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Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans

Abstract

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.

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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.

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Acknowledgements

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K. Mach, M. Laub, J. Lieb, M. Hiller, E. Harmon and J. Wang for discussions; T. Blumenthal and J. Wang for sharing unpublished results; J. Wang for wild-type poly(A) mRNA; and M. Kiraly for assistance with the Supplementary Information.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.).

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Correspondence to Stuart K. Kim.

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Roy, P., Stuart, J., Lund, J. et al. Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans. Nature 418, 975–979 (2002). https://doi.org/10.1038/nature01012

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