Masculinizer-induced dosage compensation is achieved by transcriptional downregulation of both copies of Z-linked genes in the silkworm, Bombyx mori

Abstract

The evolution of dosage compensation produces similar expression of sex-linked and autosomal genes in the heterogametic sex. The silkworm ( Bombyx mori ), a lepidopteran insect, has a female heterogametic WZ sex determination system. A Z-linked gene, Masculinizer ( Masc ), is the primary determinant of maleness and dosage compensation in B. mori . However, it remains unknown whether one of the two Z chromosomes is inactivated or both Z chromosomes are suppressed in B. mori males. Hence, we performed transcriptome analysis using hybrids between two B. mori strains and analysed allele-specific expression to distinguish these alternatives. Our analysis revealed that genes on both the maternal and paternal Z chromosomes are transcriptionally upregulated in Masc knocked down males. We therefore conclude that both Z chromosomes are transcriptionally downregulated in B. mori males, similar to the system in Caenorhabditis elegans .

Transcriptome analysis in the silkworm Bombyx mori overexpressing piRNA-resistant Masculinizer gene

“…2 and 3). This finding was consistent with previous studies demonstrating the global hyperactivation of Z-linked genes in Masc knocked down males [8,10].…”

“…It The silkworm Bombyx mori, a model species of lepidopteran insects, uses a WZ sex-determination system [7]. The expression from the single Z in WZ females matches that of ZZ males because the expression of Z-linked genes is suppressed in males [8,9]. Kiuchi et al [10] reported that a Z-linked gene Masculinizer (Masc) is essential for maleness and dosage compensation.…”

“…In WZ females, Masc mRNA is cleaved by silkworm P-element induced wimpy testis (PIWI)-like protein (Siwi) complexed with W-linked Feminizer (Fem) PIWI-interacting RNA (piRNA) [10]. In Masc knocked down males, most Z-chromosome-derived transcripts are transcriptionally upregulated [8,10], showing that Masc reduces Z-linked gene expression at the embryonic stage in ZZ males.…”

Expression of the Wolbachia male‐killing factor Oscar impairs dosage compensation in lepidopteran embryos

“…As we have previously shown, the knockdown of Masc mRNA in B. mori embryos significantly increased the expression of Z-linked genes in males, but not in females (Fig. 3A) [3,13]. Similar results were observed in Oscar-expressing B. mori embryos (Fig.…”

“…Masc is a lepidopteran-specific gene that encodes a CCCHtandem zinc finger protein required for masculinization in lepidopteran insects [4][5][6][7][8][9][10][11][12]. The transcriptome analysis of Masc-knocked down embryos revealed that maternal and paternal Z-linked genes are both upregulated in Masc-knocked down males, indicating that Masc plays an essential role in dosage compensation (DC) at least during embryogenesis by suppressing both Z chromosomes transcriptionally [3,13]. These results provide evidence that Masc plays a central role in the coordination of sex determination and DC in lepidopteran insects, similarly to the Sex-lethal gene in Drosophila [14].…”