Fourfold faster rate of genome rearrangement in nematodes than in Drosophila

Abstract

We compared the genome of the nematode Caenorhabditis elegans to 13% of that of Caenorhabditis briggsae, identifying 252 conserved segments along their chromosomes. We detected 517 chromosomal rearrangements, with the ratio of translocations to inversions to transpositions being approximately 1:1:2. We estimate that the species diverged 50-120 million years ago, and that since then there have been 4030 rearrangements between their whole genomes. Our estimate of the rearrangement rate, 0.4-1.0 chromosomal breakages/Mb per Myr, is at least four times that of Drosophila, which was previously reported to be the fastest rate among eukaryotes. The breakpoints of translocations are strongly associated with dispersed repeats and gene family members in the C. elegans genome.

Figure 1

Distribution of sizes of conserved segments, measured in units of kilobases (A) and genes (B) with respect to Caenorhabditis elegans. These conserved segments were assumed to have resulted from fissure of chromosomes by reciprocal translocations.

Figure 2

The Caenorhabditis elegans region surrounding the sex-1 locus (F44A6.2B), and the corresponding region in Caenorhabditis briggsae. The pale blue bar wrapped over two lines represents the region between coordinates 10.18–10.23 Mb of C. elegans chromosome X, and the navy bar represents 3.50–3.57 Mb of C. briggsae contig RWRA. There are five orthologous briggsae:elegans genes (red) in the conserved segment, which are identified by the same number (1–5) in the two species, and are named on the C. elegans map. Inversion (I) and transposition (T) breakpoints are marked with orange arrows, which are shown arbitrarily on the C. briggsae chromosome. A region including three genes (C07A4.1, F09B9.3, and F09B9.2) has been inverted in either C. elegans or C. briggsae since speciation. Furthermore, a region comprising six genes (gray) between C07A4.1 and F44A6.1 in C. elegans has transposed to another part of the C. briggsae genome, or has transposed into this part of the C. elegans genome.

Figure 3

(A) Location of conserved segments in the Caenorhabditis elegans genome. Gray bars under the autosomes show the “central clusters” described by Barnes et al. (1995). The segments cover ∼15% of chromosome I, 7% of II, 10% of III, 13% of IV, 15% of V, and 20% of X. (B) Matrix plot comparison between the C. elegans genome (vertical axis) and the nine Caenorhabditis briggsae contigs (horizontal axis). Conserved segments are indicated by lines drawn between the positions of the outermost genes in each species.

Figure 4

Estimates of the briggsae–elegans speciation date from 92 sets of Caenorhabditis briggsae, Caenorhabditis elegans, Drosophila, and human orthologs, calculated by taking the nematode–arthropod divergence date to be 1000 Mya.

Figure 5

(A) Sizes of inversions in kilobases, with respect to Caenorhabditis elegans. (B) Sizes of inversions, measured in units of genes. (C) Sizes of transpositions in kilobases. (D) Sizes of transpositions, measured in units of genes.

Figure 6

Method of detecting inversions and transpositions. (A) To detect transpositions to or from unsequenced parts of the Caenorhabditis briggsae genome, we looked along C. briggsae contigs for adjacent genes b1 and b2 whose Caenorhabditis elegans orthologs e1 and e2 are on the same chromosome, where between e1 and e2 there are 1–50 C. elegans genes with unknown C. briggsae orthologs. We assumed that the genes between 1 and 2 have transposed in either C. briggsae or C. elegans. (T) Transposition breakpoints. (B) To detect transpositions to or from sequenced parts of the C. briggsae genome, we looked along C. briggsae contigs for three conserved segments in a row, where in C. elegans the first and third segments were close together on the same chromosome, and the middle segment was far away on the same C. elegans chromosome or on a different C. elegans chromosome. We assumed that the middle segment (genes 4–5) had transposed in either C. briggsae or C. elegans. (C) To detect inversions, we looked along C. briggsae contigs for three conserved segments in a row, where in C. elegans the first and third segments were close together on the same chromosome, and the middle segment was far away on the same C. elegans chromosome or on a different C. elegans chromosome, and either the first or third segment, or both, had inverted in either C. briggsae or C. elegans. Here the third segment (genes 6–7) has inverted.