–136 (1995)

    CAS  Article  Google Scholar 

  11. Blumenthal, T. Gene clusters and polycistronic transcription in eukaryotes. BioEssays 20, 480–487 (1998)

    CAS  Article  Google Scholar 

  12. Reinke, V. et al. A global profile of germline gene expression in C. elegans. Mol. Cell 6, 605–616 (2000)

    CAS  Article  Google Scholar 

  13. Kim, S. K. et al. A gene expression map for Caenorhabditis elegans. Science 293, 2087–2092 (2001)

    ADS  CAS  Article  Google Scholar 

  14. Cohen, B. A., Mitra, R. D., Hughes, J. D. & Church, G. M. A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nature Genet. 26, 183–186 (2000)

    CAS  Article  Google Scholar 

  15. Caron, H. et al. The human transcriptome map: clustering of highly expressed genes in chromosomal domains. Science 291, 1289–1292 (2001)

    ADS  CAS  Article  Google Scholar 

  16. Hebbes, T. R., Clayton, A. L., Thorne, A. W. & Crane-Robinson, C. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken β-globin chromosomal domain. EMBO J. 13, 1823–1830 (1994)

    CAS  Article  Google Scholar 

  17. Stalder, J. et al. Tissue-specific DNA cleavages in the globin chromatin domain introduced by DNAase I. Cell 20, 451–460 (1980)

    CAS  Article  Google Scholar 

  18. Goodwin, E. B., Okkema, P. G., Evans, T. C. & Kimble, J. Translational regulation of tra-2 by its 3′ untranslated region controls sexual identity in C. elegans. Cell 75, 329–339 (1993)

    CAS  Article  Google Scholar 

  19. Wang, E., Miller, L. D., Ohnmacht, G. A., Liu, E. T. & Marincola, F. M. High-fidelity mRNA amplification for gene profiling. Nature Biotechnol. 18, 457–459 (2000)

    CAS  Article  Google Scholar 

  20. Tenenbaum, S. A., Carson, C. C., Lager, P. J. & Keene, J. D. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc. Natl Acad. Sci. USA 97, 14085–14090 (2000)

    ADS  CAS  Article  Google Scholar 

Download references


We thank J. Shaw, K. Mach, M. Laub, J. Lieb, M. Hiller, E. Harmon and J. Wang for discussions; T. Blumenthal and J. Wang for sharing unpublished results; J. Wang for wild-type poly(A) mRNA; and M. Kiraly for assistance with the Supplementary Information. We also thank the programmers at the Stanford Microarray Database for microarray analysis and database management, and Proteome and Wormbase for annotation of C. elegans genes. P.J.R. is a Stanford University Beckman Fellow. This work was supported by a Human Frontiers Fellowship (P.J.R.) and grants from the National Institutes of Health (S.K.K.).

Author information

Authors and Affiliations


Corresponding author

Correspondence to Stuart K. Kim.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Roy, P., Stuart, J., Lund, J. et al. Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans. Nature 418, 975–979 (2002).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing