Drosophila Muller F Elements Maintain a Distinct Set of Genomic Properties Over 40 Million Years of Evolution

作者：Wilson Leung, C. Shaffer, Laura K Reed, Sheryl T. Smith, William D. Barshop, William Dirkes, Matthew Dothager, Paul C. Lee, Jeannette Wong, David D. Xiong, Han Yuan, James E. J. Bedard, Joshua F Machone, Seantay D Patterson, Amber Price, Bryce A. Turner, Srebrenka Robic, Erin K Luippold, Shannon R McCartha, Tezin Walji, Chelsea A. Walker, Kenneth Saville, Marita K Abrams, Andrew Armstrong, William F. Armstrong, Robert J. Bailey, Chelsea R Barberi, Lauren Beck, Amanda L. Blaker, Christopher Blunden, Jordan Brand, Ethan J. Brock, Dana W Brooks, Marie Brown, Sarah C Butzler, Eric M. Clark, Nicole Clark, Ashley A Collins, Rebecca J Cotteleer, Peterson R Cullimore, Seth G Dawson, Carter T Docking, Sasha L Dorsett, Grace Dougherty, Kaitlyn A Downey, Andrew Drake, Erica K Earl, Trevor G Floyd, Joshua D Forsyth, Jonathan D Foust, Spencer L Franchi, James Geary, Cynthia K. Hanson, Taylor Harding, Cameron B. Harris, Jonathan M Heckman, Heather L Holderness, Nicole A Howey, Dontae A Jacobs, Elizabeth S. Jewell, Maria Kaisler, Elizabeth A Karaska, James Kehoe, Hannah C. Koaches, Jessica Koehler, Dana Koenig, Alexander J Kujawski, Jordan E Kus, Jennifer A Lammers, Rachel R. Leads, Emily C Leatherman, Rachel N. Lippert, Gregory S Messenger, Adam T Morrow, Victoria Newcomb, Haley J Plasman, Stephanie J Potocny, Michelle K Powers, Rachel M Reem, Jonathan Rennhack, Katherine R. Reynolds, Lyndsey A. Reynolds, Dong Kwon Rhee, Allyson B. Rivard, Adam J. Ronk, Meghan B Rooney, Lainey S Rubin, Luke R. Salbert, Rasleen K Saluja, Taylor Schauder, Allison R Schneiter, Robert W Schulz, Karl E. Smith, Sarah J. Spencer, Bryant R Swanson, Melissa A Tache, Ashley A Tewilliager, Amanda K. Tilot, Eve VanEck, Matthew M Villerot, Megan B Vylonis, David T. Watson, Juliana A Wurzler, Lauren M Wysocki, Monica Yalamanchili, Matthew A. Zaborowicz, Julia A. Emerson, Carlos Martínez-Ortiz, Frederic J Deuschle, Lauren A DiLorenzo, Katie L Goeller, Christopher R Macchi, Sarah E Muller, Brittany D Pasierb, Joseph E Sable, Jessica M Tucci, Marykathryn Tynon, David A. Dunbar, Levent H Beken, Alaina C Conturso, Benjamin L Danner, Gabriella A DeMichele, Justin A Gonzales, Maureen S Hammond, Colleen Kelley, Elisabeth A Kelly, Danielle Kulich, Catherine M. Mageeney, Nikie L McCabe, Alyssa M. Newman, Lindsay A Spaeder, Richard A Tumminello, Dennis Revie, Jonathon M Benson, Michael C Cristostomo, Paolo A DaSilva, Katherine S. Harker, Jenifer N Jarrell, Luis A. Jiménez, Brandon M Katz, William R. Kennedy, Kimberly S Kolibas, Mark T LeBlanc, Trung T. Nguyen, Daniel S Nicolas, Melissa D