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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.

SUBMITTER: Leung W 

PROVIDER: S-EPMC4426361 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Drosophila muller f elements maintain a distinct set of genomic properties over 40 million years of evolution.

Leung Wilson W   Shaffer Christopher D CD   Reed Laura K LK   Smith Sheryl T ST   Barshop William W   Dirkes William W   Dothager Matthew M   Lee Paul P   Wong Jeannette J   Xiong David D   Yuan Han H   Bedard James E J JE   Machone Joshua F JF   Patterson Seantay D SD   Price Amber L AL   Turner Bryce A BA   Robic Srebrenka S   Luippold Erin K EK   McCartha Shannon R SR   Walji Tezin A TA   Walker Chelsea A CA   Saville Kenneth K   Abrams Marita K MK   Armstrong Andrew R AR   Armstrong William W   Bailey Robert J RJ   Barberi Chelsea R CR   Beck Lauren R LR   Blaker Amanda L AL   Blunden Christopher E CE   Brand Jordan P JP   Brock Ethan J EJ   Brooks Dana W DW   Brown Marie M   Butzler Sarah C SC   Clark Eric M EM   Clark Nicole B NB   Collins Ashley A AA   Cotteleer Rebecca J RJ   Cullimore Peterson R PR   Dawson Seth G SG   Docking Carter T CT   Dorsett Sasha L SL   Dougherty Grace A GA   Downey Kaitlyn A KA   Drake Andrew P AP   Earl Erica K EK   Floyd Trevor G TG   Forsyth Joshua D JD   Foust Jonathan D JD   Franchi Spencer L SL   Geary James F JF   Hanson Cynthia K CK   Harding Taylor S TS   Harris Cameron B CB   Heckman Jonathan M JM   Holderness Heather L HL   Howey Nicole A NA   Jacobs Dontae A DA   Jewell Elizabeth S ES   Kaisler Maria M   Karaska Elizabeth A EA   Kehoe James L JL   Koaches Hannah C HC   Koehler Jessica J   Koenig Dana D   Kujawski Alexander J AJ   Kus Jordan E JE   Lammers Jennifer A JA   Leads Rachel R RR   Leatherman Emily C EC   Lippert Rachel N RN   Messenger Gregory S GS   Morrow Adam T AT   Newcomb Victoria V   Plasman Haley J HJ   Potocny Stephanie J SJ   Powers Michelle K MK   Reem Rachel M RM   Rennhack Jonathan P JP   Reynolds Katherine R KR   Reynolds Lyndsey A LA   Rhee Dong K DK   Rivard Allyson B AB   Ronk Adam J AJ   Rooney Meghan B MB   Rubin Lainey S LS   Salbert Luke R LR   Saluja Rasleen K RK   Schauder Taylor T   Schneiter Allison R AR   Schulz Robert W RW   Smith Karl E KE   Spencer Sarah S   Swanson Bryant R BR   Tache Melissa A MA   Tewilliager Ashley A AA   Tilot Amanda K AK   VanEck Eve E   Villerot Matthew M MM   Vylonis Megan B MB   Watson David T DT   Wurzler Juliana A JA   Wysocki Lauren M LM   Yalamanchili Monica M   Zaborowicz Matthew A MA   Emerson Julia A JA   Ortiz Carlos C   Deuschle Frederic J FJ   DiLorenzo Lauren A LA   Goeller Katie L KL   Macchi Christopher R CR   Muller Sarah E SE   Pasierb Brittany D BD   Sable Joseph E JE   Tucci Jessica M JM   Tynon Marykathryn M   Dunbar David A DA   Beken Levent H LH   Conturso Alaina C AC   Danner Benjamin L BL   DeMichele Gabriella A GA   Gonzales Justin A JA   Hammond Maureen S MS   Kelley Colleen V CV   Kelly Elisabeth A EA   Kulich Danielle D   Mageeney Catherine M CM   McCabe Nikie L NL   Newman Alyssa M AM   Spaeder Lindsay A LA   Tumminello Richard A RA   Revie Dennis D   Benson Jonathon M JM   Cristostomo Michael C MC   DaSilva Paolo A PA   Harker Katherine S KS   Jarrell Jenifer N JN   Jimenez Luis A LA   Katz Brandon M BM   Kennedy William R WR   Kolibas Kimberly S KS   LeBlanc Mark T MT   Nguyen Trung T TT   Nicolas Daniel S DS   Patao Melissa D MD   Patao Shane M SM   Rupley Bryan J BJ   Sessions Bridget J BJ   Weaver Jennifer A JA   Goodman Anya L AL   Alvendia Erica L EL   Baldassari Shana M SM   Brown Ashley S AS   Chase Ian O IO   Chen Maida M   Chiang Scott S   Cromwell Avery B AB   Custer Ashley F AF   DiTommaso Tia M TM   El-Adaimi Jad J   Goscinski Nora C NC   Grove Ryan A RA   Gutierrez Nestor N   Harnoto Raechel S RS   Hedeen Heather H   Hong Emily L EL   Hopkins Barbara L BL   Huerta Vilma F VF   Khoshabian Colin C   LaForge Kristin M KM   Lee Cassidy T CT   Lewis Benjamin M BM   Lydon Anniken M AM   Maniaci Brian J BJ   Mitchell Ryan D RD   Morlock Elaine V EV   Morris William M WM   Naik Priyanka P   Olson Nicole C NC   Osterloh Jeannette M JM   Perez Marcos A MA   Presley Jonathan D JD   Randazzo Matt J MJ   Regan Melanie K MK   Rossi Franca G FG   Smith Melanie A MA   Soliterman Eugenia A EA   Sparks Ciani J CJ   Tran Danny L DL   Wan Tiffany T   Welker Anne A AA   Wong Jeremy N JN   Sreenivasan Aparna A   Youngblom Jim J   Adams Andrew A   Alldredge Justin J   Bryant Ashley A   Carranza David D   Cifelli Alyssa A   Coulson Kevin K   Debow Calise C   Delacruz Noelle N   Emerson Charlene C   Farrar Cassandra C   Foret Don D   Garibay Edgar E   Gooch John J   Heslop Michelle M   Kaur Sukhjit S   Khan Ambreen A   Kim Van V   Lamb Travis T   Lindbeck Peter P   Lucas Gabi G   Macias Elizabeth E   Martiniuc Daniela D   Mayorga Lissett L   Medina Joseph J   Membreno Nelson N   Messiah Shady S   Neufeld Lacey L   Nguyen San Francisco SF   Nichols Zachary Z   Odisho George G   Peterson Daymon D   Rodela Laura L   Rodriguez Priscilla P   Rodriguez Vanessa V   Ruiz Jorge J   Sherrill Will W   Silva Valeria V   Sparks Jeri J   Statton Geeta G   Townsend Ashley A   Valdez Isabel I   Waters Mary M   Westphal Kyle K   Winkler Stacey S   Zumkehr Joannee J   DeJong Randall J RJ   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Nicole C NC   Buhler Jeremy J   Mardis Elaine R ER   Elgin Sarah C R SC  

G3 (Bethesda, Md.) 20150304 5


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 re  ...[more]

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