Molecular Evolution of Two Paralogous Tandemly Repeated Heterochromatic Gene Clusters Linked to the X and Y Chromosomes of Drosophila melanogaster

Abstract

Here we report the peculiarities of molecular evolution and divergence of paralogous heterochromatic clusters of the testis- expressed X-linked Stellate and Y-linked Su(Ste) tandem repeats. It was suggested that Stellate and Su(Ste) clusters affecting male fertility are the amplified derivatives of the unique euchromatic gene betaCK2tes encoding the putative testis-specific beta-subunit of protein kinase CK2. The putative Su(Ste)-like evolutionary intermediate was detected on the Y chromosome as an orphon outside of the Su(Ste) cluster. The orphon shows extensive homology to the Su(Ste) repeat, but contains several Stellate-like diagnostic nucleotide substitutions, as well as a 10-bp insertion and a 3' splice site of the first intron typical of the Stellate unit. The orphon looks like a pseudogene carrying a drastically damaged Su(Ste) open reading frame (ORF). The putative Su(Ste) ORF, as compared with the Stellate one, carries numerous synonymous substitutions leading to the major codon preference. We conclude that Su(Ste) ORFs evolved on the Y chromosome under the pressure of translational selection. Direct sequencing shows that the efficiency of concerted evolution between adjacent repeats is 5-10 times as high in the Stellate heterochromatic cluster on the X chromosome as that in the Y-linked Su(Ste) cluster, judging by the frequencies of nucleotide substitutions and single-nucleotide deletions.

Expansion and Evolution of the X-Linked Testis Specific Multigene Families in the melanogaster Species Subgroup

“…sechellia lineage, but have led to the formation of Stellate cluster in D. melanogaster . The similarity of the tandemly repeated ORFs of novel young Stellate genes (2,5% divergency), which may be maintained by an unknown mechanism of homogenization [24], [25], is significantly higher than the extent of similarity of the homologous more ancient CK2ßtes - like copies in D. sechellia/D. simulans (Fig.…”

Promoter contribution to the testis-specific expression of Stellate gene family in Drosophila melanogaster

“…The Stellate sequences were extensively homogenized and were maintained by natural selection (Kogan et al, 2000). To compare promoters of the examined gene clusters, we aligned their sequences and compared locations of the found E-boxes (Fig.…”

“…7, for alignments see also Usakin et al, 2005). It should be noted that whole intra-locus divergences of Stellate promoter sequences from both euchromatic and heterochromatic clusters are slightly higher, as compared with the ones of CDSs, 1.1-4.5% against 0.2%-2.5% (Kogan et al, 2000). However, all Stellate genes from both clusters contain three conserved E-boxes.…”

The Y chromosome as a target for acquired and amplified genetic material in evolution

“…(58) The Stellate and Su(Ste) clusters include tens to hundreds of copies, showing substantial sequence variations among the Su(Ste) copies. (24,59,60) The X-linked Stellate repeats and their paralogous Y-linked suppressors can be derived from a testis-expressed autosomal gene encoding a putative regulatory b-subunit required to activate the catalytic subunit of protein kinase CK2. (45,61) Specifically, both Stellate and Su(Ste) repeats appear to have been spawned as chimeric precursors carrying the coding region of an autosomal gene and an alien promoter of an Xlinked testis-expressed gene of unknown function (Fig.…”

“…(1,21) Both the Drosophila and human Y chromosomes have also been considered as newly evolved structures that are capable of acquiring genetic material from the rest of the genome. (22)(23)(24)(25) In this review, we will focus on the evidence for the Y chromosome as a target for recruited and amplified genome material. While this view of the Y chromosome evolution has been put forward previously, (22,23) we present additional arguments to support it.…”