Patao, Shane M Patao, Bryan J Rupley, Bridget J Sessions, Jennifer Weaver, Anya Goodman, Erica L Alvendia, Shana M Baldassari, Ashley Brown, Ian O Chase, Maida Chen, Scott Chiang, Avery B Cromwell, Ashley F. Custer, Tia DiTommaso, Jad El-Adaimi, Nora C. Goscinski, Ryan Grove, N. A. Gutierrez, Raechel Harnoto, Heather A Hedeen, Emily L Hong, Barbara Hopkins, Vilma F Huerta, Colin Khoshabian, Kristin M LaForge, Cassidy T. Lee, Benjamin M. Lewis, Anniken Lydon, Brian Maniaci, Ryan Mitchell, Elaine V. Morlock, William Morris, Priyanka Naik, Nicole Olson, Jeannette M. Osterloh, Marcos Perez, Jonathan D Presley, Matt J Randazzo, Melanie Regan, Franca Rossi, Melanie A. Smith, Eugenia A Soliterman, Ciani J Sparks, Danny L Tran, Tiffany Wan, Anne A Welker, J. C. S. Wong, Aparna Sreenivasan, Jim Youngblom, Andrew K. Adams, Justin Alldredge, Ashley Bryant, David Carranza, Alyssa Cifelli, Kevin Coulson, Calise Debow, Noelle Delacruz, Charlene H. Emerson, Cassandra Farrar, Don Foret, Edgar Garibay, John Gooch, Michelle Heslop, Sukhjit Kaur, Ambreen Khan, Van Kim, Travis Lamb, Peter Lindbeck, G Chase Lucas, Elizabeth Macias, Daniela Martiniuc, Lissett Mayorga, Joseph Medina, Nelson Membreno, Shadi Messiah, Lacey Neufeld, San Francisco Nguyen, Zachary Nichols, George Odisho, Daymon Peterson, Laura Rodela, Priscilla Rodriguez, Vanessa Rodríguez‐Fanjul, Jorge Ruiz, Will Sherrill, Valeria Silva, Jeri Sparks, Geeta Statton, Ashley T. Townsend, Isabel Celeste Valdez, Mary Waters, Kyle Westphal, Stacey Winkler, Joannee Zumkehr, Randall J. DeJong, Arlene J. Hoogewerf, Cheri M. Ackerman, Isaac Armistead, Lara Baatenburg, Matthew J. Borr, Lindsay K Brouwer, Brandon J. Burkhart, Kelsey T. Bushhouse, Lejla Cesko, Tiffany Y Y Choi, Heather Cohen, Amanda M Damsteegt, Jess M Darusz, Cory M Dauphin, Yelena P. Davis, Emily J Diekema, Melissa Drewry, Michelle E M Eisen, Hayley M Faber, Katherine J Faber, Elizabeth Feenstra, Isabella Theresa Felzer-Kim, Brandy L Hammond, Jesse Hendriksma, Milton R Herrold, Julia A Hilbrands, Emily J Howell, Sarah A Jelgerhuis, Timothy R Jelsema, Benjamin K. Johnson, Kelly Jones, Anna Kim, Ross D Kooienga, Erika E Menyes, Eric A. Nollet, Brittany E Plescher, Lindsay Rios, Jenny L Rose, Allison Schepers, G.M. Scott, Joshua R. Smith, Allison M Sterling, Jenna C Tenney, Chris Uitvlugt, Rachel E VanDyken, Marielle VanderVennen, Samantha Vue, Nighat P. Kokan, Kwabea Agbley, Sampson K. Boham, Daniel Broomfield, Kayla Chapman, Ali Dobbe, Ian Dobbe, William F. Harrington, Marwan Ibrahem, Andre Kennedy, Chad A Koplinsky, Cassandra Kubricky, Danielle Ladzekpo, Claire Pattison, Roman E Ramirez, Lucia Wande, Sarah Woehlke, Matthew Wawersik, Elizabeth Kiernan, Jeffrey S. Thompson, Roxanne Banker, Justina R Bartling, Chinmoy I Bhatiya, Anna L. 