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Evolution of an insect-specific GROUCHO-interaction motif in the ENGRAILED selector protein.

ABSTRACT: Animal morphology evolves through alterations in the genetic regulatory networks that control development. Regulatory connections are commonly added, subtracted, or modified via mutations in cis-regulatory elements, but several cases are also known where transcription factors have gained or lost activity-modulating peptide motifs. In order to better assess the role of novel transcription factor peptide motifs in evolution, we searched for synapomorphic motifs in the homeotic selectors of Drosophila melanogaster and related insects. Here, we describe an evolutionarily novel GROUCHO (GRO)-interaction motif in the ENGRAILED (EN) selector protein. This "ehIFRPF" motif is not homologous to the previously characterized "engrailed homology 1" (eh1) GRO-interaction motif of EN. This second motif is an insect-specific "WRPW"-type motif that has been maintained by purifying selection in at least the dipteran/lepidopteran lineage. We demonstrate that this motif contributes to in vivo repression of the wingless (wg) target gene and to interaction with GRO in vitro. The acquisition and conservation of this auxiliary peptide motif shows how the number and activity of short peptide motifs can evolve in transcription factors while existing regulatory functions are maintained.

SUBMITTER: Hittinger CT

PROVIDER: S-EPMC2597661 | biostudies-literature | 2008 Sep-Oct

REPOSITORIES: biostudies-literature

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Evolution of an insect-specific GROUCHO-interaction motif in the ENGRAILED selector protein.

Hittinger Chris Todd CT Carroll Sean B SB

Evolution & development 20080901 5

Animal morphology evolves through alterations in the genetic regulatory networks that control development. Regulatory connections are commonly added, subtracted, or modified via mutations in cis-regulatory elements, but several cases are also known where transcription factors have gained or lost activity-modulating peptide motifs. In order to better assess the role of novel transcription factor peptide motifs in evolution, we searched for synapomorphic motifs in the homeotic selectors of Drosoph ...[more]

PMID: 18803772

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Project description:BackgroundThe Fox gene family comprises a large and functionally diverse group of forkhead-related transcriptional regulators, many of which are essential for metazoan embryogenesis and physiology. Defining conserved functional domains that mediate the transcriptional activity of Fox proteins will contribute to a comprehensive understanding of the biological function of Fox family genes.ResultsSystematic analysis of 458 protein sequences of the metazoan Fox family was performed to identify the presence of the engrailed homology-1 motif (eh1), a motif known to mediate physical interaction with transcriptional corepressors of the TLE/Groucho family. Greater than 50% of Fox proteins contain sequences with high similarity to the eh1 motif, including ten of the nineteen Fox subclasses (A, B, C, D, E, G, H, I, L, and Q) and Fox proteins of early divergent species such as marine sponge. The eh1 motif is not detected in Fox proteins of the F, J, K, M, N, O, P, R and S subclasses, or in yeast Fox proteins. The eh1-like motifs are positioned C-terminal to the winged helix DNA-binding domain in all subclasses except for FoxG proteins, which have an N-terminal motif. Two similar eh1-like motifs are found in the zebrafish FoxQ1 and in FoxG proteins of sea urchin and amphioxus. The identification of eh1-like motifs by manual sequence alignment was validated by statistical analyses of the Swiss protein database, confirming a high frequency of occurrence of eh1-like sequences in Fox family proteins. Structural predictions suggest that the majority of identified eh1-like motifs are short alpha-helices, and wheel modeling revealed an amphipathicity that supports this secondary structure prediction.ConclusionA search for eh1 Groucho interaction motifs in the Fox gene family has identified eh1-like sequences in greater than 50% of Fox proteins. The results predict a physical and functional interaction of TLE/Groucho corepressors with many members of the Fox family of transcriptional regulators. Given the functional importance of the eh1 motif in transcriptional regulation, our annotation of this motif in the Fox gene family will facilitate further study of the diverse transcriptional and regulatory roles of Fox family proteins.

Dataset Information

Evolution of an insect-specific GROUCHO-interaction motif in the ENGRAILED selector protein.

Publications

Evolution of an insect-specific GROUCHO-interaction motif in the ENGRAILED selector protein.

Similar Datasets

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