Caenorhabditis elegans operons contain a higher proportion of genes with multiple transcripts and use 3' splice sites differentially

Abstract

RNA splicing generates multiple transcript isoforms from a single gene and enhances the complexity of eukaryotic gene expression. In some eukaryotes, operon exists as an ancient regulatory mechanism of gene expression that requires strict positional and regulatory relationships among its genes. It remains unknown whether operonic genes generate transcript isoforms in a similar manner as non-operonic genes do, the expression of which is less likely limited by their positions and relationships with surrounding genes. We analyzed the number of transcript isoforms of Caenorhabditis elegans operonic genes and found that C. elegans operons contain a much higher proportion of genes with multiple transcript isoforms than non-operonic genes do. For genes that express multiple transcript isoforms, there is no apparent difference between the number of isoforms in operonic and non-operonic genes. C. elegans operonic genes also have a different preference of the 20 most common 3' splice sites compared to non-operonic genes. Our analyses suggest that C. elegans operons enhance expression complexity by increasing the proportion of genes that express multiple transcript isoforms and maintain splicing efficiency by differential use of common 3' splice sites.

Figure 1. C. elegans operons contain a higher proportion of genes that express multiple transcript isoforms.

(A) C. elegans operonic genes express more transcript isoforms per gene than non-operonic genes do. (B) C. elegans operons contain a higher proportion of genes that express multiple transcript isoforms than non-operonic genes do. (C) Alternatively spliced C. elegans operonic genes and non-operonic genes have a similar number of transcript isoforms per gene. Z-test was performed (Figure 1A and 1C) to evaluate the significance of difference between the means of transcript numbers. Error bars represent standard deviations.

Figure 2. Common 3′ splice sites are used differentially by C. elegans operonic genes.

The proportions of each 3′ splice site (X axis) of operonic and non-operonic genes were compared to that of all genes of the whole genome and were presented as fold changes (Y axis). Pairwise Z-test was performed (see Table 2) to evaluate the significance of difference between the proportions of each 3′ splice site in operonic genes and non-operonic genes. *: p≤0.01.