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McDonald, Amanda Mercer, Nicholaus Monsma, Kristine Ostby, Alen Ramic, Devon Shallman, Matthew Simon, Eric Spencer, Trisha Tomkins, Pete Wendland, Anna Wylie, Michael J. Wolyniak, Gregory M Robertson, Samuel I Smith, Justin R. DiAngelo, Eric D. Sassu, Satish C. Bhalla, Karim A. Sharif, Tenzin Choeying, Jason S Macias, Fareed Sanusi, Karvyn Torchon, April E. Bednarski, Consuelo J. Alvarez, Kristen C. Davis, Carrie A Dunham, Alaina J Grantham, Amber N Hare, Jennifer Schottler, Zackary W Scott, Gary A. Kuleck, Nicole Yu, Marian Kaehler, Jacob Jipp, Paul Overvoorde, Elizabeth Shoop, Olivia Cyrankowski, Betsy Hoover, Matt J. Kusner, Devry Lin, Tijana Martinov, Jonathan Misch, Garrett A. Salzman, Holly Schiedermayer, Michael Snavely, Stephanie Zarrasola, Susan Parrish, Atlee Baker, Alissa Beckett, Carissa Belella, Julie Bryant, Turner Conrad, Adam D. Fearnow, Carolina Gomez, Robert A. Herbstsomer, Sarah E. Hirsch, Christen Johnson, Melissa K. Jones, Rita Kabaso, Eric Lemmon, Carolina Marques dos Santos Vieira, Darryl McFarland, Christopher S. McLaughlin, Abbie Morgan, Sepo Musokotwane, William Neutzling, Jana Nietmann, Christina Paluskievicz, Jessica Penn, Emily E Peoples, Caitlin Pozmanter, Emily Reed, Nichole Rigby, Lasse Schmidt, M. Shelton, Rebecca Shuford, Tiara Tirasawasdichai, Blair Undem, Damian Urick, Kayla Vondy, Bryan Yarrington, Todd T. Eckdahl, Jeffrey L. Poet, Alica B Allen, John E. Anderson, Jason Barnett, Jordan Baumgardner, Adam Brown, Jordan E Carney, Ramiro A Chavez, Shelbi Christgen, Jordan S Christie, Andrea N Clary, Michel A Conn, Kristen M Cooper, Matt J Crowley, Samuel T. Crowley, Jennifer S Doty, Brian A. Dow, Curtis Edwards, Darcie D Elder, John P. Fanning, Bridget M Janssen, Anthony K Lambright, Curtiss E Lane, Austin B Limle, Tammy Mazur, Marly R McCracken, Alexa M McDonough, Amy D Melton, Phillip J Minnick, Adam E Musick, William Henry Newhart, Joseph W Noynaert, Bradley J Ogden, Michael W Sandusky, Samantha M. Schmuecker, Anna Shipman, Anna Smith, Kristen M. Thomsen, Matthew R Unzicker, William Vernon, Wesley W Winn, Dustin Woyski, Xiao Fan Zhu, Chunguang Du, Caitlin M. Ament, Soham Aso, Laura Simone Bisogno, Jason Caronna, Nadezhda Fefelova, Lenin Lopez, Lorraine Malkowitz, Jonathan Marra, Daniella Menillo, Ifeanyi Obiorah, Eric Nyabeta Onsarigo, Shekerah Primus, Mahdi Soos, Archana Tare, Ameer Zidan, Christopher J. Jones, Todd Aronhalt, James M Bellush, Christa Burke, Steve DeFazio, Benjamin R Does, Todd D. Johnson, Nicholas Keysock, Nelson H. Knudsen, James Messler, Kevin Myirski, Jade Lea Rekai, Ryan