Abstract

The oriental fruit fly, Bactrocera dorsalis (Hendel), is one of the most devastating and highly invasive agricultural pests world-wide, resulting in severe economic loss. Thus, it is of great interest to understand the transcriptional changes that occur during the activation of its zygotic genome at the early stages of embryonic development, especially the expression of genes involved in sex determination and the cellularization processes. In this study, we applied Illumina sequencing to identify B. dorsalis sex determination genes and early zygotic genes by analyzing transcripts from three early embryonic stages at 0–1, 2–4, and 5–8 h post-oviposition, which include the initiation of sex determination and cellularization. These tests generated 13,489 unigenes with an average length of 2185 bp. In total, 1683, 3201 and 3134 unigenes had significant changes in expression levels at times after oviposition including at 2–4 h versus 0–1 h, 5–8 h versus 0–1 h, and 5–8 h versus 2–4 h, respectively. Clusters of gene orthology (GO) and the Kyoto Encyclopedia of Genes and Genomes (KEGG) annotations were performed throughout embryonic development to better understand the functions of differentially expressed unigenes. We observed that the RNA binding and spliceosome pathways were highly enriched and overrepresented during the early stage of embryogenesis. Additionally, transcripts for 21 sex-determination and three cellularization genes were identified, and expression pattern analysis revealed that the majority of these genes were highly expressed during embryogenesis. This study is the first assembly performed for B. dorsalis based on Illumina next-generation sequencing technology during embryogenesis. Our data should contribute significantly to the fundamental understanding of sex determination and early embryogenesis in tephritid fruit flies, and provide gene promoter and effector gene candidates for transgenic pest-management strategies for these economically important species.

Highlights

  • The oriental fruit fly, Bactrocera dorsalis (Hendel), is one of the most devastating and highly invasive agricultural pests in the world that causes severe economic loss due to damage to over 250 types of fruits and vegetables throughout Southeast Asia and several Pacific Islands [1,2]

  • We present a preliminary scenario of early zygotic gene expression during the maternal-to-zygotic transition (MTZ) in this non-model organism

  • We have identified several sex determination and early zygotic genes that should contribute to the development of novel genetic control strategies for B. dorsalis and related pest species

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Summary

Introduction

The oriental fruit fly, Bactrocera dorsalis (Hendel), is one of the most devastating and highly invasive agricultural pests in the world that causes severe economic loss due to damage to over 250 types of fruits and vegetables throughout Southeast Asia and several Pacific Islands [1,2]. Insects 2020, 11, 323 are currently considered to be the most effective tool to control fruit flies; resistance to commonly applied chemical insecticides in B. dorsalis has been increasing [3,4], and it is, urgent to develop new environmentally acceptable methods to control this pest and related tephritid pests. The primary biological method for tephritid fruit fly control has been the sterile insect techniques (SIT); sterile males generated by irradiation or chemosterilants in traditional methods have decreased mating performance, which reduces population control efficiency [5]. Genetically-enhanced SIT, that include transgenic genetic male sterility and sexing strains, have shown significant potential for fruit fly management [6,7,8,9,10,11,12]. Based on the identification of key sex-determining genes in insects, it has been possible to obtain male-only progeny by knocking down the female determining genes transformer (tra) and transformer-2 (tra-2) for male-only populations [13,14,15,16,17,18,19]

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