1. Drosophila muller f elements maintain a distinct set of genomic properties over 40 million years of evolution.
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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, Zhang Y, Rosenwald AG, Burg MG, Adams SJ, Baker M, Botsford B, Brinkley B, Brown C, Emiah S, Enoch E, Gier C, Greenwell A, Hoogenboom L, Matthews JE, McDonald M, Mercer A, Monsma N, Ostby K, Ramic A, Shallman D, Simon M, Spencer E, Tomkins T, Wendland P, Wylie A, Wolyniak MJ, Robertson GM, Smith SI, DiAngelo JR, Sassu ED, Bhalla SC, Sharif KA, Choeying T, Macias JS, Sanusi F, Torchon K, Bednarski AE, Alvarez CJ, Davis KC, Dunham CA, Grantham AJ, Hare AN, Schottler J, Scott ZW, Kuleck GA, Yu NS, Kaehler MM, Jipp J, Overvoorde PJ, Shoop E, Cyrankowski O, Hoover B, Kusner M, Lin D, Martinov T, Misch J, Salzman G, Schiedermayer H, Snavely M, Zarrasola S, Parrish S, Baker A, Beckett A, Belella C, Bryant J, Conrad T, Fearnow A, Gomez C, Herbstsomer RA, Hirsch S, Johnson C, Jones M, Kabaso R, Lemmon E, Vieira CM, McFarland D, McLaughlin C, Morgan A, Musokotwane S, Neutzling W, Nietmann J, Paluskievicz C, Penn J, Peoples E, Pozmanter C, Reed E, Rigby N, Schmidt L, Shelton M, Shuford R, Tirasawasdichai T, Undem B, Urick D, Vondy K, Yarrington B, Eckdahl TT, Poet JL, Allen AB, Anderson JE, Barnett JM, Baumgardner JS, Brown AD, Carney JE, Chavez RA, Christgen SL, Christie JS, Clary AN, Conn MA, Cooper KM, Crowley MJ, Crowley ST, Doty JS, Dow BA, Edwards CR, Elder DD, Fanning JP, Janssen BM, Lambright AK, Lane CE, Limle AB, Mazur T, McCracken MR, McDonough AM, Melton AD, Minnick PJ, Musick AE, Newhart WH, Noynaert JW, Ogden BJ, Sandusky MW, Schmuecker SM, Shipman AL, Smith AL, Thomsen KM, Unzicker MR, Vernon WB, Winn WW, Woyski DS, Zhu X, Du C, Ament C, Aso S, Bisogno LS, Caronna J, Fefelova N, Lopez L, Malkowitz L, Marra J, Menillo D, Obiorah I, Onsarigo EN, Primus S, Soos M, Tare A, Zidan A, Jones CJ, Aronhalt T, Bellush JM, Burke C, DeFazio S, Does BR, Johnson TD, Keysock N, Knudsen NH, Messler J, Myirski K, Rekai JL, Rempe RM, Salgado MS, Stagaard E, Starcher JR, Waggoner AW, Yemelyanova AK, Hark AT, Bertolet A, Kuschner CE, Parry K, Quach M, Shantzer L, Shaw ME, Smith MA, Glenn O, Mason P, Williams C, Key SC, Henry TC, Johnson AG, White JX, Haberman A, Asinof S, Drumm K, Freeburg T, Safa N, Schultz D, Shevin Y, Svoronos P, Vuong T, Wellinghoff J, Hoopes LL, Chau KM, Ward A, Regisford EG, Augustine L, Davis-Reyes B, Echendu V, Hales J, Ibarra S, Johnson L, Ovu S, Braverman JM, Bahr TJ, Caesar NM, Campana C, Cassidy DW, Cognetti PA, English JD, Fadus MC, Fick CN, Freda PJ, Hennessy BM, Hockenberger K, Jones JK, King JE, Knob CR, Kraftmann KJ, Li L, Lupey LN, Minniti CJ, Minton TF, Moran JV, Mudumbi K, Nordman EC, Puetz WJ, Robinson LM, Rose TJ, Sweeney EP, Timko AS, Paetkau DW, Eisler