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Rapid sequence evolution of transcription factors controlling neuron differentiation in Caenorhabditis.

ABSTRACT: Whether phenotypic evolution proceeds predominantly through changes in regulatory sequences is a controversial issue in evolutionary genetics. Ample evidence indicates that the evolution of gene regulatory networks via changes in cis-regulatory sequences is an important determinant of phenotypic diversity. However, recent experimental work suggests that the role of transcription factor (TF) divergence in developmental evolution may be underestimated. In order to help understand what levels of constraints are acting on the coding sequence of developmental regulatory genes, evolutionary rates were investigated among 48 TFs required for neuronal development in Caenorhabditis elegans. Allelic variation was then sampled for 28 of these genes within a population of the related species Caenorhabditis remanei. Neuronal TFs are more divergent, both within and between species, than structural genes. TFs affecting different neuronal classes are under different levels of selective constraints. The regulatory genes controlling the differentiation of chemosensory neurons evolve particularly fast and exhibit higher levels of within- and between-species nucleotide variation than TFs required for the development of several neuronal classes and TFs required for motorneuron differentiation. The TFs affecting chemosensory neuron development are also more divergent than chemosensory genes expressed in the neurons they differentiate. These results illustrate that TFs are not as highly constrained as commonly thought and suggest that the role of divergence in developmental regulatory genes during the evolution of gene regulatory networks requires further attention.

SUBMITTER: Jovelin R

PROVIDER: S-EPMC2766936 | biostudies-literature | 2009 Oct

REPOSITORIES: biostudies-literature

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Rapid sequence evolution of transcription factors controlling neuron differentiation in Caenorhabditis.

Jovelin Richard R

Molecular biology and evolution 20090709 10

Whether phenotypic evolution proceeds predominantly through changes in regulatory sequences is a controversial issue in evolutionary genetics. Ample evidence indicates that the evolution of gene regulatory networks via changes in cis-regulatory sequences is an important determinant of phenotypic diversity. However, recent experimental work suggests that the role of transcription factor (TF) divergence in developmental evolution may be underestimated. In order to help understand what levels of co ...[more]

PMID: 19589887

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Project description:BackgroundMuch of the morphological diversity in eukaryotes results from differential regulation of gene expression in which transcription factors (TFs) play a central role. The nematode Caenorhabditis elegans is an established model organism for the study of the roles of TFs in controlling the spatiotemporal pattern of gene expression. Using the fully sequenced genomes of three Caenorhabditid nematode species as well as genome information from additional more distantly related organisms (fruit fly, mouse, and human) we sought to identify orthologous TFs and characterized their patterns of evolution.ResultsWe identified 988 TF genes in C. elegans, and inferred corresponding sets in C. briggsae and C. remanei, containing 995 and 1093 TF genes, respectively. Analysis of the three gene sets revealed 652 3-way reciprocal 'best hit' orthologs (nematode TF set), approximately half of which are zinc finger (ZF-C2H2 and ZF-C4/NHR types) and HOX family members. Examination of the TF genes in C. elegans and C. briggsae identified the presence of significant tandem clustering on chromosome V, the majority of which belong to ZF-C4/NHR family. We also found evidence for lineage-specific duplications and rapid evolution of many of the TF genes in the two species. A search of the TFs conserved among nematodes in Drosophila melanogaster, Mus musculus and Homo sapiens revealed 150 reciprocal orthologs, many of which are associated with important biological processes and human diseases. Finally, a comparison of the sequence, gene interactions and function indicates that nematode TFs conserved across phyla exhibit significantly more interactions and are enriched in genes with annotated mutant phenotypes compared to those that lack orthologs in other species.ConclusionOur study represents the first comprehensive genome-wide analysis of TFs across three nematode species and other organisms. The findings indicate substantial conservation of transcription factors even across distant evolutionary lineages and form the basis for future experiments to examine TF gene function in nematodes and other divergent phyla.

Dataset Information

Rapid sequence evolution of transcription factors controlling neuron differentiation in Caenorhabditis.

Publications

Rapid sequence evolution of transcription factors controlling neuron differentiation in Caenorhabditis.

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