Schlank orchestrates insect developmental transition by switching H3K27 acetylation to trimethylation in the prothoracic gland

成果类型:
Article
署名作者:
Yuan, Dongqin; Zhang, Xing; Yang, Yan; Wei, Ling; Li, Hao; Zhao, Tujing; Guo, Mengge; Li, Zheng; Huang, Zhu; Wang, Min; Dai, Zongcai; Li, Peixin; Xia, Qingyou; Qian, Wenliang; Cheng, Daojun
署名单位:
Southwest University - China; Southwest University - China; Southwest University - China
刊物名称:
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
ISSN/ISSBN:
0027-10658
DOI:
10.1073/pnas.2401861121
发表日期:
2024-08-27
关键词:
transcriptional regulation histone modifications ecdysone ceramide schlank cbp biosynthesis demethylase repression LESSONS
摘要:
Insect developmental transitions are precisely coordinated by ecdysone and juvenile hormone (JH). We previously revealed that accumulated H3K27 trimethylation (H3K27me3) at the locus encoding JH signal transducer Hairy is involved in the larval- pupal transition in insects, but the underlying mechanism remains to be fully defined. Here, we show in Drosophila and Bombyx that Rpd3- mediated H3K27 deacetylation in the prothoracic gland during the last larval instar promotes ecdysone biosynthesis and the larval-pupal transition by enabling H3K27me3 accumulation at the Hairy locus to induce its transcriptional repression. Importantly, we find that the homeodomain transcription factor Schlank acts to switch active H3K27 acetylation (H3K27ac) to repressive H3K27me3 at the Hairy locus by directly binding to the Hairy promoter and then recruiting the histone deacetylase Rpd3 and the histone methyltransferase PRC2 component Su(z)12 through physical interactions. Moreover, Schlank inhibits Hairy transcription to facilitate the larval-pupal transition, and the Schlank signaling cascade is suppressed by JH but regulated in a positive feedback manner by ecdysone. Together, our data uncover that Schlank mediates epigenetic reprogramming of H3K27 modifications in hormone actions during insect developmental transition.