Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolution

Participating Students and Faculty of the Genomics Education Partnership

Research output: Contribution to journalArticle

41 Citations (Scopus)

Abstract

The Muller F element (4.2 Mb, ~80 protein-coding genes) is an unusual autosome of Drosophila melanogaster; it is mostly heterochromatic with a low recombination rate. To investigate how these properties impact the evolution of repeats and genes, we manually improved the sequence and annotated the genes on the D. erecta, D. mojavensis, and D. grimshawi F elements and euchromatic domains from the Muller D element. We find that F elements have greater transposon density (25-50%) than euchromatic reference regions (3-11%). Among the F elements, D. grimshawi has the lowest transposon density (particularly DINE-1: 2% vs. 11-27%). F element genes have larger coding spans, more coding exons, larger introns, and lower codon bias. Comparison of the Effective Number of Codons with the Codon Adaptation Index shows that, in contrast to the other species, codon bias in D. grimshawi F element genes can be attributed primarily to selection instead of mutational biases, suggesting that density and types of transposons affect the degree of local heterochromatin formation. F element genes have lower estimated DNA melting temperatures than D element genes, potentially facilitating transcription through heterochromatin. Most F element genes (~90%) have remained on that element, but the F element has smaller syntenic blocks than genome averages (3.4-3.6 vs. 8.4-8.8 genes per block), indicating greater rates of inversion despite lower rates of recombination.Overall, the F element has maintained characteristics that are distinct from other autosomes in the Drosophila lineage, illuminating the constraints imposed by a heterochromatic milieu.

Original languageEnglish (US)
Pages (from-to)719-740
Number of pages22
JournalG3: Genes, Genomes, Genetics
Volume5
Issue number5
DOIs
StatePublished - Jan 1 2015

Fingerprint

Drosophila
Codon
Genes
Heterochromatin
Genetic Recombination
Nucleic Acid Denaturation
Drosophila melanogaster
Introns
Exons
Genome
Temperature
Proteins

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Genetics
  • Genetics(clinical)

Cite this

Participating Students and Faculty of the Genomics Education Partnership. / Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolution. In: G3: Genes, Genomes, Genetics. 2015 ; Vol. 5, No. 5. pp. 719-740.
@article{39eadabbc78742e1b9c3bf911787a1f5,
title = "Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolution",
abstract = "The Muller F element (4.2 Mb, ~80 protein-coding genes) is an unusual autosome of Drosophila melanogaster; it is mostly heterochromatic with a low recombination rate. To investigate how these properties impact the evolution of repeats and genes, we manually improved the sequence and annotated the genes on the D. erecta, D. mojavensis, and D. grimshawi F elements and euchromatic domains from the Muller D element. We find that F elements have greater transposon density (25-50{\%}) than euchromatic reference regions (3-11{\%}). Among the F elements, D. grimshawi has the lowest transposon density (particularly DINE-1: 2{\%} vs. 11-27{\%}). F element genes have larger coding spans, more coding exons, larger introns, and lower codon bias. Comparison of the Effective Number of Codons with the Codon Adaptation Index shows that, in contrast to the other species, codon bias in D. grimshawi F element genes can be attributed primarily to selection instead of mutational biases, suggesting that density and types of transposons affect the degree of local heterochromatin formation. F element genes have lower estimated DNA melting temperatures than D element genes, potentially facilitating transcription through heterochromatin. Most F element genes (~90{\%}) have remained on that element, but the F element has smaller syntenic blocks than genome averages (3.4-3.6 vs. 8.4-8.8 genes per block), indicating greater rates of inversion despite lower rates of recombination.Overall, the F element has maintained characteristics that are distinct from other autosomes in the Drosophila lineage, illuminating the constraints imposed by a heterochromatic milieu.",
author = "{Participating Students and Faculty of the Genomics Education Partnership} and Wilson Leung and Shaffer, {Christopher D.} and Reed, {Laura K.} and Smith, {Sheryl T.} and William Barshop and William Dirkes and Matthew Dothager and Paul Lee and Jeannette Wong and David Xiong and Han Yuan and Bedard, {James E.J.} and Machone, {Joshua F.} and Patterson, {Seantay D.} and Price, {Amber L.} and Turner, {Bryce A.} and Srebrenka Robic and Luippold, {Erin K.} and McCartha, {Shannon R.} and Walji, {Tezin A.} and Walker, {Chelsea A.} and Kenneth Saville and Abrams, {Marita K.} and Armstrong, {Andrew R.} and William Armstrong and Bailey, {Robert J.} and Barberi, {Chelsea R.} and Beck, {Lauren R.} and Blaker, {Amanda L.} and Blunden, {Christopher E.} and Brand, {Jordan P.} and Brock, {Ethan J.} and Brooks, {Dana W.} and Marie Brown and Butzler, {Sarah C.} and Clark, {Eric M.} and Clark, {Nicole B.} and Collins, {Ashley A.} and Cotteleer, {Rebecca J.} and Cullimore, {Peterson R.} and Dawson, {Seth G.} and Docking, {Carter T.} and Dorsett, {Sasha L.} and Dougherty, {Grace A.} and Downey, {Kaitlyn A.} and Drake, {Andrew P.} and Earl, {Erica K.} and Floyd, {Trevor G.} and Forsyth, {Joshua D.} and Diangelo, {Justin Robert}",
year = "2015",
month = "1",
day = "1",
doi = "10.1534/g3.114.015966",
language = "English (US)",
volume = "5",
pages = "719--740",
journal = "G3: Genes, Genomes, Genetics",
issn = "2160-1836",
publisher = "Genetics Society of America",
number = "5",

}

Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolution. / Participating Students and Faculty of the Genomics Education Partnership.

