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

Abstract

Genome clustering of homeobox genes is often thought to reflect arrangements of tandem gene duplicates maintained by advantageous coordinated gene regulation. Here we analyse the chromosomal organization of the NK homeobox genes, presumed to be part of a single cluster in the Bilaterian ancestor, across 20 arthropods. We find that the ProtoNK cluster was extensively fragmented in some lineages, showing that NK clustering in Drosophila species does not reflect selectively maintained gene arrangements. More importantly, the arrangement of NK and neighbouring genes across the phylogeny supports that, in two instances within the Drosophila genus, some cluster remnants became reunited via large-scale chromosomal rearrangements. Simulated scenarios of chromosome evolution indicate that these reunion events are unlikely unless the genome neighbourhoods harbouring the participating genes tend to colocalize in the nucleus. Our results underscore how mechanisms other than tandem gene duplication can result in paralogous gene clustering during genome evolution.

Expression of NK cluster genes in the onychophoran Euperipatoides rowelli: implications for the evolution of NK family genes in nephrozoans

“…These results show that, apart from the duplication of NK6 in onychophorans (or the onychophoran subgroup containing E. rowelli ), onychophorans and tardigrades possess an identical set of eight NK cluster genes, whereas NK7 is missing in both taxa. However, the presence of NK7 in the genomes of several arthropods [Additional file 1 ; 23 , 58 ] as well as other bilaterians [Additional file 1 ; 24 , 59 ] suggests that a complete “protoNK cluster” [ 7 , 23 , 60 , 61 ] consisting of nine genes was present in the last common ancestor of Panarthropoda and that NK7 was most likely lost in the onychophoran and tardigrade lineages.…”

“…Like the Hox and ParaHox genes, the NK genes are typically arranged in one or several clusters. However, the NK cluster shows a much higher degree of rearrangement due to extensive breakup, inversion and reunion events in different taxa [ 22 , 23 ]. Based on the composition of the NK cluster in insects, combined with the information from chordates, it has been deduced that the ancestral bilaterian NK cluster comprised nine genes, namely NK1 , NK3 , NK4 , NK5 , NK6 , NK7 , Msx , Lbx and Tlx [ 7 , 21 – 24 ].…”

“…Comparative genomic analyses and gene expression studies revealed that the NK cluster genes are expressed in mesodermal derivatives across bilaterians, including the dorsal pulsatile vessel or heart, the visceral mesoderm, and various somatic muscles [ 6 , 23 , 25 – 27 ]. For example, NK4 is involved in the development of pulsatile organs in all bilaterians studied thus far [ 18 , 19 , 28 – 30 ].…”

Chromoanagenesis: a piece of the macroevolution scenario

“…The discovery of homeobox genes first in Drosophila and then in vertebrates has given rise to renewed interest in the concept of discontinuous evolution and macroevolution [47]. Phylogenic studies of the vertebrate Hox cluster and linked genes have suggested that the homeobox genes organization in malleable gene clusters occurred through processes of large-scale chromosomal rearrangements that reshape gene organization over evolutionary time [48,49].…”

Evolution of Homeobox Gene Clusters in Animals: The Giga-Cluster and Primary vs. Secondary Clustering

“…The NK cluster also presents one of the clearest examples yet of the uncertainty that we have about the dynamics and polarity of evolutionary change in homeobox gene clusters: ancient clusters breaking apart vs. dispersed genes coming together (perhaps multiple times independently such that clusters might not be homologous). A recent analysis of NK gene locations across the densely sampled drosophilids revealed that these genes can come together secondarily by multiple intrachromosomal rearrangements over relatively short evolutionary periods, i.e., within genera rather than across phyla, at least for genes that are already linked on the same chromosome (Chan et al, 2015). In contrast, the presence of NK clusters in sponges, insects and now hemichordates pushes us to assume that there was an ancestral NK cluster formed via the types of tandem duplications Many of these families are more ancient than the PDA.…”