G3: Genes, Genomes, Genetics (Aug 2017)

Retrotransposons Are the Major Contributors to the Expansion of the Drosophila ananassae Muller F Element

  • Wilson Leung,
  • Christopher D. Shaffer,
  • Elizabeth J. Chen,
  • Thomas J. Quisenberry,
  • Kevin Ko,
  • John M. Braverman,
  • Thomas C. Giarla,
  • Nathan T. Mortimer,
  • Laura K. Reed,
  • Sheryl T. Smith,
  • Srebrenka Robic,
  • Shannon R. McCartha,
  • Danielle R. Perry,
  • Lindsay M. Prescod,
  • Zenyth A. Sheppard,
  • Ken J. Saville,
  • Allison McClish,
  • Emily A. Morlock,
  • Victoria R. Sochor,
  • Brittney Stanton,
  • Isaac C. Veysey-White,
  • Dennis Revie,
  • Luis A. Jimenez,
  • Jennifer J. Palomino,
  • Melissa D. Patao,
  • Shane M. Patao,
  • Edward T. Himelblau,
  • Jaclyn D. Campbell,
  • Alexandra L. Hertz,
  • Maddison F. McEvilly,
  • Allison R. Wagner,
  • James Youngblom,
  • Baljit Bedi,
  • Jeffery Bettincourt,
  • Erin Duso,
  • Maiye Her,
  • William Hilton,
  • Samantha House,
  • Masud Karimi,
  • Kevin Kumimoto,
  • Rebekah Lee,
  • Darryl Lopez,
  • George Odisho,
  • Ricky Prasad,
  • Holly Lyn Robbins,
  • Tanveer Sandhu,
  • Tracy Selfridge,
  • Kara Tsukashima,
  • Hani Yosif,
  • Nighat P. Kokan,
  • Latia Britt,
  • Alycia Zoellner,
  • Eric P. Spana,
  • Ben T. Chlebina,
  • Insun Chong,
  • Harrison Friedman,
  • Danny A. Mammo,
  • Chun L. Ng,
  • Vinayak S. Nikam,
  • Nicholas U. Schwartz,
  • Thomas Q. Xu,
  • Martin G. Burg,
  • Spencer M. Batten,
  • Lindsay M. Corbeill,
  • Erica Enoch,
  • Jesse J. Ensign,
  • Mary E. Franks,
  • Breanna Haiker,
  • Judith A. Ingles,
  • Lyndsay D. Kirkland,
  • Joshua M. Lorenz-Guertin,
  • Jordan Matthews,
  • Cody M. Mittig,
  • Nicholaus Monsma,
  • Katherine J. Olson,
  • Guillermo Perez-Aragon,
  • Alen Ramic,
  • Jordan R. Ramirez,
  • Christopher Scheiber,
  • Patrick A. Schneider,
  • Devon E. Schultz,
  • Matthew Simon,
  • Eric Spencer,
  • Adam C. Wernette,
  • Maxine E. Wykle,
  • Elizabeth Zavala-Arellano,
  • Mitchell J. McDonald,
  • Kristine Ostby,
  • Peter Wendland,
  • Justin R. DiAngelo,
  • Alexis M. Ceasrine,
  • Amanda H. Cox,
  • James E.B. Docherty,
  • Robert M. Gingras,
  • Stephanie M. Grieb,
  • Michael J. Pavia,
  • Casey L. Personius,
  • Grzegorz L. Polak,
  • Dale L. Beach,
  • Heaven L. Cerritos,
  • Edward A. Horansky,
  • Karim A. Sharif,
  • Ryan Moran,
  • Susan Parrish,
  • Kirsten Bickford,
  • Jennifer Bland,
  • Juliana Broussard,
  • Kerry Campbell,
  • Katelynn E. Deibel,
  • Richard Forka,
  • Monika C. Lemke,
  • Marlee B. Nelson,
  • Catherine O'Keeffe,
  • S. Mariel Ramey,
  • Luke Schmidt,
  • Paola Villegas,
  • Christopher J. Jones,
  • Stephanie L. Christ,
  • Sami Mamari,
  • Adam S. Rinaldi,
  • Ghazal Stity,
  • Amy T. Hark,
  • Mark Scheuerman,
  • S. Catherine Silver Key,
  • Briana D. McRae,
  • Adam S. Haberman,
  • Sam Asinof,
  • Harriette Carrington,
  • Kelly Drumm,
  • Terrance Embry,
  • Richard McGuire,
  • Drew Miller-Foreman,
  • Stella Rosen,
  • Nadia Safa,
  • Darrin Schultz,
  • Matt Segal,
  • Yakov Shevin,
  • Petros Svoronos,
  • Tam Vuong,
  • Gary Skuse,
  • Don W. Paetkau,
  • Rachael K. Bridgman,
  • Charlotte M. Brown,
  • Alicia R. Carroll,
  • Francesca M. Gifford,
  • Julie Beth Gillespie,
  • Susan E. Herman,
  • Krystal L. Holtcamp,
  • Misha A. Host,
  • Gabrielle Hussey,
  • Danielle M. Kramer,
  • Joan Q. Lawrence,
  • Madeline M. Martin,
  • Ellen N. Niemiec,
  • Ashleigh P. O'Reilly,
  • Olivia A. Pahl,
  • Guadalupe Quintana,
  • Elizabeth A.S. Rettie,
  • Torie L. Richardson,
  • Arianne E. Rodriguez,
  • Mona O. Rodriguez,
  • Laura Schiraldi,
  • Joanna J. Smith,
  • Kelsey F. Sugrue,
  • Lindsey J. Suriano,
  • Kaitlyn E. Takach,
  • Arielle M. Vasquez,
  • Ximena Velez,
  • Elizabeth J. Villafuerte,
  • Laura T. Vives,
  • Victoria R. Zellmer,
  • Jeanette Hauke,
  • Charles R. Hauser,
  • Karolyn Barker,
  • Laurie Cannon,
  • Perouza Parsamian,
  • Samantha Parsons,
  • Zachariah Wichman,
  • Christopher W. Bazinet,
  • Diana E. Johnson,
  • Abubakarr Bangura,
  • Jordan A. Black,
  • Victoria Chevee,
  • Sarah A. Einsteen,
  • Sarah K. Hilton,
  • Max Kollmer,
  • Rahul Nadendla,
  • Joyce Stamm,
  • Antoinette E. Fafara-Thompson,
  • Amber M. Gygi,
  • Emmy E. Ogawa,
  • Matt Van Camp,
  • Zuzana Kocsisova,
  • Judith L. Leatherman,
  • Cassie M. Modahl,
  • Michael R. Rubin,
  • Susana S. Apiz-Saab,
  • Suzette M. Arias-Mejias,
  • Carlos F. Carrion-Ortiz,
  • Patricia N. Claudio-Vazquez,
  • Debbie M. Espada-Green,
  • Marium Feliciano-Camacho,
  • Karina M. Gonzalez-Bonilla,
  • Mariela Taboas-Arroyo,
  • Dorianmarie Vargas-Franco,
  • Raquel Montañez-Gonzalez,
  • Joseph Perez-Otero,
  • Myrielis Rivera-Burgos,
  • Francisco J. Rivera-Rosario,
  • Heather L. Eisler,
  • Jackie Alexander,
  • Samatha K. Begley,
  • Deana Gabbard,
  • Robert J. Allen,
  • Wint Yan Aung,
  • William D. Barshop,
  • Amanda Boozalis,
  • Vanessa P. Chu,
  • Jeremy S. Davis,
  • Ryan N. Duggal,
  • Robert Franklin,
  • Katherine Gavinski,
  • Heran Gebreyesus,
  • Henry Z. Gong,
  • Rachel A. Greenstein,
  • Averill D. Guo,
  • Casey Hanson,
  • Kaitlin E. Homa,
  • Simon C. Hsu,
  • Yi Huang,
  • Lucy Huo,
  • Sarah Jacobs,
  • Sasha Jia,
  • Kyle L. Jung,
  • Sarah Wai-Chee Kong,
  • Matthew R. Kroll,
  • Brandon M. Lee,
  • Paul F. Lee,
  • Kevin M. Levine,
  • Amy S. Li,
  • Chengyu Liu,
  • Max Mian Liu,
  • Adam P. Lousararian,
  • Peter B. Lowery,
  • Allyson P. Mallya,
  • Joseph E. Marcus,
  • Patrick C. Ng,
  • Hien P. Nguyen,
  • Ruchik Patel,
  • Hashini Precht,
  • Suchita Rastogi,
  • Jonathan M. Sarezky,
  • Adam Schefkind,
  • Michael B. Schultz,
  • Delia Shen,
  • Tara Skorupa,
  • Nicholas C. Spies,
  • Gabriel Stancu,
  • Hiu Man Vivian Tsang,
  • Alice L. Turski,
  • Rohit Venkat,
  • Leah E. Waldman,
  • Kaidi Wang,
  • Tracy Wang,
  • Jeffrey W. Wei,
  • Dennis Y. Wu,
  • David D. Xiong,
  • Jack Yu,
  • Karen Zhou,
  • Gerard P. McNeil,
  • Robert W. Fernandez,
  • Patrick Gomez Menzies,
  • Tingting Gu,
  • Jeremy Buhler,
  • Elaine R. Mardis,
  • Sarah C.R. Elgin

