Chromosomal Rearrangement Inferred From Comparisons of 12 Drosophila Genomes

Abstract

The availability of 12 complete genomes of various species of genus Drosophila provides a unique opportunity to analyze genome-scale chromosomal rearrangements among a group of closely related species. This article reports on the comparison of gene order between these 12 species and on the fixed rearrangement events that disrupt gene order. Three major themes are addressed: the conservation of syntenic blocks across species, the disruption of syntenic blocks (via chromosomal inversion events) and its relationship to the phylogenetic distribution of these species, and the rate of rearrangement events over evolutionary time. Comparison of syntenic blocks across this large genomic data set confirms that genetic elements are largely (95%) localized to the same Muller element across genus Drosophila species and paracentric inversions serve as the dominant mechanism for shuffling the order of genes along a chromosome. Gene-order scrambling between species is in accordance with the estimated evolutionary distances between them and we find it to approximate a linear process over time (linear to exponential with alternate divergence time estimates). We find the distribution of synteny segment sizes to be biased by a large number of small segments with comparatively fewer large segments. Our results provide estimated chromosomal evolution rates across this set of species on the basis of whole-genome synteny analysis, which are found to be higher than those previously reported. Identification of conserved syntenic blocks across these genomes suggests a large number of conserved blocks with varying levels of embryonic expression correlation in Drosophila melanogaster. On the other hand, an analysis of the disruption of syntenic blocks between species allowed the identification of fixed inversion breakpoints and estimates of breakpoint reuse and lineage-specific breakpoint event segregation. D ROSOPHILA research has a rich history in the study of genome rearrangements that now culminates with the analysis of complete genomic sequences. Comparative genomics in Drosophila began when linkage maps of morphological traits were used to establish the homologies of six chromosomal arms in closely related species (Donald 1936;Sturtevant and Tan 1937;Muller 1940;Sturtevant and Novitski 1941). These early studies established the idea that genes are syntenic or conserved on the same chromosome arm among species. One difficulty encountered with these early comparative genomic analyses was that chromosomal arm nomenclatures varied among species (Crew and Lamy 1935;Sturtevant and Tan 1937). Muller (1940) overcame this problem when he developed a standard nomenclature that assigned a letter to each of the chromosomal arms or elements on the basis of the Drosophila melanogaster genome (chromosomal arm equals Muller element: X ¼ A, 2L ¼ B, 2R ¼ C, 3L ¼ D, 3R ¼ E, 4 ¼ F). Sturtevant and Novitski (1941) showed that the conservation of chromosomal elements extended to species across the entire genus of Drosophila.The conservation of the ...

A molecular perspective on a complex polymorphic inversion system with cytological evidence of multiply reused breakpoints

“…This coincidental occurrence of a rearrangement breakpoint in the same region in two or more species is referred to as breakpoint reuse. In Drosophila, there is both cytological and molecular evidence that the breakpoints of some fixed inversions have been used more than once through evolutionary time (for example, Tonzetich et al, 1988;Ruiz and Wasserman, 1993;Ranz et al, 2007;Bhutkar et al, 2008;von Grotthuss et al, 2010). Even at the much shorter intraspecific timescale, a similar observation of some reused breakpoints has emerged from cytological studies of chromosomal inversion polymorphism in different Drosophila species (Kunze-Mühl and Müller, 1958;Aulard et al, 2002).…”

Remodelling of a homeobox gene cluster by multiple independent gene reunions in Drosophila

“…In the lancelet, NK7, and not NK1 (slou) as in D. melanogaster, is downstream of Tlx. Evolutionary stability of the lancelet genome at the structural level compared with other deuterostome 24,25 and some protostome lineages, such as those of Diptera 26,27 , point to Tlx-NK7 as the most likely ancestral contiguity in the Bilaterian common ancestor. Further, and unlike in other reconstructions of the NK gene organization in this ancestor 13,15,23 , NK1 was inferred to be adjacent to Msx because of their proximity (B76 kb and three intervening genes) within the scaffold 186 of the D. pulex assembly (Supplementary Data 1 and 2).…”

“…Next, we tested the consistency of the extended NK clustering by examining the structurally dynamic genome of Drosophila species 26,27 . We determined which chromosomal regions with conserved local gene order, that is, microsynteny blocks, among the 2,683 delineated across nine Drosophila species 27 harbour at least one NK gene.…”

“…First, a close proximity between focal NK genes can only be maintained if the chromosomal region where they reside escapes from, or is refractory to, the chromosomal rearrangements that have reshaped the Drosophila genome. This is specially unlikely considering the thousands of paracentric inversions estimated to have occurred 26,27 , and the lack of evidence for extended functional constraints keeping most NK genes together. Second, analyses of gene neighbourhoods within and outside of the genus Drosophila show that several NK genes, including C15 and NK7.1, ananassae.…”

Two genomic regions together cause dark abdominal pigmentation in Drosophila tenebrosa

“…Pigmentation in D. tenebrosa MJ Bray et al scale conservation of most genes to Muller Elements across Drosophila (Bhutkar et al, 2008).…”