Michael Rempe, Michael S Salgado, Erica Stagaard, Justin R Starcher, Andrew W Waggoner, Anastasia K Yemelyanova, Amy T. Hark, Anne Bertolet, Cyrus E. Kuschner, Kesley Parry, Michael Quach, Lindsey Shantzer, Mary Shaw, Mary Ann Smith, Omolara Glenn, Portia Mason, Charlotte Williams, S. Catherine Silver Key, Tyneshia C P Henry, Ashlee G Johnson, Jackie X White, Adam Haberman, Sam Asinof, Kelly Drumm, Trip Freeburg, Nadia Safa, Darrin T. Schultz, Yakov Shevin, Petros Svoronos, Tam D. Vuong, Jules Wellinghoff, Laura L. Mays Hoopes, Kim Chau, Alyssa Ward, E. Gloria C. Regisford, LaJerald Augustine, Brionna Davis-Reyes, Vivienne Echendu, Jasmine Hales, Sharon Ibarra, L. Steven Johnson, Steven Ovu, John M. Braverman, Thomas J Bahr, Nicole M. Caesar, Christopher Campana, Daniel W Cassidy, Peter A. Cognetti, Johnathan D English, Matthew C. Fadus, Cameron Fick, Philip J. Freda, Bryan M Hennessy, Kelsey Hockenberger, Jennifer K. Jones, Jessica E. King, Christopher Knob, Karen J Kraftmann, Linghui Li, Lena N. Lupey, Carl J. Minniti, Thomas F. Minton, Joseph Moran, Krishna C. Mudumbi, Elizabeth C Nordman, William J. Puetz, Lauren M. Robinson, Thomas J. Rose, Edward P Sweeney, Ashley S Timko, Don Paetkau, Heather Eisler, Megan E Aldrup, Jessica M Bodenberg, Mara Cole, Kelly M Deranek, Megan DeShetler, Rose M. Dowd, Alexandra K Eckardt, Sharon C Ehret, Jessica Fese, Amanda D. Garrett, Anna Kammrath, Michelle L Kappes, Morgan R Light, Anne C Meier, Allison O’Rouke, Mallory Perella, Kimberley D. Ramsey, Jennifer R Ramthun, Mary Reilly, Deirdre Robinett, Nadine L Rossi, Mary G. Schueler, Emma Shoemaker, Kristin M Starkey, Ashley Vetor, Abby Vrable, Vidya Chandrasekaran, Christopher W. Beck, Kristen R Hatfield, Douglas A Herrick, Christopher B. Khoury, Charlotte Lea, Christopher A Louie, Shannon M Lowell, Thomas J Reynolds, Jeanine Schibler, Alexandra H Scoma, Maxwell T Smith-Gee, Sarah Tuberty, Christopher D. 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Song, Diana Johnson, Mai Abdelnabi, Alexi Archambault, Norma Chamma, Shailly Gaur, Deborah L. Hammett, Adrese Kandahari, Guzal Khayrullina, Sonali Kumar, Samantha Lawrence, Nigel Madden, Max Mandelbaum, Heather Milnthorp, Shiv Mohini, Roshni Patel, Sarah Peacock, Emily Perling, Amber Quintana, Michael Rahimi, Kristen Aufiero Ramirez, Rishi Singhal, Corinne Weeks, Tiffany B Wong, Aubree T Gillis, Zachary Moore, Christopher D Savell, Reece Watson, Stephanie F. Mel, Arjun Andrew Anilkumar, Paul Bilinski, Rostislav Castillo, Michael Closser, Nathalia M Cruz, Tiffany Dai, Giancarlo F Garbagnati, Lanor S Horton, Dongyeon Kim, Joyce Lau, James Z Liu, Sandy D Mach, Thu A Phan, Yi Ren, Kenneth Stapleton, Jean