Intronic AT skew is a defendable proxy for germline transcription but does not predict crossing-over or protein evolution rates in Drosophila melanogaster

Claudia C Weber, Laurence D Hurst

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Abstract

Recent evidence suggests that germline transcription may affect both protein evolutionary rates, possibly mediated by repair processes, and recombination rates, possibly mediated by chromatin and epigenetic modification. Here, we test these propositions in Drosophila melanogaster. The challenge for such analyses is to provide defendable measures of germline gene expression. Intronic AT skew is a good candidate measure as it is thought to be a consequence, at least in part, of transcription-coupled repair. Prior evidence suggests that intronic AT skew in D. melanogaster is not affected by proximity to intron extremities and differs between transcribed DNA and flanking sequence. We now also establish that intronic AT skew is a defendable proxy for germline expression as (a) it is more similar than expected by chance between introns of the same gene (which is not accounted for by physical proximity), (b) is correlated with male germline expression, and (c) is more pronounced in broadly expressed genes. Furthermore, (d) a trend for intronic skew to differ between 3' and 5' ends of genes is particular to broadly expressed genes. Finally, (e) controlling for physical distance, introns of proximate genes are most different in skew if they have different tissue specificity. We find that intronic AT skew, employed as a proxy for germline transcription, correlates neither with recombination rates nor with the rate of protein evolution. We conclude that there is no prima facie evidence that germline expression modulates recombination rates or monotonically affects protein evolution rates in D. melanogaster.
Original languageEnglish
Pages (from-to)415-426
Number of pages12
JournalJournal of Molecular Evolution
Volume71
Issue number5-6
DOIs
Publication statusPublished - Dec 2010

Fingerprint

crossing over
Proxy
Drosophila melanogaster
germ cells
transcription (genetics)
protein
Introns
gene
recombination
Genes
introns
Proteins
proteins
Genetic Recombination
genes
repair
Recombinational DNA Repair
Organ Specificity
Epigenomics
Chromatin

Keywords

  • germline expression
  • recombination
  • Drosophila melanogaster
  • intronic AT skew
  • somatic gene expression
  • tissue specificity
  • nucleotide asymmetry

Cite this

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title = "Intronic AT skew is a defendable proxy for germline transcription but does not predict crossing-over or protein evolution rates in Drosophila melanogaster",
abstract = "Recent evidence suggests that germline transcription may affect both protein evolutionary rates, possibly mediated by repair processes, and recombination rates, possibly mediated by chromatin and epigenetic modification. Here, we test these propositions in Drosophila melanogaster. The challenge for such analyses is to provide defendable measures of germline gene expression. Intronic AT skew is a good candidate measure as it is thought to be a consequence, at least in part, of transcription-coupled repair. Prior evidence suggests that intronic AT skew in D. melanogaster is not affected by proximity to intron extremities and differs between transcribed DNA and flanking sequence. We now also establish that intronic AT skew is a defendable proxy for germline expression as (a) it is more similar than expected by chance between introns of the same gene (which is not accounted for by physical proximity), (b) is correlated with male germline expression, and (c) is more pronounced in broadly expressed genes. Furthermore, (d) a trend for intronic skew to differ between 3' and 5' ends of genes is particular to broadly expressed genes. Finally, (e) controlling for physical distance, introns of proximate genes are most different in skew if they have different tissue specificity. We find that intronic AT skew, employed as a proxy for germline transcription, correlates neither with recombination rates nor with the rate of protein evolution. We conclude that there is no prima facie evidence that germline expression modulates recombination rates or monotonically affects protein evolution rates in D. melanogaster.",
keywords = "germline expression, recombination, Drosophila melanogaster, intronic AT skew, somatic gene expression, tissue specificity, nucleotide asymmetry",
author = "Weber, {Claudia C} and Hurst, {Laurence D}",
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T1 - Intronic AT skew is a defendable proxy for germline transcription but does not predict crossing-over or protein evolution rates in Drosophila melanogaster

AU - Weber, Claudia C

AU - Hurst, Laurence D

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N2 - Recent evidence suggests that germline transcription may affect both protein evolutionary rates, possibly mediated by repair processes, and recombination rates, possibly mediated by chromatin and epigenetic modification. Here, we test these propositions in Drosophila melanogaster. The challenge for such analyses is to provide defendable measures of germline gene expression. Intronic AT skew is a good candidate measure as it is thought to be a consequence, at least in part, of transcription-coupled repair. Prior evidence suggests that intronic AT skew in D. melanogaster is not affected by proximity to intron extremities and differs between transcribed DNA and flanking sequence. We now also establish that intronic AT skew is a defendable proxy for germline expression as (a) it is more similar than expected by chance between introns of the same gene (which is not accounted for by physical proximity), (b) is correlated with male germline expression, and (c) is more pronounced in broadly expressed genes. Furthermore, (d) a trend for intronic skew to differ between 3' and 5' ends of genes is particular to broadly expressed genes. Finally, (e) controlling for physical distance, introns of proximate genes are most different in skew if they have different tissue specificity. We find that intronic AT skew, employed as a proxy for germline transcription, correlates neither with recombination rates nor with the rate of protein evolution. We conclude that there is no prima facie evidence that germline expression modulates recombination rates or monotonically affects protein evolution rates in D. melanogaster.

AB - Recent evidence suggests that germline transcription may affect both protein evolutionary rates, possibly mediated by repair processes, and recombination rates, possibly mediated by chromatin and epigenetic modification. Here, we test these propositions in Drosophila melanogaster. The challenge for such analyses is to provide defendable measures of germline gene expression. Intronic AT skew is a good candidate measure as it is thought to be a consequence, at least in part, of transcription-coupled repair. Prior evidence suggests that intronic AT skew in D. melanogaster is not affected by proximity to intron extremities and differs between transcribed DNA and flanking sequence. We now also establish that intronic AT skew is a defendable proxy for germline expression as (a) it is more similar than expected by chance between introns of the same gene (which is not accounted for by physical proximity), (b) is correlated with male germline expression, and (c) is more pronounced in broadly expressed genes. Furthermore, (d) a trend for intronic skew to differ between 3' and 5' ends of genes is particular to broadly expressed genes. Finally, (e) controlling for physical distance, introns of proximate genes are most different in skew if they have different tissue specificity. We find that intronic AT skew, employed as a proxy for germline transcription, correlates neither with recombination rates nor with the rate of protein evolution. We conclude that there is no prima facie evidence that germline expression modulates recombination rates or monotonically affects protein evolution rates in D. melanogaster.

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KW - somatic gene expression

KW - tissue specificity

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