HL, Aldrup ME, Bodenberg JM, Cole MG, Deranek KM, DeShetler M, Dowd RM, Eckardt AK, Ehret SC, Fese J, Garrett AD, Kammrath A, Kappes ML, Light MR, Meier AC, O'Rouke A, Perella M, Ramsey K, Ramthun JR, Reilly MT, Robinett D, Rossi NL, Schueler MG, Shoemaker E, Starkey KM, Vetor A, Vrable A, Chandrasekaran V, Beck C, Hatfield KR, Herrick DA, Khoury CB, Lea C, Louie CA, Lowell SM, Reynolds TJ, Schibler J, Scoma AH, Smith-Gee MT, Tuberty S, Smith CD, Lopilato JE, Hauke J, Roecklein-Canfield JA, Corrielus M, Gilman H, Intriago S, Maffa A, Rauf SA, Thistle K, Trieu M, Winters J, Yang B, Hauser CR, Abusheikh T, Ashrawi Y, Benitez P, Boudreaux LR, Bourland M, Chavez M, Cruz S, Elliott G, Farek JR, Flohr S, Flores AH, Friedrichs C, Fusco Z, Goodwin Z, Helmreich E, Kiley J, Knepper JM, Langner C, Martinez M, Mendoza C, Naik M, Ochoa A, Ragland N, Raimey E, Rathore S, Reza E, Sadovsky G, Seydoux MI, Smith JE, Unruh AK, Velasquez V, Wolski MW, Gosser Y, Govind S, Clarke-Medley N, Guadron L, Lau D, Lu A, Mazzeo C, Meghdari M, Ng S, Pamnani B, Plante O, Shum YK, Song R, Johnson DE, Abdelnabi M, Archambault A, Chamma N, Gaur S, Hammett D, Kandahari A, Khayrullina G, Kumar S, Lawrence S, Madden N, Mandelbaum M, Milnthorp H, Mohini S, Patel R, Peacock SJ, Perling E, Quintana A, Rahimi M, Ramirez K, Singhal R, Weeks C, Wong T, Gillis AT, Moore ZD, Savell CD, Watson R, Mel SF, Anilkumar AA, Bilinski P, Castillo R, Closser M, Cruz NM, Dai T, Garbagnati GF, Horton LS, Kim D, Lau JH, Liu JZ, Mach SD, Phan TA, Ren Y, Stapleton KE, Strelitz JM, Sunjed R, Stamm J, Anderson MC, Bonifield BG, Coomes D, Dillman A, Durchholz EJ, Fafara-Thompson AE, Gross MJ, Gygi AM, Jackson LE, Johnson A, Kocsisova Z, Manghelli JL, McNeil K, Murillo M, Naylor KL, Neely J, Ogawa EE, Rich A, Rogers A, Spencer JD, Stemler KM, Throm AA, Van Camp M, Weihbrecht K, Wiles TA, Williams MA, Williams M, Zoll K, Bailey C, Zhou L, Balthaser DM, Bashiri A, Bower ME, Florian KA, Ghavam N, Greiner-Sosanko ES, Karim H, Mullen VW, Pelchen CE, Yenerall PM, Zhang J, Rubin MR, Arias-Mejias SM, Bermudez-Capo AG, Bernal-Vega GV, Colon-Vazquez M, Flores-Vazquez A, Gines-Rosario M, Llavona-Cartagena IG, Martinez-Rodriguez JO, Ortiz-Fuentes L, Perez-Colomba EO, Perez-Otero J, Rivera E, Rodriguez-Giron LJ, Santiago-Sanabria AJ, Senquiz-Gonzalez AM, delValle FR, Vargas-Franco D, Velázquez-Soto KI, Zambrana-Burgos JD, Martinez-Cruzado JC, Asencio-Zayas L, Babilonia-Figueroa K, Beauchamp-Pérez FD, Belén-Rodríguez J, Bracero-Quiñones L, Burgos-Bula AP, Collado-Méndez XA, Colón-Cruz LR, Correa-Muller AI, Crooke-Rosado JL, Cruz-García JM, Defendini-Ávila M, Delgado-Peraza FM, Feliciano-Cancela AJ, Gónzalez-Pérez VM, Guiblet W, Heredia-Negrón A, Hernández-Muñiz J, Irizarry-González LN, Laboy-Corales ÁL, Llaurador-Caraballo GA, Marín-Maldonado F, Marrero-Llerena