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

Abstract

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 characteristics that are distinct from other autosomes in the Drosophila lineage, illuminating the constraints imposed by a heterochromatic milieu.

DOI: 10.1534/g3.114.015966

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@inproceedings{Leung2015DrosophilaMF, title={Drosophila Muller F Elements Maintain a Distinct Set of Genomic Properties Over 40 Million Years of Evolution}, author={Wilson Ho Yin Leung and C. David Shaffer and Laura K Reed and Sheryl T. Smith and William D. Barshop and William Dirkes and Matthew Dothager and Paul F. Lee and Jeannette Wong and David D. Xiong and Han Yuan and James E. J. Bedard and Joshua F. Machone and Seantay D. Patterson and Amber L. Price and Bryce A. Turner and Srebrenka Robic and Erin K. Luippold and Shannon R. McCartha and Tezin A. Walji and Chelsea A. Walker and Kenneth J. Saville and Marita K. Abrams and Andrew R. Armstrong and William O. Armstrong and Robert J. Bailey and Chelsea R. Barberi and Lauren R. Beck and Amanda L. Blaker and Christopher E. Blunden and Jordan P. Brand and Ethan J. Brock and Dana W. Brooks and Marie Brown and Sarah C. Butzler and Eric M. Clark and Nicole B. Clark and Ashley A. Collins and Rebecca J. Cotteleer and Peterson R. 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Fitzgibbons and Harrison Friedman and Osagie Ighile and Andrew J. Kim and Kristin A Knouse and Faith Kung and Danny A. Mammo and Chun Leung Ng and Vinayak S. Nikam and Diana Norton and Philip Pham and Jessica W. Polk and Shreya Prasad and Helen Rankin and Camille D. Ratliff and Victoria Scala and Nicholas U. Schwartz and Jessica A. Shuen and Amy Z Xu and Thomas Q. Xu and Yi Zhang and Anne G. Rosenwald and Martin G. Burg and Stephanie J. Adams and Morgan Baker and Bobbi Botsford and Briana Brinkley and Carter Brown and Shadie Emiah and Erica Enoch and Chad Gier and Alyson Greenwell and Lindsay Hoogenboom and Jordan E. Matthews and Mitchell J. McDonald and Amanda Mercer and Nicholaus Monsma and Kristine Ostby and Alen Ramic and Devon Shallman and Matthew L Simon and Eric Spencer and Trisha Tomkins and Pete Wendland and Anna Wylie and Michael J. Wolyniak and Gregory M. Robertson and Samuel I. Smith and Justin R Diangelo and Eric D. Sassu and Satish C. Bhalla and Karim A. 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