September 21, 2019  |  

Retrotransposons are the major contributors to the expansion of the Drosophila ananassae Muller F element.

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

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. Copyright © 2017 Leung et al.

Journal: G3
DOI: 10.1534/g3.117.040907
Year: 2017

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