U, Martell-Martínez HA, Martínez-Traverso IM, Medina-Ortega KN, Méndez-Castellanos SG, Menéndez-Serrano KC, Morales-Caraballo CI, Ortiz-DeChoudens S, Ortiz-Ortiz P, Pagán-Torres H, Pérez-Afanador D, Quintana-Torres EM, Ramírez-Aponte EG, Riascos-Cuero C, Rivera-Llovet MS, Rivera-Pagán IT, Rivera-Vicéns RE, Robles-Juarbe F, Rodríguez-Bonilla L, Rodríguez-Echevarría BO, Rodríguez-García PM, Rodríguez-Laboy AE, Rodríguez-Santiago S, Rojas-Vargas ML, Rubio-Marrero EN, Santiago-Colón A, Santiago-Ortiz JL, Santos-Ramos CE, Serrano-González J, Tamayo-Figueroa AM, Tascón-Peñaranda EP, Torres-Castillo JL, Valentín-Feliciano NA, Valentín-Feliciano YM, Vargas-Barreto NM, Vélez-Vázquez M, Vilanova-Vélez LR, Zambrana-Echevarría C, MacKinnon C, Chung HM, Kay C, Pinto A, Kopp OR, Burkhardt J, Harward C, Allen R, Bhat P, Chang JH, Chen Y, Chesley C, Cohn D, DuPuis D, Fasano M, Fazzio N, Gavinski K, Gebreyesus H, Giarla T, Gostelow M, Greenstein R, Gunasinghe H, Hanson C, Hay A, He TJ, Homa K, Howe R, Howenstein J, Huang H, Khatri A, Kim YL, Knowles O, Kong S, Krock R, Kroll M, Kuhn J, Kwong M, Lee B, Lee R, Levine K, Li Y, Liu B, Liu L, Liu M, Lousararian A, Ma J, Mallya A, Manchee C, Marcus J, McDaniel S, Miller ML, Molleston JM, Diez CM, Ng P, Ngai N, Nguyen H, Nylander A, Pollack J, Rastogi S, Reddy H, Regenold N, Sarezky J, Schultz M, Shim J, Skorupa T, Smith K, Spencer SJ, Srikanth P, Stancu G, Stein AP, Strother M, Sudmeier L, Sun M, Sundaram V, Tazudeen N, Tseng A, Tzeng A, Venkat R, Venkataram S, Waldman L, Wang T, Yang H, Yu JY, Zheng Y, Preuss ML, Garcia A, Juergens M, Morris RW, Nagengast AA, Azarewicz J, Carr TJ, Chichearo N, Colgan M, Donegan M, Gardner B, Kolba N, Krumm JL, Lytle S, MacMillian L, Miller M, Montgomery A, Moretti A, Offenbacker B, Polen M, Toth J, Woytanowski J, Kadlec L, Crawford J, Spratt ML, Adams AL, Barnard BK, Cheramie MN, Eime AM, Golden KL, Hawkins AP, Hill JE, Kampmeier JA, Kern CD, Magnuson EE, Miller AR, Morrow CM, Peairs JC, Pickett GL, Popelka SA, Scott AJ, Teepe EJ, TerMeer KA, Watchinski CA, Watson LA, Weber RE, Woodard KA, Barnard DC, Appiah I, Giddens MM, McNeil GP, Adebayo A, Bagaeva K, Chinwong J, Dol C, George E, Haltaufderhyde K, Haye J, Kaur M, Semon M, Serjanov D, Toorie A, Wilson C, Riddle NC, Buhler J, Mardis ER, and Elgin SC
- Subjects
- Animals, Codon, Computational Biology, DNA Transposable Elements, Drosophila melanogaster genetics, Exons, Gene Rearrangement, Heterochromatin, Introns, Molecular Sequence Annotation, Polytene Chromosomes, Repetitive Sequences, Nucleic Acid, Selection, Genetic, Species Specificity, Drosophila genetics, Drosophila Proteins genetics, Evolution, Molecular, Genome, Genomics
- 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., (Copyright © 2015 Leung et al.)
- Published
- 2015
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