The Caenorhabditis chemoreceptor gene families

Abstract

Background: Chemoreceptor proteins mediate the first step in the transduction of environmental chemical stimuli, defining the breadth of detection and conferring stimulus specificity. Animal genomes contain families of genes encoding chemoreceptors that mediate taste, olfaction, and pheromone responses. The size and diversity of these families reflect the biology of chemoperception in specific species.

Results: Based on manual curation and sequence comparisons among putative G-protein-coupled chemoreceptor genes in the nematode Caenorhabditis elegans, we identified approximately 1300 genes and 400 pseudogenes in the 19 largest gene families, most of which fall into larger superfamilies. In the related species C. briggsae and C. remanei, we identified most or all genes in each of the 19 families. For most families, C. elegans has the largest number of genes and C. briggsae the smallest number, suggesting changes in the importance of chemoperception among the species. Protein trees reveal family-specific and species-specific patterns of gene duplication and gene loss. The frequency of strict orthologs varies among the families, from just over 50% in two families to less than 5% in three families. Several families include large species-specific expansions, mostly in C. elegans and C. remanei.

Conclusion: Chemoreceptor gene families in Caenorhabditis species are large and evolutionarily dynamic as a result of gene duplication and gene loss. These dynamics shape the chemoreceptor gene complements in Caenorhabditis species and define the receptor space available for chemosensory responses. To explain these patterns, we propose the gray pawn hypothesis: individual genes are of little significance, but the aggregate of a large number of diverse genes is required to cover a large phenotype space.

Figure 1

Sample protein tree. This tree is a section from the complete SRG protein tree (Additional file 20). Protein names are colored by species (green is Caenorhabditis elegans, blue is C. briggsae, and red is C. remanei). In addition to identifiers, each name includes the genome position of the corresponding gene. Open circles on branches indicate a branch support value of 0.9 or higher, as computed by phyml-alrt. The scale bar indicates number of amino acid changes per site. Probable strict ortholog trios are marked with filled black squares. A representative gene expansion in C. elegans is marked and a view of the gene arrangement is expanded to the right (adapted from the WormBase genome browser, WS170). An alignment of four of the C. elegans proteins from this gene expansion is shown in the lower right. Blue coloring is proportional to amino acid conservation.

Figure 2

Negative correlation between orthology and nonfunctional gene frequencies in Caenorhabditis elegans. Each of the 19 gene families is plotted once. The X-axis is the fraction of C. elegans genes in the family with single orthologs in both C. briggsae and C. remanei. The Y-axis is the fraction of C. elegans genes in the family with probable defective alleles in the N2 reference genome sequence. The correlation shown is much stronger than that between family size and fraction of defective genes (see Additional file 9). R is the Pearson correlation coefficient.