Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny

Abstract

To determine whether the distinctive features of Caenorhabditis elegans chromosomal organization are shared with the C. briggsae genome, we constructed a single nucleotide polymorphism-based genetic map to order and orient the whole genome shotgun assembly along the six C. briggsae chromosomes. Although these species are of the same genus, their most recent common ancestor existed 80-110 million years ago, and thus they are more evolutionarily distant than, for example, human and mouse. We found that, like C. elegans chromosomes, C. briggsae chromosomes exhibit high levels of recombination on the arms along with higher repeat density, a higher fraction of intronic sequence, and a lower fraction of exonic sequence compared with chromosome centers. Despite extensive intrachromosomal rearrangements, 1:1 orthologs tend to remain in the same region of the chromosome, and colinear blocks of orthologs tend to be longer in chromosome centers compared with arms. More strikingly, the two species show an almost complete conservation of synteny, with 1:1 orthologs present on a single chromosome in one species also found on a single chromosome in the other. The conservation of both chromosomal organization and synteny between these two distantly related species suggests roles for chromosome organization in the fitness of an organism that are only poorly understood presently.

Figure 1. Percent Recovery of the AF16 Allele in the RI Lines for Each of the Markers Plotted against Its Position in cM on C. briggsae Chromosomes CbIII and CbIV

Alleles from AF16 are less frequently recovered for much of CbIII, whereas for CbIV, the opposite holds. See Dataset S2 for other chromosomes.

Figure 2. Example of the Transition in Synteny for an Assembly with Discrepant Genetic Markers

For fpc contig cb25.fpc2454, the positions of 1:1 orthologs pairs are plotted both along the C. briggsae sequence (x-axis) and the C. elegans genome sequence (y-axis). The regions shown from two C. elegans chromosomes accounted for almost all of the orthologs from cb25.fpc2454. The positions of the SNP markers with their C. briggsae genetic map assignments are indicated along the x-axis. The region between the rightmost chromosome II ortholog at 524,614 and the leftmost chromosome V ortholog at 531,820 contained a single gap at 527,846 between supercontigs; the fpc contig was split at this gap.

Figure 3. Recombination and Physical Distance in C. briggsae

The panels show Marey plots [16] for chromosomes CbI (A) and CbX (B) in which the position in cM is plotted against the sequence position for each SNP marker. Recombination is high on the arms of CbI and low in the center. Other autosomes broadly follow this pattern (Figure S4). The difference between arms and centers on CbX is less marked.

Figure 4. Variation of Features by Chromosomal Region Illustrated Using C. briggsae Chromosome III

Features were examined in 500-kb windows in 100-kb steps along each chromosome. (A) The greater percentage of intronic sequence, the increased density of percentage of repeats (scale on left axis), and the greater number of telomere repeat sequences (TTAGGC) on the arms of CbIII (scale on the right axis). (B) The percentage of sequence present in exons (scale on left axis) and the percentage of exons in 1:1 orthologs (scale on right axis) for CbIII. Other autosomes all show this general pattern, with some variation for each feature (see Figures S1 and S2 for both C. briggsae and C. elegans).

Figure 5. Chromosomal Positions of Orthologs

The chromosomal positions of the orthologs in the two species reveals colinearity and breakpoints. The positions of ortholog pairs along the chromosomes of the two species are plotted against one another for chromosomes IV (A) and X (B). The position of each pair is designated with a “+”. Extensive colinearity of pairs produces an apparent line. The box in the center of each panel (dotted line) delimits the region of low recombination based on inspection of the Marey plots (Table 6). See Figure S4 for other chromosomes and for similar data for C. elegans.

Figure 6. Sequence Similarity of Syntenic and Nonsyntenic Ortholog Pairs

Syntenic and nonsyntenic ortholog pairs differ in their sequence similarity. The distribution of the percent identity, binned in five percentile bins, is shown both for pairs on the same chromosome (syntenic) and on different chromosomes (nonsyntenic).