Microsatellite repeat instability fuels evolution of embryonic enhancers in Hawaiian Drosophila

Andrew Brittain; Elizabeth Stroebele; Albert Erives

doi:10.1371/journal.pone.0101177

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Microsatellite repeat instability fuels evolution of embryonic enhancers in Hawaiian Drosophila

Journal article

Open access

Peer reviewed

Microsatellite repeat instability fuels evolution of embryonic enhancers in Hawaiian Drosophila

Andrew Brittain, Elizabeth Stroebele and Albert Erives

PloS one, Vol.9(6), pp.e101177-e101177

2014

DOI: 10.1371/journal.pone.0101177

PMCID: PMC4076327

PMID: 24978198

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Abstract

For ∼30 million years, the eggs of Hawaiian Drosophila were laid in ever-changing environments caused by high rates of island formation. The associated diversification of the size and developmental rate of the syncytial fly embryo would have altered morphogenic gradients, thus necessitating frequent evolutionary compensation of transcriptional responses. We investigate the consequences these radiations had on transcriptional enhancers patterning the embryo to see whether their pattern of molecular evolution is different from non-Hawaiian species. We identify and functionally assay in transgenic D. melanogaster the Neurogenic Ectoderm Enhancers from two different Hawaiian Drosophila groups: (i) the picture wing group, and (ii) the modified mouthparts group. We find that the binding sites in this set of well-characterized enhancers are footprinted by diverse microsatellite repeat (MSR) sequences. We further show that Hawaiian embryonic enhancers in general are enriched in MSR relative to both Hawaiian non-embryonic enhancers and non-Hawaiian embryonic enhancers. We propose embryonic enhancers are sensitive to Activator spacing because they often serve as assembly scaffolds for the aggregation of transcription factor activator complexes. Furthermore, as most indels are produced by microsatellite repeat slippage, enhancers from Hawaiian Drosophila lineages, which experience dynamic evolutionary pressures, would become grossly enriched in MSR content.

Conserved Sequence - genetics

Drosophila melanogaster - embryology

Microsatellite Instability

Nucleotide Motifs - genetics

Embryo, Nonmammalian - metabolism

Hawaii

Molecular Sequence Data

DNA, Intergenic - genetics

Drosophila melanogaster - genetics

Microsatellite Repeats - genetics

Neurogenesis - genetics

Ectoderm - metabolism

Animals

Enhancer Elements, Genetic

Base Sequence

Body Patterning - genetics

Evolution, Molecular

Details

Title: Subtitle: Microsatellite repeat instability fuels evolution of embryonic enhancers in Hawaiian Drosophila
Creators: Andrew Brittain - Department of Biology, University of Iowa, Iowa City, Iowa, United States of America
Elizabeth Stroebele - Department of Biology, University of Iowa, Iowa City, Iowa, United States of America
Albert Erives - Department of Biology, University of Iowa, Iowa City, Iowa, United States of America
Resource Type: Journal article
Publication Details: PloS one, Vol.9(6), pp.e101177-e101177
DOI: 10.1371/journal.pone.0101177
PMID: 24978198
PMCID: PMC4076327
NLM abbreviation: PLoS One
ISSN: 1932-6203
eISSN: 1932-6203
Publisher: United States
Grant note: T32GM082729 / NIGMS NIH HHS
Language: English
Date published: 2014
Academic Unit: Biology
Record Identifier: 9983991997302771

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7 Times Cited - Web of Science