Drosophila Muller F elements maintain a distinct set of genomic properties over 40 million years of evolution

  • Leung W
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The Muller F element (4.2 Mb, ~80 protein-­‐coding genes) is an unusual autosome of 5 Drosophila melanogaster; it is mostly heterochromatic with a low recombination rate. To 6 investigate how these properties impact the evolution of repeats and genes, we manually 7 improved the sequence and annotated the genes on the D. erecta, D. mojavensis, and D. 8 grimshawi F elements and euchromatic domains from the Muller D element. We find that F 9 elements have higher transposon density (25%–50%) than euchromatic reference regions 10 (3%–11%). Among the F elements, D. grimshawi has the lowest transposon density 11 (particularly DINE-­‐1: 2% versus 11%–27%). F element genes have larger coding spans, 12 more coding exons, larger introns, and lower codon bias. Comparison of the Effective 13 Number of Codons with the Codon Adaptation Index shows that, in contrast to the other 14 species, codon bias in D. grimshawi F element genes can be attributed primarily to selection 15 instead of mutational biases, suggesting that density and types of transposons affect the 16 degree of local heterochromatin formation. F element genes have lower estimated DNA 17 melting temperatures than D element genes, potentially facilitating transcription through 18 heterochromatin. Most F element genes (~90%) have remained on that element, but the F 19 element has smaller syntenic blocks than genome averages (3.4–3.6 versus 8.4–8.8 genes 20 per block), indicating higher rates of inversion despite lower rates of recombination. 21 Overall, the F element has maintained characteristics that are distinct from other 22 autosomes in the Drosophila lineage, illuminating the constraints imposed by a 23 heterochromatic milieu. 24 INTRODUCTION 25 Classically, chromatin has been demarcated into two major types based on the staining 26 patterns in interphase nuclei. Regions that remain densely stained throughout the cell cycle 27 are classified as heterochromatin, while regions that stain weakly during interphase are 28 classified as euchromatin (HEITZ 1928). Heterochromatic regions generally are late 29 replicating, have lower rates of recombination, lower gene density, higher repeat density, 30 higher levels of histone 3 lysine 9 di-­‐ and tri-­‐methylation (H3K9me2/3) and associated 31 Heterochromatin Protein 1a (HP1a) compared to euchromatic regions (reviewed in 32 (GREWAL and ELGIN 2007)). 33 34 With an estimated size of 4.2 Mb overall, the Drosophila melanogaster Muller F element, 35 (also known as the dot chromosome, or the fourth chromosome in that species) is unusual 36 in that it appears entirely heterochromatic by most criteria, but the distal 1.3 Mb has a gene 37 density and fraction of active genes (~50% in S2 cells) that are similar to the euchromatic 38 regions of the D. melanogaster genome (RIDDLE et al. 2009, 2012). Insertion of a PEV 39 reporter (hsp70-­‐driven white) in most cases results in a variegating phenotype (partial 40 silencing; see SUPPLEMENTAL TEXT), indicating that even this distal region of the F 41 element is packaged as heterochromatin (SUN et al. 2004; RIDDLE et al. 2008; Riddle et al. 42 2009). Subsequent high-­‐resolution mapping of the chromatin landscape of the F element 43

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  • Wilson Leung

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