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. 2008 Mar;18(3):412-21.
doi: 10.1101/gr.7112608. Epub 2008 Jan 24.

Evolutionary dynamics of nematode operons: easy come, slow go

Wenfeng Qian  1 , Jianzhi Zhang
Affiliations

Evolutionary dynamics of nematode operons: easy come, slow go

Wenfeng Qian et al. Genome Res. 2008 Mar.

Abstract

Operons are widespread in prokaryotes, but are uncommon in eukaryotes, except nematode worms, where approximately 15% of genes reside in over 1100 operons in the model organism Caenorhabditis elegans. It is unclear how operons have become abundant in nematode genomes. The "one-way street" hypothesis asserts that once formed by chance, operons are very difficult to break, because the breakage would leave downstream genes in an operon without a promoter, and hence, unexpressed. To test this hypothesis, we analyzed the presence and absence of C. elegans operons in Caenorhabditis briggsae, Caenorhabditis remanei, and Caenorhabditis brenneri, using Pristionchus pacificus and Brugia malayi as outgroups, and identified numerous operon gains and losses. Coupled with experimental examination of trans-splicing patterns, our comparative genomic analysis revealed diverse molecular mechanisms of operon losses, including inversion, insertion, and relocation, but the presence of internal promoters was not found to facilitate operon losses. In several cases, the data allowed inference of mechanisms by which downstream genes are expressed after operon breakage. We found that the rate of operon gain is approximately 3.3 times that of operon loss. Thus, the evolutionary dynamics of nematode operons is better described as "easy come, slow go," rather than a "one-way street." Based on a mathematic model of operon gains and losses and additional assumptions, we projected that the number of operons in C. elegans will continue to rise by 6%-18% in future evolution before reaching equilibrium between operon gains and losses.

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Figures

Figure 1.
Figure 1.
Gains and losses of operons in Caenorhabditis nematodes. The numbers of C. elegans operons showing various presence/absence phylogenetic distributions are given at the top of the figure, with the inferred numbers of operon gains (circled) and losses presented on tree branches. There are no C. elegans operons that are absent in all of the other three Caenorhabditis species, but present in one or two of the outgroups (P. pacificus and B. malayi). A pair of linked black circles shows the presence of an operon, while a pair of unlinked white circles shows the absence of the operon. Dashes show undetermined status.
Figure 2.
Figure 2.
Relationship between the proportion (f) of genes that can potentially be included in operons and the projected number of operons in the genome at equilibrium (left Y-axis) and that between f and the predicted evolutionary time since the origin of operons (right Y-axis), in unit of T, the divergence time between C. elegans and C. briggsae.
Figure 3.
Figure 3.
Proportions of genes showing different RNAi phenotypes in different gene categories. The phenotypic data are from Kamath et al. (2003). Error bars show one standard error.
Figure 4.
Figure 4.
Mechanisms of operon losses. Black arrows stand for genes belonging to operons in C. elegans or their orthologs in other species, with the circled numbers above the arrows showing the order of the genes in the C. elegans operon. Gray arrows show other genes. In C. elegans, horizontal solid lines link genes belonging to the same operon (boxed) and horizontal dash lines link genes not belonging to the same operon. In other species, genes inferred to be in the same operons are linked by horizontal solid lines; otherwise, they are linked by horizontal dash lines. Dotted lines show orthologous relationship between genes. In C. elegans, Caenorhabditis Genetics Center (CGC) names or sequence names are shown above the gene model, while in other species, the names are shown if they exist in WormBase release WS182. The operon breakage mechanisms shown here include inversion (A), relocation (B), and insertion (C).
Figure 5.
Figure 5.
RT–PCR results showing the trans-splicing forms of various genes of C. briggsae. DNA bands are shown in white, while the background is black. Primers used are listed in Supplemental Table S3.
Figure 6.
Figure 6.
Mechanisms of operon gains. Black arrows stand for genes belonging to operons in C. elegans or their orthologs in other species, with the circled numbers above the arrows showing the order of the genes in the C. elegans operon. Gray arrows show other genes. In C. elegans, horizontal solid lines link genes belonging to the same operon (boxed) and horizontal dash lines link genes not belonging to the same operon. In other species, genes inferred to be in the same operons are linked by horizontal solid lines; otherwise, they are linked by horizontal dash lines. Dotted lines show orthologous relationship between genes. In C. elegans, Caenorhabditis Genetics Center (CGC), names or sequence names are shown above the gene model, while in other species, the names are shown if they exist in WormBase release WS182. (A) Formation of a new operon in C. elegans. (B) Comparison of intergenic distances between old operons and new operons. New operons are those formed after the divergence between C. elegans and C. briggsae, while old operons are those formed before that divergence. (C) Expansion of an existing operon by addition of F54E12.2 as the first gene in CEOP4440 in the C. elegans lineage.
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