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


ABSTRACT: 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.

SUBMITTER: Leung W 

PROVIDER: S-EPMC5555453 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Retrotransposons Are the Major Contributors to the Expansion of the <i>Drosophila ananassae</i> Muller F Element.

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

G3 (Bethesda, Md.) 20170807 8


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 <i>Drosophila melanogaster</i>, but it is substantially larger (>18.7 Mb) in <i>D. ananassae</i> 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 <i>D. ananassae</i> F element, and  ...[more]

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