Strelitz, Ray Sunjed, Joyce Stamm, Morgan C Anderson, Bethany Grace Bonifield, Daniel Coomes, Adam Dillman, Elaine J Durchholz, Antoinette E Fafara-Thompson, Meleah J Gross, Amber M Gygi, Lesley E. Jackson, Amy J. Johnson, Zuzana Kocsisova, Joshua Manghelli, Kylie McNeil, Michael Murillo, Kierstin L Naylor, Jessica Neely, Emmy E Ogawa, Ashley Rich, Anna Rogers, James Spencer, Kristina M. Stemler, Allison A. Throm, Matt Van Camp, Katie Weihbrecht, Timothy A. Wiles, Mallory A Williams, Matthew Williams, Kyle E Zoll, Cheryl Bailey, Leming Zhou, Darla M Balthaser, Azita Bashiri, Mindy E Bower, Kayla A Florian, Nazanin Ghavam, Elizabeth S Greiner-Sosanko, Helmet T. Karim, Victor W Mullen, Carly E Pelchen, Paul Yenerall, Jiayu Zhang, Michael R. Rubin, Suzette M. Arias‐Mejias, Armando G Bermudez-Capo, Gabriela V Bernal-Vega, Mariela Colon-Vazquez, Arelys Flores-Vazquez, Mariela Gines-Rosario, Ivan G Llavona-Cartagena, Javier O Martinez-Rodriguez, Lionel Ortiz-Fuentes, Eliezer O Perez-Colomba, Joseph Perez-Otero, Elisandra Rivera, Luke J Rodriguez-Giron, Arnaldo J Santiago-Sanabria, Andrea M Senquiz-Gonzalez, Frank R Soto delValle, Dorianmarie Vargas‐Franco, Karla I Velázquez-Soto, Joan D Zambrana-Burgos, Juan Carlos Martínez‐Cruzado, Lillyann Asencio-Zayas, Kevin Babilonia-Figueroa, Francis D. Beauchamp-Pérez, Juliana Belén-Rodríguez, Luciann Bracero-Quiñones, Andrea P Burgos-Bula, Xavier A Collado-Méndez, Luis R Colón-Cruz, Ana I Correa-Muller, Jonathan Crooke‐Rosado, José M Cruz-García, Marianna Defendini-Ávila, Francheska M Delgado-Peraza, Alex J Feliciano-Cancela, Valerie M Gónzalez-Pérez, Wilfried M. Guiblet, Aldo Heredia-Negrón, Jennifer Hernández-Muñiz, Lourdes N Irizarry-González, Ángel L Laboy-Corales, Gabriela A Llaurador-Caraballo, Frances Marín‐Maldonado, Ulises Marrero-Llerena, Héctor Martell-Martínez, Idaliz M Martínez-Traverso, Kiara N Medina-Ortega, Sonya G Méndez-Castellanos, Krizia C Menéndez-Serrano, Carol I Morales-Caraballo, Saryleine Ortiz-DeChoudens, Patricia Ortiz-Ortiz, Hendrick Pagán-Torres, Diana Pérez-Afanador, Enid M Quintana-Torres, Edwin G. Ramirez‐Aponte, Carolina Riascos, Michelle S Rivera-Llovet, Ingrid T. Rivera-Pagán, Ramón E. Rivera‐Vicéns, Fabiola Robles-Juarbe, Lorraine Rodríguez‐Bonilla, Brian O Rodríguez-Echevarría, Priscila M Rodríguez-García, Abneris E Rodríguez-Laboy, Susana Rodríguez-Santiago, Michael L Rojas-Vargas, Eva N. Rubio‐Marrero, Albeliz Santiago‐Colón, Jorge L. Santiago-Ortiz, Carlos E Santos-Ramos, Joseline Serrano-González, Alina M Tamayo-Figueroa, Edna P Tascón-Peñaranda, Jose Torres‐Castillo, Nelson A Valentín-Feliciano, Yashira M Valentín-Feliciano, Nadyan M Vargas-Barreto, Miguel Vélez-Vázquez, Luis R