Dynamic turnover of centromeres drives karyotype evolution in Drosophila

Abstract

Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high-quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene-rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat-content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.

Near-chromosome level genome assembly of the fruit pestDrosophila suzukiiusing long-read sequencing

“…The long-read assembly presented here constitutes a clear improvement which is in line with other assemblies obtained using the long-read technology which bypasses the limitations of short-read sequencing (e.g. (Bracewell et al, 2019;Chakraborty et al, 2018;Miller et al, 2018)). Besides improving general assembly statistics, we made this assembly as workable as possible, notably for molecular biologists.…”

“…Long inversions could also be searched using methods that detect physical linkage between regions of the genome (e.g. Hi-C, (Bracewell et al, 2019;Dudchenko et al, 2017;Harewood et al, 2017)). Our results also suggest that despite the tremendous progress in sequencing technology, the complexity and diversity of genomic structures and sequences, even within an isogenized strain, might make fully chromosome-length assemblies difficult to reach for some regions in some species, and the problem worsens for wild individuals.…”

“…Genome assemblies using long read sequencing have been generated for at least 18 Drosophila species (Allen, Delaney, Kopp, & Chenoweth, n.d.;Bracewell, Chatla, Nalley, & Bachtrog, 2019;Mahajan, Wei, Nalley, Gibilisco, & Bachtrog, 2018;Miller, Staber, Zeitlinger, & Hawley, 2018).Somewhat surprisingly given its economic importance, D.…”

Topologically associating domains and their role in the evolution of genome structure and function inDrosophila

“…H igh-throughput chromatin conformation capture (Hi-C) data is used to verify the global continuity of the assembly and identified a large (~9.7 Mb) pericentromeric inversion (Supplemental Fig. S1) on the X chromosome between our assembly and previous assemblies of this species (Bracewell et al 2019;Richards et al 2005) . We annotated 13,413 gene models using supporting evidence from RNA-seq data and full length mRNA sequencing (Iso-seq) from females (22,237 isoforms) and males (15,372 isoforms) ( Supplemental Table S5 -6).…”

“…However, most of these studies are conducted in D. melanogaster . Hi-C data available for other Drosophila species are more commonly used for genome scaffolding and are too low in coverage for spatial organization analysis (Bracewell et al 2019;Mahajan et al 2018) . Thus, in-depth comparison between species is still lacking for Drosophila , while such studies are needed to reveal the evolutionary role of spatial genome organization on Drosophila genome biology.…”