Abstract

BackgroundChemoreceptor 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.ResultsBased 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.ConclusionChemoreceptor 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.

Highlights

  • Chemoreceptor proteins mediate the first step in the transduction of environmental chemical stimuli, defining the breadth of detection and conferring stimulus specificity

  • Curation of C. elegans chemoreceptor gene families Genes encoding potential G protein coupled receptor (GPCR) proteins were identified using a variety of methods

  • Most of the GPCR gene candidates fell into families that are unrelated or distantly related to genes in other phyla

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Summary

Introduction

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. Detailed analysis of the cellular basis of chemosensory responses in Caenorhabditis elegans has shown that a small number of sensory neurons mediate all known responses [1]. Despite this cellular simplicity, a huge number of genes encode candidate receptors for chemical stimuli. This work identified several small genomic clusters of related genes encoding members of the rhodopsin superfamily of G-protein-coupled receptors (GPCRs), many of which were shown to be expressed in chemosensory neurons [2]. Subsequent analysis of the (page number not for citation purposes)

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