Identification of five new genes on the Y chromosome of Drosophila melanogaster

Abstract

The heterochromatic state of the Drosophila Y chromosome has made the cloning and identification of Y-linked genes a challenging process. Here, we report application of a procedure to identify Y-linked gene fragments from the unmapped residue of the whole genome sequencing effort. Previously identified Y-linked genes appear in sequenced scaffolds as individual exons, apparently because many introns have become heterochromatic, growing to enormous size and becoming virtually unclonable. A TBLASTN search using all known proteins as query sequences, tested against a blastable database of the unmapped fragments, produced a number of matches consistent with this scenario. Reverse transcription-PCR and genetic methods were used to confirm those that are expressed, Y-linked genes. The five genes reported here include three protein phosphatases (Pp1-Y1, Pp1-Y2, and PPr-Y), an occludin-related gene (ORY), and a coiled-coils gene (CCY). This brings the total to nine protein-coding genes identified on the Drosophila Y chromosome. ORY and CCY may correspond, respectively, to the fertility factors ks-1 and ks-2, whereas the three protein phosphatases represent novel genes. There remains a strong functional coherence to male function among the genes on the Drosophila Y chromosome.

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

“…The Y chromosome is required for male fertility in most Drosophila species (Ashburner et al, 2005) even though it does not contain a male-determining gene. Instead, most if not all of the~14 protein-coding genes present on the Y chromosomes of Drosophila melanogaster, D. simulans and other closely related species have male-specific functions and are exclusively expressed in the testis (Gepner and Hays, 1993;Carvalho et al, 2000;Carvalho et al, 2001;Vibranovski et al, 2008). Nevertheless, a suite of studies have shown that genetic variation present on the Y of Drosophila underlie phenotypic variation in male fitness (Chippindale and Rice, 2001;Yee et al, 2015), sex ratio distortion (Carvalho et al, 1997;Montchamp-Moreau et al, 2001;Branco et al, 2013a, b), tolerance to temperature extremes (Rohmer et al, 2004;David et al, 2005), behavior (Stoltenberg and Hirsch, 1997;Huttunen and Aspi, 2003), gene expression (Lemos et al, 2008;Sackton et al, 2011;Branco et al, 2013a, b) and chromatin states in somatic tissues .…”

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

“…(51) A new computational analysis of the D. melanogaster genome may shed light on this matter, however, it complements the data on transposition of autosomal genes into the Y chromosome. (8) Computational approaches to reveal Y chromosome genes and their autosomal counterparts Carvalho and colleagues developed a computational method to identify the genes essential for male fertility on the Drosophila Y chromosome. (8) This method involves revealing the homologs of protein-coding DNA sequences among nonrepetitive unmapped sequences in D. melanogaster.…”

“…(8) Computational approaches to reveal Y chromosome genes and their autosomal counterparts Carvalho and colleagues developed a computational method to identify the genes essential for male fertility on the Drosophila Y chromosome. (8) This method involves revealing the homologs of protein-coding DNA sequences among nonrepetitive unmapped sequences in D. melanogaster. They found Y-linked coding sequences with large introns containing repetitive sequences.…”

“…Five more Ylinked genes that have close autosomal homologs were identified, suggesting that they were acquired by transpositions from autosomes. (8) These ORFs were localized in the Y chromosomal region carrying the fertility factors. To date, Carvalho and collegues have succeeded in identifying at least 16 Y-linked genes that have no homologs on the X chromosome but which always have a clear autosomal paralog.…”

“…(3,8) The driving forces for the accumulation of the amplified genetic material in the heterochromatin of the Y chromosome have remained obscure. It has been proposed that repetitive sequences are maintained in heterochromatin due to their ability to replicate in the genome as selfish DNA.…”