Nucleolar Dominance of the Y Chromosome in Drosophila melanogaster

Abstract

The rDNA genes are transcribed by RNA polymerase I to make structural RNAs for ribosomes. Hundreds of rDNA genes are typically arranged in an array that spans megabase pairs of DNA. These arrays are the major sites of transcription in growing cells, accounting for as much as 50% of RNA synthesis. The repetitive rDNA arrays are thought to use heterochromatic gene silencing as a mechanism for metabolic regulation, since repeated sequences nucleate heterochromatin formation in eukaryotes. Drosophila melanogaster carries an rDNA array on the X chromosome and on the Y chromosome, and genetic analysis has suggested that both are transcribed. However, using a chromatin-marking assay, we find that the entire X chromosome rDNA array is normally silenced in D. melanogaster males, while the Y chromosome rDNA array is dominant and expressed. This resembles "nucleolar dominance," a phenomenon that occurs in interspecific hybrids where an rDNA array from one parental species is silenced, and that from the other parent is preferentially transcribed. Interspecies nucleolar dominance is thought to result from incompatibilities between speciesspecific transcription factors and the rDNA promoters in the hybrid, but our results show that nucleolar dominance is a normal feature of rDNA regulation. Nucleolar dominance within D. melanogaster is only partially dependent on known components of heterochromatic gene silencing, implying that a distinctive chromatin regulatory system may act at rDNA genes. Finally, we isolate variant Y chromosomes that allow X chromosome array expression and suggest that the large-scale organization of rDNA arrays contribute to nucleolar dominance. This is the first example of allelic inactivation in D. melanogaster.

Dynamic Sex Chromosome Expression in Drosophila Male Germ Cells

“…The only homology between the X and Y chromosome is the rDNA clusters. Interestingly, only the Y-linked rDNAs are expressed; the X-linked cluster is inactive (69), which is consistent with the pattern we observed chromosome-wide. The probes recognizing satellite sequences of the Y chromosome showed a patchy distribution in the region separating the three main chromosome territories ( Fig.…”

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

“…However, the origin is not strictly immediate and we cannot rule out that new mutations in it might have contributed to the difference in progeny number across grandparental backgrounds. On the other hand, sex chromosomes are sensitive to parental origin in Drosophila (Golic et al, 1998;Maggert and Golic, 2002), including substantial consequences to testis-specific gene expression and epigenetic states elsewhere in the genome (Greil and Ahmad, 2012;Zhou et al, 2012;Lemos et al, 2014). Collectively, our observations raise the prospect that genetic or epigenetic variation acquired during the making of the focal males is partially responsible for modulating hybrid male sterility.…”

The Y chromosome contributes to sex-specific aging in Drosophila

“…The rDNA locus is highly transcribed, and possible collusions between the replication and transcription machinery are thought to contribute to genomic instability of the rDNA (Helmrich, et al 2013). In male Drosophila, transcription of rDNA is normally restricted to the Y chromosome (nucleolar dominance (Greil and Ahmad 2012)), and transcriptionally active Y--linked rDNA copies are preferentially lost in aging germline stem cells (Lu, et al 2018). Flies with only a single rDNA cluster (i.e.…”