Genome-wide gene expression effects of sex chromosome imprinting in Drosophila

Abstract

Imprinting is well-documented in both plant and animal species. In Drosophila, the Y chromosome is differently modified when transmitted through the male and female germlines. Here, we report genome-wide gene expression effects resulting from reversed parent-of-origin of the X and Y chromosomes. We found that hundreds of genes are differentially expressed between adult male Drosophila melanogaster that differ in the maternal and paternal origin of the sex chromosomes. Many of the differentially regulated genes are expressed specifically in testis and midgut cells, suggesting that sex chromosome imprinting might globally impact gene expression in these tissues. In contrast, we observed much fewer Y-linked parent-of-origin effects on genome-wide gene expression in females carrying a Y chromosome, indicating that gene expression in females is less sensitive to sex chromosome parent-of-origin. Genes whose expression differs between females inheriting a maternal or paternal Y chromosome also show sex chromosome parent-of-origin effects in males, but the direction of the effects on gene expression (overexpression or underexpression) differ between the sexes. We suggest that passage of sex chromosome chromatin through male meiosis may be required for wild-type function in F1 progeny, whereas disruption of Y-chromosome function through passage in the female germline likely arises because the chromosome is not adapted to the female germline environment.

Keywords: Drosophila; imprinting; microarray; sex chromosome.

Figure 1

Crosses used to generate individuals with reversed sex chromosome parent-of-origin inheritance. Both free and attached X and Y chromosomes were substituted into a common autosomal background (Figure S1). Only the sex chromosomes are depicted for each cross. Hundreds of individual flies of each genotype were pooled for gene expression analysis.

Figure 2

Tissue-specific expression effects of reversed parent-of-origin sex chromosome inheritance. Shown are the distributions of parent-of-origin effects for genes expressed specifically in the testes, the adult midgut, and all other genes. (A) Log2 expression differences between X_MY_P and X_PY_M males. The median fold-change of all three groups of genes is significantly different from zero (testis-specific genes = 0.24; midgut-specific genes = −0.23; all other genes = −0.03; P_MW < 0.0001 in all three cases). (B) Log2 expression differences between XY_MY_P and XY_PY_M males. The median fold-change of all three groups of genes is significantly different from zero (testis-specific genes = 0.22; midgut-specific genes = −0.36; all other genes = −0.02; P_MW < 0.0001 in all three cases).

Figure 3

Gene expression differences in X/Y males and XY/Y males with reversed sex chromosome parent-of-origin inheritance. Orange points indicate genes significantly differently expressed between both X_MY_P vs. X_PY_M and XY_MY_P vs. XY_PY_M males. The two experiments are highly significantly correlated (P < 0.0001), both for all genes (ρ = 0.68) and the set of 205 differentially expressed genes common to both the XY/Y and X/Y experiments (ρ = 0.85). Dashed line has a slope of one.

Figure 4

Expression differences in males and females for genes significantly differently expressed between females with reversed sex chromosome parent-of-origin inheritance. (A) Expression in X/Y males and XY/X females. There is a marginally significant negative correlation between gene expression effects attributable to parent-of-origin of the free X chromosome or the Y chromosome in males vs. females. (B) Expression in XY/Y males and XY/X females. There is a significant negative correlation between parent-of-origin effects attributable to the free Y chromosome in males and the attached X-Y chromosome in females. (C) Expression in X/Y and XY/Y males. There is a highly significant positive correlation attributable to parent-of-origin effects on the X chromosome or the free Y chromosome between these two male genotypes.