Origin and evolution of the transcribed repeated sequences of the Y chromosome lampbrush loops of Drosophila hydei

Abstract

The molecular evolution and patterns of conservation of clones from four Y chromosome lampbrush loops of Drosophila hydei were investigated. Each loop contains a discrete family of transcribed repeats that are only slightly conserved even in the hydei subgroup species. Sequencing of clones from the four D. hydei loops indicates that all transcribed repeats evolved from A+T-rich elements of the genome. Evidence is presented that suggests a Y-specific family evolved as a result of the transposition of repeated sequences from an autosomal site to the Y chromosome with the concomitant acquisition of transcriptional activity and loss of non-Y sequences. The results support a structural role for the loops in shaping a spermatocyte-specific nuclear organization. Transcribed heterochomatic sequences could play a similar role in nuclear organization in many cell types. Analysis of cloned sequences from four different loops of D. hydei has shown that the loops consist of tandemly arranged repeated sequences. These sequences are transcribed, the transcripts varying in size from lOS to 60S. The transcripts are confined to the nuclei of primary spermatocytes and disappear, along with the loops, prior to first meiotic metaphase (refs. 5, 7; unpublished data Blot hybridizations were done according to Southern (14), and dot tests and RNA transfers as described by Thomas (15). The DNA-RNA in situ hybridization procedure (16) was detailed by Lifschytz et al. (5), and in situ hybridizations to metaphase chromosomes (17) were as described by Lifschytz and Hareven (18). All in situ hybridization experiments were conducted under the stringent conditions specified in the above references for intraspecies tests. This is especially important in light of the high A+T content of all sequences. RESULTSClones representing transcribed repeated sequences from four lampbrush loops of D. hydei (Y2ONs and Y23Ns of the two "nooses" loops, Y18CI of the "clubs" loop and Y22Tr of the "tubular ribbons" loop) were tested for homology with other species. The sequences ofD. hydei loops bear no homology to spermatocyte RNA, or male genomic DNA, of the distantly related species D. melanogaster and D. virilis or even of the closely related species D. repleta (data not shown). We therefore proceeded to the analysis of homologies with three species within the hydei subgroup. The primary spermatocytes of these species are shown in Fig. 1. They are arranged according to their phylogenetic distance from D. hydei (Fig. la), with D. neohydei (Fig. lb) being the closest, and D. bifuca (Fig. ld) the most remotely related species (19).The "clubs" clone, Y18CI, includes a 0.9-kb (EcoRIHindIII) fragment, which is transcribed, and a 1.1-kb nontranscribed fragment (Fig. 2a and unpublished data). The transcribed EcoRI-HindIII fragment is characterized by a high A+T/G+C ratio and reiteration of a 7-base consensus sequence, GATTGAT. A perfect 40-base palindrome at the beginning of the satellite-like (i.e., short repeats) section is underlined (Fig. 2b). The 1.1-kb ...

Potential genetic functions of tandem repeated DNA sequence blocks in the human genome are based on a highly conserved ?chromatin folding code?

“…The simple sequence unit (GTCT)n seems to be the basic structural element of the lampbrushloop, "tubular ribbons" (Wlaschek et al 1988). Another fertility gene associated with the lampbrush structure, "clubs", contains clusters of the (GATTGAT)n-minisatellite sequence family (Hareven et al 1986). All these simple sequence clusters are transcribed at the stage of primary spermatocyte development only in the male germ line.…”

Selection of DNA sequences from interval 6 of the human Y chromosome with homology to a Y chromosomal fertility gene sequence of Drosophila hydei

“…It may therefore be reasonable to assume that the "functional DNA structure" of a male fertility gene on the Y chromosome of the mouse or human should have conserved, at least in part, a sequence composition related to the "functional DNA structure" of Y chromosomal fertility genes of Drosophila. This molecular structure has been studied extensively in the species Drosophila hydei (Vogt et al 1982;Vogt and Hennig 1986a, b;Hareven et al 1986;Wlaschek et al 1988). The main common conclusion is that the molecular structure of these fertility genes is mainly composed of a complex locus-specific sequence organization of repetitive DNA sequences of the "satellite" or "simple sequence" type.…”

Degenerating gypsy retrotransposons in a male fertility gene on the Y chromosome of Drosophila hydei

“…However, arguments in favor of a similar structure of the loops are the similar molecular composition from repetitive DNA sequences and the rapid rate at which such sequences are substituted. Transcribed Y-specific repeats of D. hydei, such as ay 1, are present only in the closely related species D. neohydei and D. eohydei (Vogt et al 1986;Hareven et al 1986;Wlaschek et al 1988). Rally repeats, which are transcribed in the Threads" and Pseudonucleolus, are found exclusively in D. hydei (Huijser and Hennig 1987).…”