Dosage compensation in Bombyx mori is achieved by partial repression of both Z chromosomes in males

Abstract

Interphase chromatin is organized precisely to facilitate accurate gene expression. The structure-function relationship of chromatin is epitomized in sex chromosome dosage compensation (DC), where sex-linked gene expression is balanced between males and females via sex-specific alterations to 3D chromosome structure. Studies in ZW-bearing species suggest that DC is absent or incomplete in most lineages except butterflies and moths, where male (ZZ) chZ expression is reduced by half to equal females (ZW). However, whether one chZ is inactivated (as in mammals) or both are partially repressed (as in C. elegans) is unknown. Using Oligopaints in the silkworm, Bombyx mori, we visualize autosome and chZ organization in somatic cells from both sexes for the first time. We find that B. mori interphase chromosomes are highly compact relative to Drosophila chromosomes. Importantly, we show that in B. mori males, both chZs are similar in size and shape and are more compact than autosomes or the female chZ after DC establishment, suggesting that both male chZs are partially and equally downregulated. We also find that in the early stages of DC, the female chZ repositions toward the nuclear center concomitant with increased Z-linked gene expression, revealing the first non-sequencing-based support for Ohno's hypothesis. These studies represent the first visualization of interphase genome organization and chZ structure in Lepidoptera. We uncover striking similarities between DC in B. mori and C. elegans, despite these lineages harboring evolutionarily distinct sex chromosomes (ZW/XY), suggesting convergent evolution of DC mechanisms and a possible role for holocentricity in DC evolution.

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

“…Therefore, our results showed that B. mori establishes nematode-like dosage compensation, which equally suppresses both copies of the male Z chromosome. These results corroborate a recent study showing that both male Z chromosomes are similar in size and shape and more compact than either autosomes or the female Z chromosome using Oligopaint FISH [13].…”

“…Findings demonstrated that both male Z chromosomes are similar in size and shape. They were also shown to be more compact than either autosomes or the female Z chromosome [13]. Although their results suggest that both male Z chromosomes are repressed, this model is not directly confirmed by comparing the expression levels of genes on different Z chromosomes in males.…”

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

“…Recently, Rosin et al . [17] visualized B. mori chromosomes by Oligopaint fluorescence in situ hybridization, which demonstrated that both Z chromosomes in males are similar in size and shape unlike the visibly silenced X chromosome in mammals (the Barr body). As both Z chromosomes were more compact than either the autosomes or the Z chromosome in females, the results suggested that both Z chromosomes in males are repressed [17].…”

ZW sex-chromosome evolution and contagious parthenogenesis in Artemia brine shrimp

“…2014; Katsuma et al . 2019; Rosin et al . 2022), making this an outstanding new model clade for investigating these topics.…”