The dynamic landscape of gene regulation during Bombyx mori oogenesis

Qiang Zhang,Yang Xiao,Ze Zhang,Bang-Yong Sun,Wei Sun

doi:10.1186/s12864-017-4123-6

Abstract

BackgroundOogenesis in the domestic silkworm (Bombyx mori) is a complex process involving previtellogenesis, vitellogenesis and choriogenesis. During this process, follicles show drastic morphological and physiological changes. However, the genome-wide regulatory profiles of gene expression during oogenesis remain to be determined.ResultsIn this study, we obtained time-series transcriptome data and used these data to reveal the dynamic landscape of gene regulation during oogenesis. A total of 1932 genes were identified to be differentially expressed among different stages, most of which occurred during the transition from late vitellogenesis to early choriogenesis. Using weighted gene co-expression network analysis, we identified six stage-specific gene modules that correspond to multiple regulatory pathways. Strikingly, the biosynthesis pathway of the molting hormone 20-hydroxyecdysone (20E) was enriched in one of the modules. Further analysis showed that the ecdysteroid 20-hydroxylase gene (CYP314A1) of steroidgenesis genes was mainly expressed in previtellogenesis and early vitellogenesis. However, the 20E–inactivated genes, particularly the ecdysteroid 26-hydroxylase encoding gene (Cyp18a1), were highly expressed in late vitellogenesis. These distinct expression patterns between 20E synthesis and catabolism-related genes might ensure the rapid decline of the hormone titer at the transition point from vitellogenesis to choriogenesis. In addition, we compared landscapes of gene regulation between silkworm (Lepidoptera) and fruit fly (Diptera) oogeneses. Our results show that there is some consensus in the modules of gene co-expression during oogenesis in these insects.ConclusionsThe data presented in this study provide new insights into the regulatory mechanisms underlying oogenesis in insects with polytrophic meroistic ovaries. The results also provide clues for further investigating the roles of epigenetic reconfiguration and circadian rhythm in insect oogenesis.

Highlights

Oogenesis in the domestic silkworm (Bombyx mori) is a complex process involving previtellogenesis, vitellogenesis and choriogenesis
The goal of the study was to determine the dynamic landscape of gene regulation during domestic silkworm oogenesis by analyzing time-series transcriptome data
Drastic morphological changes during oogenesis In polytrophic meroistic ovarioles, the germarium is the area at the tip of the ovarioles where egg formation is initiated, containing germ line stem cells, somatic stem cells, and their niches [9]

Summary

Introduction

Oogenesis in the domestic silkworm (Bombyx mori) is a complex process involving previtellogenesis, vitellogenesis and choriogenesis. During this process, follicles show drastic morphological and physiological changes. The genome-wide regulatory profiles of gene expression during oogenesis remain to be determined. Relatively simple processes such as the oogenesis of the domestic silkworm Bombyx mori (Lepidoptera) and that of the fruit fly Drosophila melanogaster (Diptera) have been widely used to reveal the molecular mechanisms of developmental regulation [1]. Much research progress has been made toward understanding the changes in gene expression and the role of hormones in insect oogenesis [1,2,3]. While Drosophila oogenesis is regulated by both juvenile hormone (JH) and 20E [5], it

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