DOI
https://doi.org/10.1534/g3.117.040907
Journal volume & issue
Vol. 7, no. 8
pp. 2439 – 2460

Abstract

Read online

The discordance between genome size and the complexity of eukaryotes can partly be attributed to differences in repeat density. The Muller F element (∼5.2 Mb) is the smallest chromosome in Drosophila melanogaster, but it is substantially larger (>18.7 Mb) in D. ananassae. To identify the major contributors to the expansion of the F element and to assess their impact, we improved the genome sequence and annotated the genes in a 1.4-Mb region of the D. ananassae F element, and a 1.7-Mb region from the D element for comparison. We find that transposons (particularly LTR and LINE retrotransposons) are major contributors to this expansion (78.6%), while Wolbachia sequences integrated into the D. ananassae genome are minor contributors (0.02%). Both D. melanogaster and D. ananassae F-element genes exhibit distinct characteristics compared to D-element genes (e.g., larger coding spans, larger introns, more coding exons, and lower codon bias), but these differences are exaggerated in D. ananassae. Compared to D. melanogaster, the codon bias observed in D. ananassae F-element genes can primarily be attributed to mutational biases instead of selection. The 5′ ends of F-element genes in both species are enriched in dimethylation of lysine 4 on histone 3 (H3K4me2), while the coding spans are enriched in H3K9me2. Despite differences in repeat density and gene characteristics, D. ananassae F-element genes show a similar range of expression levels compared to genes in euchromatic domains. This study improves our understanding of how transposons can affect genome size and how genes can function within highly repetitive domains.

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