Hemolymph Ecdysteroid Titer Affects Maternal mRNAs during Bombyx mori Oogenesis.

Meirong Zhang,Tao Chen,Pingzhen Xu

doi:10.3390/insects12110969

Abstract

Simple SummaryBoth maternal genes and ecdysteroids play important roles during embryonic development. In this study, we aimed to characterize the dynamic landscape of maternal mRNAs and the relationship between maternal genes and ecdysteroids during silkworm oogenesis. For the first time, we determined the start of the accumulation of maternal mRNAs in the ovary at the wandering stage during the larval period. We detected the developmental expression profiles of each gene in the ovary or ovariole. We finally confirmed the role of 20-hydroxyecdysone in regulating maternal gene expression. Taken together, our findings expand the understanding of insect oogenesis and provide a perspective on the embryonic development of the silkworm.Silkworm larval–pupal metamorphosis and the first half of pupal–adult development occur during oogenesis from previtellogenesis to vitellogenesis and include two peaks of the hemolymph ecdysteroid titer. Moreover, a rise in 20-hydroxyecdysone titer in early pupae can trigger the first major transition from previtellogenesis to vitellogenesis in silkworm oogenesis. In this study, we first investigated the expression patterns of 66 maternal genes in the ovary at the wandering stage. We then examined the developmental expression profiles in six time-series samples of ovaries or ovarioles by reverse transcription–quantitative PCR. We found that the transcripts of 22 maternal genes were regulated by 20-hydroxyecdysone in the isolated abdomens of the pupae following a single injection of 20-hydroxyecdysone. This study is the first to determine the relationship between 20-hydroxyecdysone and maternal genes during silkworm oogenesis. These findings provide a basis for further research into the embryonic development of Bombyx mori.

Highlights

Embryonic development occurs in the absence of de novo transcription and is maternally regulated [1,2]
Our data demonstrate the start of the accumulation of maternal mRNAs during stage 3 of the oogenesis developmental period of previtellogenesis in the larva
At stage 3, a small rise in ecdysteroid titer occurs at the start of wandering, and this is followed by a plateau [24]; glycogen synthesis begins in the oocyte, and the follicle cells near the oocyte–nurse cells interface begin to migrate centripetally between the oocyte and the nurse cells [23]

Summary

Introduction

Embryonic development occurs in the absence of de novo transcription and is maternally regulated [1,2]. Most striking during the MZT is the elimination of maternal transcripts and the onset of transcription from the newly activated zygote’s genome [2,5,6]. This transition has been well studied in model organisms, and many early developmental processes are highly conserved and are critical for organism survival [7]. RNA-binding proteins (RBPs) regulate the translation, stability, and localization of maternal mRNAs [8]; Smaug (SMG) RBP is essential to maternal mRNAs degradation in Drosophila melanogaster [9]. The transcription factors critical to the activation of the zygotic genome following maternal mRNA degradation have been identified in Drosophila (Zelda) [14], zebrafish (Nanog, Pou5f1 and SoxB1) [15], mice (Dux, Nfy, Dppa, and Dppa4) [16,17,18], and humans (OCT4 and DUX4) [16,19,20]

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