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

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 three-dimensional chromatin structure. Studies in ZW-bearing species suggest that DC is absent or incomplete in most lineages except butterflies and moths, where male (ZZ) Z chromosome (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 Caenorhabditis elegans) is unclear. Using Oligopaints in the silkworm, Bombyx mori, we visualize autosomes and chZ in somatic cells from both sexes. We find that B. mori chromosomes are highly compact relative to Drosophila. 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 both male chZs are partially and equally downregulated. We also find that in the early stages of DC in females, chZ chromatin becomes more accessible and Z-linked expression increases. Concomitant with these changes, the female chZ repositions toward the nuclear center, revealing nonsequencing-based support for Ohno’s hypothesis. These studies visualizing interphase genome organization and chZ structure in Lepidoptera uncover intriguing similarities between DC in B. mori and C. elegans, despite these lineages harboring evolutionarily distinct sex chromosomes (ZW/XY), suggesting a possible role for holocentricity in DC mechanisms.