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Drosophila muller f elements maintain a distinct set of genomic properties over 40 million years of evolution. G3 (Bethesda) 2015 Mar 04;5(5):719-40

Date

03/06/2015

Pubmed ID

25740935

Pubmed Central ID

PMC4426361

DOI

10.1534/g3.114.015966

Scopus ID

2-s2.0-84929877972 (requires institutional sign-in at Scopus site)   65 Citations

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 List

Leung W, Shaffer CD, Reed LK, Smith ST, Barshop W, Dirkes W, Dothager M, Lee P, Wong J, Xiong D, Yuan H, Bedard JE, Machone JF, Patterson SD, Price AL, Turner BA, Robic S, Luippold EK, McCartha SR, Walji TA, Walker CA, Saville K, Abrams MK, Armstrong AR, Armstrong W, Bailey RJ, Barberi CR, Beck LR, Blaker AL, Blunden CE, Brand JP, Brock EJ, Brooks DW, Brown M, Butzler SC, Clark EM, Clark NB, Collins AA, Cotteleer RJ, Cullimore PR, Dawson SG, Docking CT, Dorsett SL, Dougherty GA, Downey KA, Drake AP, Earl EK, Floyd TG, Forsyth JD, Foust JD, Franchi SL, Geary JF, Hanson CK, Harding TS, Harris CB, Heckman JM, Holderness HL, Howey NA, Jacobs DA, Jewell ES, Kaisler M, Karaska EA, Kehoe JL, Koaches HC, Koehler J, Koenig D, Kujawski AJ, Kus JE, Lammers JA, Leads RR, Leatherman EC, Lippert RN, Messenger GS, Morrow AT, Newcomb V, Plasman HJ, Potocny SJ, Powers MK, Reem RM, Rennhack JP, Reynolds KR, Reynolds LA, Rhee DK, Rivard AB, Ronk AJ, Rooney MB, Rubin LS, Salbert LR, Saluja RK, Schauder T, Schneiter AR, Schulz RW, Smith KE, Spencer S, Swanson BR, Tache MA, Tewilliager AA, Tilot AK, VanEck E, Villerot MM, Vylonis MB, Watson DT, Wurzler JA, Wysocki LM, Yalamanchili M, Zaborowicz MA, Emerson JA, Ortiz C, Deuschle FJ, DiLorenzo LA, Goeller KL, Macchi CR, Muller SE, Pasierb BD, Sable JE, Tucci JM, Tynon M, Dunbar DA, Beken LH, Conturso AC, Danner BL, DeMichele GA, Gonzales JA, Hammond MS, Kelley CV, Kelly EA, Kulich D, Mageeney CM, McCabe NL, Newman AM, Spaeder LA, Tumminello RA, Revie D, Benson JM, Cristostomo MC, DaSilva PA, Harker KS, Jarrell JN, Jimenez LA, Katz BM, Kennedy WR, Kolibas KS, LeBlanc MT, Nguyen TT, Nicolas DS, Patao MD, Patao SM, Rupley BJ, Sessions BJ, Weaver JA, Goodman AL, Alvendia EL, Baldassari SM, Brown AS, Chase IO, Chen M, Chiang S, Cromwell AB, Custer AF, DiTommaso TM, El-Adaimi J, Goscinski NC, Grove RA, Gutierrez N, Harnoto RS, Hedeen H, Hong EL, Hopkins BL, Huerta VF, Khoshabian C, LaForge KM, Lee CT, Lewis BM, Lydon AM, Maniaci BJ, Mitchell RD, Morlock EV, Morris WM, Naik P, Olson NC, Osterloh JM, Perez MA, Presley JD, Randazzo MJ, Regan MK, Rossi FG, Smith MA, Soliterman EA, Sparks CJ, Tran DL, Wan T, Welker AA, Wong JN, Sreenivasan A, Youngblom J, Adams A, Alldredge J, Bryant A, Carranza D, Cifelli A, Coulson K, Debow C, Delacruz N, Emerson C, Farrar C, Foret D, Garibay E, Gooch J, Heslop M, Kaur S, Khan A, Kim V, Lamb T, Lindbeck P, Lucas G, Macias E, Martiniuc D, Mayorga L, Medina J, Membreno N, Messiah S, Neufeld L, Nguyen SF, Nichols Z, Odisho G, Peterson D, Rodela L, Rodriguez P, Rodriguez V, Ruiz J, Sherrill W, Silva V, Sparks J, Statton G, Townsend A, Valdez I, Waters M, Westphal K, Winkler S, Zumkehr J, DeJong RJ, Hoogewerf AJ, Ackerman CM, Armistead IO, Baatenburg L, Borr MJ, Brouwer LK, Burkhart BJ, Bushhouse KT, Cesko L, Choi TY, Cohen H, Damsteegt AM, Darusz JM, Dauphin CM, Davis YP, Diekema EJ, Drewry M, Eisen ME, Faber HM, Faber KJ, Feenstra E, Felzer-Kim IT, Hammond BL, Hendriksma J, Herrold MR, Hilbrands JA, Howell EJ, Jelgerhuis SA, Jelsema TR, Johnson BK, Jones KK, Kim A, Kooienga RD, Menyes EE, Nollet EA, Plescher BE, Rios L, Rose JL, Schepers AJ, Scott G, Smith JR, Sterling AM, Tenney JC, Uitvlugt C, VanDyken RE, VanderVennen M, Vue S, Kokan NP, Agbley K, Boham SK, Broomfield D, Chapman K, Dobbe A, Dobbe I, Harrington W, Ibrahem M, Kennedy A, Koplinsky CA, Kubricky C, Ladzekpo D, Pattison C, Ramirez RE Jr, Wande L, Woehlke S, Wawersik M, Kiernan E, Thompson JS, Banker R, Bartling JR, Bhatiya CI, Boudoures AL, Christiansen L, Fosselman DS, French KM, Gill IS, Havill JT, Johnson JL, Keny LJ, Kerber JM, Klett BM, Kufel CN, May FJ, Mecoli JP, Merry CR, Meyer LR, Miller EG, Mullen GJ, Palozola KC, Pfeil JJ, Thomas JG, Verbofsky EM, Spana EP, Agarwalla A, Chapman J, Chlebina B, Chong I, Falk IN, Fitzgibbons JD, Friedman H, Ighile O, Kim AJ, Knouse KA, Kung F, Mammo D, Ng CL, Nikam VS, Norton D, Pham P, Polk JW, Prasad S, Rankin H, Ratliff CD, Scala V, Schwartz NU, Shuen JA, Xu A, Xu TQ, Z

Authors

Bethany Marie Klett MD Adjunct Instructor in the Pediatrics department at Medical College of Wisconsin
Saryleine Ortiz De Choudens MD Instructor in the Radiation Oncology department at Medical College of Wisconsin




MESH terms used to index this publication - Major topics in bold

Animals
Codon
Computational Biology
DNA Transposable Elements
Drosophila
Drosophila Proteins
Drosophila melanogaster
Evolution, Molecular
Exons
Gene Rearrangement
Genome
Genomics
Heterochromatin
Introns
Molecular Sequence Annotation
Polytene Chromosomes
Repetitive Sequences, Nucleic Acid
Selection, Genetic
Species Specificity