Vilanova-Vélez, Cristina Zambrana-Echevarría, Christy MacKinnon, Huimin Chung, Chris Kay, Anthony Pinto, Olga R. Kopp, Joshua Burkhardt, Chris Harward, Robert J. Allen, Pavan Bhat, Jimmy Hsiang-Chun Chang, York Chen, Christopher F. Chesley, Dara Cohn, David Dupuis, Michael Fasano, Nicholas Fazzio, Katherine Gavinski, Heran Gebreyesus, Thomas C. Giarla, Marcus Gostelow, Rachel Greenstein, Hashini Gunasinghe, Casey Hanson, Amanda Hay, Tao He, Katie Homa, Ruth A. Howe, Jeff Howenstein, Henry V. Huang, Aaditya Khatri, Young Lu Kim, Olivia L Knowles, Sarah Wai-Chee Kong, Rebecca M. Krock, Matt Kroll, Julia Kuhn, Matthew Kwong, Brandon Lee, Ryan Lee, Kevin M. Levine, Yedda Li, Bo Liu, Lucy Liu, Max Liu, Adam Lousararian, Jimmy Ma, Allyson P Mallya, Charlie Manchee, Joseph E Marcus, Stephen L. McDaniel, Michelle L. Miller, Jerome M. Molleston, Cristina Montero Diez, Patrick Ng, Natalie Ngai, Hien P. Nguyen, Andrew B. Nylander, Jason Pollack, Suchita Rastogi, Himabindu Reddy, Nathaniel D. Regenold, Jon Sarezky, Michael Schultz, Jien Shim, Tara Skorupa, K. Christopher Smith, Sarah J. Spencer, Priya Srikanth, Gabriel Stancu, Andrew P. Stein, Marshall Strother, Lisa Sudmeier, Mengyang Sun, Varun Sundaram, Noor Tazudeen, Alan Tseng, Albert Tzeng, Rohit Venkat, Sandeep Venkataram, Leah E Waldman, Tracy Wang, Hao Yang, Jack Y Yu, Yin Zheng, Mary L. Preuss, Angelica Garcia, Matt Juergens, Robert Morris, Alexis Nagengast, Julie Azarewicz, Thomas J. Carr, Nicole Chichearo, Mike Colgan, Megan Donegan, Bob Gardner, Nikolai Kolba, Janice L. Krumm, Stacey Lytle, Laurell MacMillian, Mary Miller, Andrew Montgomery, Alysha Moretti, Brittney Offenbacker, Mike Polen, John A. Toth, J.R. Woytanowski, Lisa Kadlec, Justin Crawford, Mary Spratt, Ashley L. Adams, Brianna K Barnard, Martin N. Cheramie, Anne M Eime, Kathryn L Golden, Allyson P Hawkins, Jessica Hill, Jessica A Kampmeier, Cody Kern, Emily E Magnuson, Ashley Miller, Cody M Morrow, Julia C Peairs, Gentry L Pickett, Sarah A Popelka, Alexis J. Scott, Emily J Teepe, Katie A TerMeer, Carmen A Watchinski, Lucas A Watson, Rachel E Weber, Kate A Woodard, Daron Barnard, Isaac Appiah, Michelle M. Giddens, Gerard P. McNeil, Adeola Adebayo, Kate Bagaeva, Justina Chinwong, Chrystel Dol, Eunice George, Kirk Haltaufderhyde, Joanna E. Haye, Manpreet Kaur, Max Semon, Dmitri Serjanov, Anika M. Toorie, Christopher Wilson, Nicole C. Riddle, Jeremy Buhler, Elaine R. Mardis, Sarah C. R. Elgin · 发表于：G3 Genes Genomes Genetics · 年份：2015 · DOI：10.1534/g3.114.015966 · 被引用次数：101 · 研究领域：Chromosomal and Genetic Variations、Genomics and Phylogenetic Studies、RNA and protein synthesis mechanisms

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 ch...