Histone H3K27 methylation-mediated repression of regulates insect developmental transition by modulating ecdysone biosynthesis.

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 transcription in the larval prothoracic gland (PG) is required for ecdysone biosynthesis in and 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 or PG-specific knockdown of the PRC2 component in diminishes ecdysone biosynthesis and disturbs the larval-pupal transition. Mechanistically, H3K27 methylation targets the JH signal transducer to repress its transcription in the PG; PG-specific knockdown or overexpression of the gene disrupts ecdysone biosynthesis and developmental transition; and developmental defects caused by PG-specific knockdown can be partially rescued by down-regulation. The application of JH mimic to the PG decreases both H3K27me3 levels and expression. Altogether, our study reveals that PRC2-mediated H3K27 methylation at 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.