BmLid has histone lysine demethylase activity and regulates oogenesis in the silkworm, Bombyx mori

Longhao Tang; Xiangyi Wei; Liying Zhang; Zhidan Peng; Zulian Liu; Yongping Huang; Pinhua Rao; Lili Yan; Dehong Yang

doi:10.1016/j.ibmb.2025.104359

BmLid has histone lysine demethylase activity and regulates oogenesis in the silkworm, Bombyx mori

Insect Biochem Mol Biol. 2025 Jul 9:104359. doi: 10.1016/j.ibmb.2025.104359. Online ahead of print.

Authors

Longhao Tang¹, Xiangyi Wei², Liying Zhang³, Zhidan Peng⁴, Zulian Liu², Yongping Huang², Pinhua Rao¹, Lili Yan⁵, Dehong Yang⁶

Affiliations

¹ School of Chemistry and Chemical Engineering, Shanghai University of Engineering Science, 333 Longteng Road, Shanghai, 201620, China.
² School of Environmental Science and Engineering, Shanghai Jiao Tong University, Shanghai 200240, China.
³ College of Life Science, East China Normal University, Shanghai 200062, China.
⁴ Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai 200234, China.
⁵ School of Chemistry and Chemical Engineering, Shanghai University of Engineering Science, 333 Longteng Road, Shanghai, 201620, China. Electronic address: liliyan@sues.edu.cn.
⁶ School of Environmental Science and Engineering, Shanghai Jiao Tong University, Shanghai 200240, China. Electronic address: sjtu4502685@sjtu.edu.cn.

PMID: 40645420
DOI: 10.1016/j.ibmb.2025.104359

Abstract

Lepidoptera, a major threat to global agriculture, possesses robust reproductive strategies, making understanding reproduction crucial for developing sterile insect techniques (SIT). The silkworm (Bombyx mori), a model lepidopteran, exhibits polytrophic meroistic oogenesis involving trophocyte-mediated nutrient transport and vitellogenin receptor (VgR)-dependent yolk protein uptake. However, epigenetic regulation of these processes remains unclear. This study investigates the role of BmLid, a histone demethylase, in silkworm oogenesis. Using CRISPR/Cas9, we generated BmLid knockout mutants (ΔBmLid) and confirmed gene disruption via sequencing and western blotting. ΔBmLid females exhibited developmental defects and complete sterility, despite unaffected mating behavior or sperm migration. The H3K4me2/me3 and H3K9me2/me3 levels were significantly increased in ΔBmLid ovaries, indicating BmLid has broad demethylase activity in vivo, too. Transcriptomic analysis showed significant downregulation of VgR, critical for vitellogenin transport, alongside dysregulation of cell junction and apoptosis pathways. These defects disrupted follicular epithelium integrity and yolk protein deposition, mirroring similar phenotypes observed in VgR mutants. Our findings demonstrate that BmLid regulates oogenesis by modulating histone methylation to control VgR expression, cell adhesion, and cell apoptosis, thereby ensuring vitellogenesis. This study highlights epigenetic mechanisms underlying lepidopteran reproduction and identifies BmLid as a potential target for SIT-based pest management strategies.

Keywords: BmLid; Bombyx mori; Vg transport; cell apoptosis; histone methylation; oogenesis.