The genome-wide transcriptional regulatory landscape of ecdysone in the silkworm

Dong Cheng,Quan Zhang,Xi Yang,Jianfeng Fu,Jiao Gong,Tieshan Feng,Qingyou Xia,Tingcai Cheng

doi:10.1186/s13072-018-0216-y

Abstract

BackgroundThe silkworm, Bombyx mori, a typical representative of metamorphic insects, is of great agricultural and economic importance. The steroid hormone ecdysone (20-hydroxyecdysone, 20E) is the central regulator of insect developmental transitions, and its nuclear receptors are crucial for numerous biological processes, including reproduction, metabolism, and immunity. However, genome-wide DNA regulatory elements and the ecdysone receptor (EcR) that control these programs of gene expression are not well defined.ResultsIn this study, we investigated the alterations in three types of histone modification in silkworm embryonic cells treated with 20E by chromatin immunoprecipitation sequencing (ChIP-seq). We identified enhancers using histone modifications and derived genome-wide ecdysone-dependent enhancer activity maps in the silkworm. We found enhancers enriched for monomethylation of histone H3 Lys4 (H3K4me1) that showed dynamic changes in acetylation of histone H3 Lys27 (H3K27ac) after 20E treatment and functioned to regulate the transcription of specific genes. EcR regulated transcription by binding not only to proximal promoters but also to the distal enhancers of target genes. Moreover, only 52.65% EcR peaks contained ecdysone response element (EcRE) motif, suggesting that EcR regulates the expression of target genes not only by binding directly to EcRE, but also by binding with other transcription factor.ConclusionsOur findings provide novel insights into the complex regulatory landscape of hormone-responsive cell activity and a basis for understanding the complex transcriptional regulatory processes of ecdysone.

Highlights

The silkworm, Bombyx mori, a typical representative of metamorphic insects, is of great agricultural and economic importance
Previous studies have shown that trimethylation of histone H3 Lys4 (H3K4me3) is an active mark that is often found in the proximal promoter region, while monomethylation of histone H3 Lys4 (H3K4me1) is generally associated with enhancers located in the distal promoter region [18, 19]
Genome‐wide changes in histone modifications induced by treatment with 20E To examine whether histone modification statuses were altered throughout the genome by treatment with 20E, we firstly report the overlap of called peaks between 20E-treated BmE cells (“Treated”) and DMSO-treated BmE cells (“Control”)

Summary

Introduction

The silkworm, Bombyx mori, a typical representative of metamorphic insects, is of great agricultural and economic importance. Genome-wide DNA regulatory elements and the ecdysone receptor (EcR) that control these programs of gene expression are not well defined. Spatial–temporal specificity in gene expression is achieved according to information in cis-acting DNA regulatory elements including insulators, promoters, and enhancers [1, 2]. Enhancers have emerged as key cisregulatory elements, independent of their orientation or distance, to affect gene transcription [3,4,5]. Post-translational modifications of histones, such as acetylation and methylation of lysine residues of histone H3, play important roles in regulating gene expression by altering the chromatin structure [10]. Histone-modified marks allow the genome-wide prediction of regulatory elements

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