Imprinting of the Y Chromosome Influences Dosage Compensation inroX1 roX2 Drosophila melanogaster

Abstract

Drosophila melanogaster males have a well-characterized regulatory system that increases X-linked gene expression. This essential process restores the balance between X-linked and autosomal gene products in males. A complex composed of the male-specific lethal (MSL) proteins and RNA is recruited to the body of transcribed X-linked genes where it modifies chromatin to increase expression. The RNA components of this complex, roX1 and roX2 (RNA on the X1, RNA on the X2), are functionally redundant. Males mutated for both roX genes have dramatically reduced survival. We show that reversal of sex chromosome inheritance suppresses lethality in roX1 roX2 males. Genetic tests indicate that the effect on male survival depends upon the presence and source of the Y chromosome, revealing a germ line imprint that influences dosage compensation. Conventional paternal transmission of the Y chromosome enhances roX1 roX2 lethality, while maternal transmission of the Y chromosome suppresses lethality. roX1 roX2 males with both maternal and paternal Y chromosomes have very low survival, indicating dominance of the paternal imprint. In an otherwise wild-type male, the Y chromosome does not appreciably affect dosage compensation. The influence of the Y chromosome, clearly apparent in roX1 roX2 mutants, thus requires a sensitized genetic background. We believe that the Y chromosome is likely to act through modulation of a process that is defective in roX1 roX2 mutants: X chromosome recognition or chromatin modification by the MSL complex.

Satellite Repeats Identify X Chromatin for Dosage Compensation in Drosophila melanogaster Males

“…The enrichment of these motifs on the X chromosome is modest, suggesting that additional features contribute to X recognition [8]. Our prior studies led to the surprising conclusion that the siRNA pathway, and siRNA from a 1.688 X repeat, participated in X recognition [20, 21, 31]. Many of the 1.688 X repeats are transcribed and produce siRNA, making them attractive candidates for involvement in an siRNA-mediated process.…”

A Role for siRNA in X-Chromosome Dosage Compensation in Drosophila melanogaster

“…We previously reported that a maternally imprinted Y chromosome is a potent suppressor of roX1 roX2 lethality (Menon and Meller 2009). The expression of Y-linked protein-coding genes is restricted to the germline, making it unlikely that these genes influence the somatic process of dosage compensation.…”

Epigenetics and Sex-Specific Fitness: An Experimental Test Using Male-Limited Evolution in Drosophila melanogaster

“…For example, the compound X-chromosome carried by the DX females is female-limited and could accumulate son-harming genetic variation, resulting in a female-biased sex ratio or reduced fitness of sons. Some evidence for this kind of effect has been presented and interpreted as resulting from imprinting of the Y-chromosome by the X in paternal transmission [12], [36]. Unfortunately we cannot test the latter two hypotheses directly since the Affymetrix chip only contains a handful of Y-linked transcripts, too few for statistical testing, and it is unknown which genes might be associated with SA zygotic drive.…”

“…Although there has been some theoretical treatment of this issue to date [28], [29], there is relatively little empirical data on the contribution of imprinting to the resolution of intralocus sexual conflict. The fruit fly Drosophila melanogaster is known both to experience substantial intralocus sexual conflict (at least in some laboratory populations) [1], [7], [8], [30], [31] and to exhibit genomic imprinting at certain loci [32]–[36]. However the contribution of genomic imprinting to the resolution of intralocus sexual conflict has, to our knowledge, never been empirically tested.…”