Multiple Roles of the Y Chromosome in the Biology ofDrosophila melanogaster

Abstract

The X and Y chromosomes of Drosophila melanogaster were the first examples of chromosomes associated with genetic information. Thanks to the serendipitous discovery of a male with white eyes in 1910, T.H. Morgan was able to associate the X chromosome of the fruit fly with a phenotypic character (the eye color) for the first time. A few years later, his student, C.B. Bridges, demonstrated that X0 males, although phenotypically normal, are completely sterile. This means that the X chromosome, like the autosomes, harbors genes that control several phenotypic traits, while the Y chromosome is important for male fertility only. Notwithstanding its long history – almost 100 years in terms of genetic studies – most of the features of the Y chromosome are still a mystery. This is due to the intrinsic nature of this genetic element, namely, (1) its molecular composition (mainly transposable elements and satellite DNA), (2) its genetic inertia (lack of recombination due to its heterochromatic nature), (3) the absence of homology with the X (with the only exception of the nucleolar organizer), (4) the lack of visible phenotypes when it is missing (indeed, except for their sterility, X0 flies are normal males), and (5) its low density as for protein-coding sequences (to date, only 13 genes out of approximately 14,000 have been mapped on this chromosome in D. melanogaster, i.e., ~0.1% of the total). Nonetheless, a more accurate analysis reveals that this chromosome can influence several complex phenotypes: (1) it has a role in the fertility of both sexes and viability of males when over-represented; (2) it can unbalance the intracellular nucleotide pool; (3) it can interfere with the gene expression either by recruiting proteins involved in chromatin remodeling (PEV) or, to a higher extent, by influencing the expression of up to 1,000 different genes, probably by changing the availability of transcription factors; (4) it plays a major role (up to 50%) in the resistance to heat-induced male sterility; (5) it affects the behavior; and (6) it plays a role in genetic imprinting. In the present paper, all these Y-related phenotypes are described and a potential similarity with the human Y chromosome is drawn.

The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in Drosophila

“…In contrast to the X chromosome, the Y chromosome carries a handful of protein-coding genes, which are mostly monomorphic within populations (ZUROVCOVA AND EANES 1999). Despite the lack of diversity in coding regions (CDS), the 40 MB chromosome is loaded with low-complexity DNA arrays (e.g., microsatellites) and transposable elements (DIMITRI AND PISANO 1989;CARVALHO 2002;PIERGENTILI 2010;BACHTROG 2013). These repetitive elements are variable within populations (LYCKEGAARD AND CLARK 1989) and impact gene expression diversity in males (LEMOS et al 2008;LEMOS et al 2010;SACKTON et al 2011).…”

Site‐specific transgenesis of the Drosophila melanogaster Y‐chromosome using CRISPR/Cas9

“…In short, here we describe the engineering of two Y‐chromosome marked transgenic D. melanogaster lines using site‐specific CRISPR/Cas9‐mediated insertion. This may be useful for generating, identifying and tracking progeny arising from rare meiotic nondisjunction events in a more straightforward manner than is typically used (Hess and Meyer, ; Piergentili, ; Brown and Bachtrog, ). This may also be useful for detecting in vivo mosaic Y‐chromosome loss (Szabad et al ., ), although we did not observe evidence for such loss in assayed transgenic XY or XXY individuals.…”

“…The Y‐chromosome of D. melanogaster , and of most other heteromorphic sex‐chromosome‐bearing organisms, has so far presented an elusive target for site‐specific transgenesis applications. The Y‐chromosome’s degenerative, repetitive nature renders it difficult to sequence, assemble and analyse genomically (Carvalho, ; Piergentili, ; Hall et al ., ); additionally, it is almost entirely heterochromatic (Elgin and Reuter, ), which likely makes it refractory to transgene integration and/or robust transgene expression (Bernardini et al ., ). These contributing factors have made it difficult to manipulate the Y‐chromosome in a precise fashion.…”

The Y chromosome as a regulatory element shaping immune cell transcriptomes and susceptibility to autoimmune disease

“…regulating gene expression and phenotypic differences among males (Piergentili 2010). The degree of ChrY-linked regulatory variation inversely correlates with the number of ribosomal DNA (rDNA) units within the ChrY rDNA locus, which is a tandemly repeated array consisting of hundreds of units that comprise ;10% on the entire ChrY (Paredes et al 2011;Zhou et al 2012).…”

“…Aside from its role in male development, the Drosophila ChrY differentially regulates the expression of autosomal and ChrX genes, including a preferential enrichment of genes associated with the immune response, by altering chromatin between the heterochromatic and euchromatic state, thereby influencing numerous complex phenotypes (Lemos et al 2008(Lemos et al , 2010Piergentili 2010;Paredes et al 2011). The ability of ChrY to alter chromatin dynamics and regulate gene expression is attributed to natural polymorphic variation in the multicopy ribosomal genes present on ChrY (Paredes et al 2011;Zhou et al 2012).…”