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Comparative Study
. 2003 Feb;13(2):238-43.
doi: 10.1101/gr.553803.

Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes

Martin J Lercher  1 , Thomas Blumenthal, Laurence D Hurst
Affiliations
Comparative Study

Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes

Martin J Lercher et al. Genome Res. 2003 Feb.

Abstract

In many eukaryotic species, gene order is not random. In humans, flies, and yeast, there is clustering of coexpressed genes that cannot be explained as a trivial consequence of tandem duplication. In the worm genome this is taken a step further with many genes being organized into operons. Here we analyze the relationship between gene location and expression in Caenorhabditis elegans and find evidence for at least three different processes resulting in local expression similarity. Not surprisingly, the strongest effect comes from genes organized in operons. However, coexpression within operons is not perfect, and is influenced by some distance-dependent regulation. Beyond operons, there is a relationship between physical distance, expression similarity, and sequence similarity, acting over several megabases. This is consistent with a model of tandem duplicate genes diverging over time in sequence and expression pattern, while moving apart owing to chromosomal rearrangements. However, at a very local level, nonduplicate genes on opposite strands (hence not in operons) show similar expression patterns. This suggests that such genes may share regulatory elements or be regulated at the level of chromatin structure. The central importance of tandem duplicate genes in these patterns renders the worm genome different from both yeast and human.

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Figures

Figure 1.
Figure 1.
Level of coexpression for 20-kb distance bins, for microarray data (A) and for functional classes (B). (Insets) Data for 2-kb distance bins. The solid lines are linear regressions (microarray data: R2 = 0.88, functions: R2 = 0.21 for 0.5–5 Mb).
Figure 1.
Figure 1.
Level of coexpression for 20-kb distance bins, for microarray data (A) and for functional classes (B). (Insets) Data for 2-kb distance bins. The solid lines are linear regressions (microarray data: R2 = 0.88, functions: R2 = 0.21 for 0.5–5 Mb).
Figure 2.
Figure 2.
Distance dependence of coexpression for gene pairs within operons, including all gene pairs and after the exclusion of duplicate gene pairs. In both cases, we find a significant negative correlation (all genes: R2 = 0.79, P = 0.00003; excl. duplicates: R2 = 0.67, P = 0.0005).
Figure 3.
Figure 3.
Level of coexpression for 20-kb distance bins after removal of duplicate genes, for microarray data (A) and for functional classes (B). For comparison, the open symbols show data before the removal of duplicates [circles: all genes; triangles: random subsets of 2679 genes (A) and 1959 genes (B)].
Figure 3.
Figure 3.
Level of coexpression for 20-kb distance bins after removal of duplicate genes, for microarray data (A) and for functional classes (B). For comparison, the open symbols show data before the removal of duplicates [circles: all genes; triangles: random subsets of 2679 genes (A) and 1959 genes (B)].
Figure 4.
Figure 4.
Distribution of duplicate genes in 20-kb distance bins. (A) Fraction of duplicate gene pairs relative to all pairs at this distance; (B) mean log(Expect) as a measure of similarity. The insets show data for 2-kb distance bins. The solid lines are linear regressions (duplicate fraction: R2 = 0.70, log(Expect): R2 = 0.66 for 0.5–5 Mb). The functional form seems to change at ∼30 kb and at ∼200 kb.
Figure 4.
Figure 4.
Distribution of duplicate genes in 20-kb distance bins. (A) Fraction of duplicate gene pairs relative to all pairs at this distance; (B) mean log(Expect) as a measure of similarity. The insets show data for 2-kb distance bins. The solid lines are linear regressions (duplicate fraction: R2 = 0.70, log(Expect): R2 = 0.66 for 0.5–5 Mb). The functional form seems to change at ∼30 kb and at ∼200 kb.
Figure 5.
Figure 5.
Simplified representation of three putative modes of coexpression in C. elegans. The indicated distances are meant for rough guidance only. The fourth putative mode, chromatin-level regulation, is not depicted.
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