In: G3: Genes, Genomes, Genetics, Vol. 5, No. 5, 01.01.2015, p. 719-740.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolution

AU - Participating Students and Faculty of the Genomics Education Partnership

AU - Leung, Wilson

AU - Shaffer, Christopher D.

AU - Reed, Laura K.

AU - Smith, Sheryl T.

AU - Barshop, William

AU - Dirkes, William

AU - Dothager, Matthew

AU - Lee, Paul

AU - Wong, Jeannette

AU - Xiong, David

AU - Yuan, Han

AU - Bedard, James E.J.

AU - Machone, Joshua F.

AU - Patterson, Seantay D.

AU - Price, Amber L.

AU - Turner, Bryce A.

AU - Robic, Srebrenka

AU - Luippold, Erin K.

AU - McCartha, Shannon R.

AU - Walji, Tezin A.

AU - Walker, Chelsea A.

AU - Saville, Kenneth

AU - Abrams, Marita K.

AU - Armstrong, Andrew R.

AU - Armstrong, William

AU - Bailey, Robert J.

AU - Barberi, Chelsea R.

AU - Beck, Lauren R.

AU - Blaker, Amanda L.

AU - Blunden, Christopher E.

AU - Brand, Jordan P.

AU - Brock, Ethan J.

AU - Brooks, Dana W.

AU - Brown, Marie

AU - Butzler, Sarah C.

AU - Clark, Eric M.

AU - Clark, Nicole B.

AU - Collins, Ashley A.

AU - Cotteleer, Rebecca J.

AU - Cullimore, Peterson R.

AU - Dawson, Seth G.

AU - Docking, Carter T.

AU - Dorsett, Sasha L.

AU - Dougherty, Grace A.

AU - Downey, Kaitlyn A.

AU - Drake, Andrew P.

AU - Earl, Erica K.

AU - Floyd, Trevor G.

AU - Forsyth, Joshua D.

AU - Diangelo, Justin Robert

PY - 2015/1/1

Y1 - 2015/1/1

N2 - The Muller F element (4.2 Mb, ~80 protein-coding genes) is an unusual autosome of Drosophila melanogaster; it is mostly heterochromatic with a low recombination rate. To investigate how these properties impact the evolution of repeats and genes, we manually improved the sequence and annotated the genes on the D. erecta, D. mojavensis, and D. grimshawi F elements and euchromatic domains from the Muller D element. We find that F elements have greater transposon density (25-50%) than euchromatic reference regions (3-11%). Among the F elements, D. grimshawi has the lowest transposon density (particularly DINE-1: 2% vs. 11-27%). F element genes have larger coding spans, more coding exons, larger introns, and lower codon bias. Comparison of the Effective Number of Codons with the Codon Adaptation Index shows that, in contrast to the other species, codon bias in D. grimshawi F element genes can be attributed primarily to selection instead of mutational biases, suggesting that density and types of transposons affect the degree of local heterochromatin formation. F element genes have lower estimated DNA melting temperatures than D element genes, potentially facilitating transcription through heterochromatin. Most F element genes (~90%) have remained on that element, but the F element has smaller syntenic blocks than genome averages (3.4-3.6 vs. 8.4-8.8 genes per block), indicating greater rates of inversion despite lower rates of recombination.Overall, the F element has maintained characteristics that are distinct from other autosomes in the Drosophila lineage, illuminating the constraints imposed by a heterochromatic milieu.

AB - The Muller F element (4.2 Mb, ~80 protein-coding genes) is an unusual autosome of Drosophila melanogaster; it is mostly heterochromatic with a low recombination rate. To investigate how these properties impact the evolution of repeats and genes, we manually improved the sequence and annotated the genes on the D. erecta, D. mojavensis, and D. grimshawi F elements and euchromatic domains from the Muller D element. We find that F elements have greater transposon density (25-50%) than euchromatic reference regions (3-11%). Among the F elements, D. grimshawi has the lowest transposon density (particularly DINE-1: 2% vs. 11-27%). F element genes have larger coding spans, more coding exons, larger introns, and lower codon bias. Comparison of the Effective Number of Codons with the Codon Adaptation Index shows that, in contrast to the other species, codon bias in D. grimshawi F element genes can be attributed primarily to selection instead of mutational biases, suggesting that density and types of transposons affect the degree of local heterochromatin formation. F element genes have lower estimated DNA melting temperatures than D element genes, potentially facilitating transcription through heterochromatin. Most F element genes (~90%) have remained on that element, but the F element has smaller syntenic blocks than genome averages (3.4-3.6 vs. 8.4-8.8 genes per block), indicating greater rates of inversion despite lower rates of recombination.Overall, the F element has maintained characteristics that are distinct from other autosomes in the Drosophila lineage, illuminating the constraints imposed by a heterochromatic milieu.

UR - http://www.scopus.com/inward/record.url?scp=84929877972&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84929877972&partnerID=8YFLogxK

U2 - 10.1534/g3.114.015966

DO - 10.1534/g3.114.015966

M3 - Article

C2 - 25740935

AN - SCOPUS:84929877972

VL - 5

SP - 719

EP - 740

JO - G3: Genes, Genomes, Genetics

JF - G3: Genes, Genomes, Genetics

SN - 2160-1836

IS - 5

ER -