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

Abstract

Dosage compensation balances the expression of sex-chromosome-linked genes with autosome-linked genes in the heterogametic sex. The silkworm (Bombyx mori), a lepidopteran model insect, uses the female heterogametic WZ sex determination system. In B. mori, a Z-linked gene, Masculinizer (Masc), is the primary determinant of maleness and dosage compensation. 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 analyzed the allele-specific expression (ASE) to solve the problem. The ASE analysis revealed that the genes located on the maternal and paternal Z chromosomes are transcriptionally upregulated in Masc knocked down males. Also, our results revealed that two Z chromosomes are transcriptionally downregulated in B. mori males as observed 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].…”

“…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]. Results also indicated that Masc-R overexpression is sufficient for the induction of dosage compensation in females, and elements necessary for dosage compensation are likely to be present in females except for Masc.…”

“…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.…”

“…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.…”

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

“…RNA-seq data and description of the dataset are available in DDBJ under accession number DRA013569. The data are provided in the electronic supplementary material [33].…”