TY - JOUR
T1 - Retrotransposons are the major contributors to the expansion of the Drosophila ananassae muller F element
AU - Participating Students and Faculty of the Genomics Education Partnership
AU - Leung, Wilson
AU - Shaffer, Christopher D.
AU - Chen, Elizabeth J.
AU - Quisenberry, Thomas J.
AU - Ko, Kevin
AU - Braverman, John M.
AU - Giarla, Thomas C.
AU - Mortimer, Nathan T.
AU - Reed, Laura K.
AU - Smith, Sheryl T.
AU - Robic, Srebrenka
AU - McCartha, Shannon R.
AU - Perry, Danielle R.
AU - Prescod, Lindsay M.
AU - Sheppard, Zenyth A.
AU - Saville, Ken J.
AU - McClish, Allison
AU - Morlock, Emily A.
AU - Sochor, Victoria R.
AU - Stanton, Brittney
AU - Veysey-White, Isaac C.
AU - Revie, Dennis
AU - Jimenez, Luis A.
AU - Palomino, Jennifer J.
AU - Patao, Melissa D.
AU - Patao, Shane M.
AU - Himelblau, Edward T.
AU - Campbell, Jaclyn D.
AU - Hertz, Alexandra L.
AU - McEvilly, Maddison F.
AU - Wagner, Allison R.
AU - Youngblom, James
AU - Bedi, Baljit
AU - Bettincourt, Jeffery
AU - Duso, Erin
AU - Her, Maiye
AU - Hilton, William
AU - House, Samantha
AU - Karimi, Masud
AU - Kumimoto, Kevin
AU - Lee, Rebekah
AU - Lopez, Darryl
AU - Odisho, George
AU - Prasad, Ricky
AU - Robbins, Holly Lyn
AU - Sandhu, Tanveer
AU - Selfridge, Tracy
AU - Tsukashima, Kara
AU - Yosif, Hani
AU - DiAngelo, Justin R.
N1 - Funding Information:
The authors would like to thank the students who worked together as a class to produce high-quality sequences and gene annotations for a given D. ananassae project. We also thank the additional students who contributed data analysis to this project, but for various reasons declined to participate in manuscript critique and revision. These students were enrolled in one of the courses listed in File S5, which includes all courses that contributed sequence improvement and annotation data to the D. ananassae project. We thank the McDonnell Genome Institute at Washington University for generating the raw sequences reported here, and for providing training and support to many of the coauthors. We thank the Genome Technology Access Center at Washington University in St. Louis for generating the D. ananassae ChIP-Seq data. This work was supported by grant #52007051 from the Howard Hughes Medical Institute (HHMI) Precollege and Undergraduate Science Education Professors Program to Washington University (to S.C.R.E.), the National Science Foundation (NSF) IUSE program under grant no. 1431407 (to S.C.R.E.), and the National Science Foundation grant MCB-1517266 (to S.C.R.E.). The support provided by the McDonnell Genome Institute was funded by grant 2U54 HG00307910 from the National Human Genome Research Institute (Richard K. Wilson, principal investigator). The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of HHMI, the NSF, the National Human Genome Research Institute, or the National Institute of General Medical Sciences.
Publisher Copyright:
© 2017 Leung et al.
PY - 2017
Y1 - 2017
N2 - 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 59 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.
AB - 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 59 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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U2 - 10.1534/g3.117.040907
DO - 10.1534/g3.117.040907
M3 - Article
C2 - 28667019
AN - SCOPUS:85027275688
VL - 7
SP - 2439
EP - 2460
JO - G3: Genes, Genomes, Genetics
JF - G3: Genes, Genomes, Genetics
SN - 2160-1836
IS - 8
ER -