RRC ID 67942
Author Yang Y, Zhao T, Li Z, Qian W, Peng J, Wei L, Yuan D, Li Y, Xia Q, Cheng D.
Title Histone H3K27 methylation-mediated repression of Hairy regulates insect developmental transition by modulating ecdysone biosynthesis.
Journal Proc Natl Acad Sci U S A
Abstract Insect development is cooperatively orchestrated by the steroid hormone ecdysone and juvenile hormone (JH). The polycomb repressive complex 2 (PRC2)-mediated histone H3K27 trimethylation (H3K27me3) epigenetically silences gene transcription and is essential for a range of biological processes, but the functions of H3K27 methylation in insect hormone action are poorly understood. Here, we demonstrate that H3K27 methylation-mediated repression of Hairy transcription in the larval prothoracic gland (PG) is required for ecdysone biosynthesis in Bombyx and Drosophila H3K27me3 levels in the PG are dynamically increased during the last larval instar. H3K27me3 reduction induced by the down-regulation of PRC2 activity via inhibitor treatment in Bombyx or PG-specific knockdown of the PRC2 component Su(z)12 in Drosophila diminishes ecdysone biosynthesis and disturbs the larval-pupal transition. Mechanistically, H3K27 methylation targets the JH signal transducer Hairy to repress its transcription in the PG; PG-specific knockdown or overexpression of the Hairy gene disrupts ecdysone biosynthesis and developmental transition; and developmental defects caused by PG-specific Su(z)12 knockdown can be partially rescued by Hairy down-regulation. The application of JH mimic to the PG decreases both H3K27me3 levels and Su(z)12 expression. Altogether, our study reveals that PRC2-mediated H3K27 methylation at Hairy in the PG during the larval period is required for ecdysone biosynthesis and the larval-pupal transition and provides insights into epigenetic regulation of the crosstalk between JH and ecdysone during insect development.
Volume 118(35)
Published 2021-8-31
DOI 10.1073/pnas.2101442118
PII 2101442118
PMID 34429358
PMC PMC8536348
MeSH Animals Basic Helix-Loop-Helix Transcription Factors / genetics* Basic Helix-Loop-Helix Transcription Factors / metabolism Bombyx / metabolism* Drosophila / metabolism* Drosophila Proteins / genetics* Drosophila Proteins / metabolism Ecdysone / biosynthesis* Epigenesis, Genetic Gene Expression Regulation, Developmental Histones / metabolism* Insect Proteins / genetics* Insect Proteins / metabolism Juvenile Hormones / metabolism Larva / metabolism Methylation Pupa / metabolism Repressor Proteins / genetics* Repressor Proteins / metabolism Signal Transduction Steroids / metabolism
IF 9.412