Transcriptome analysis of the Oriental fruit fly Bactrocera dorsalis early embryos

Authors: PENG, WEI - Huazhong Agricultural University; YU, SHUNING - Huazhong Agricultural University; Handler, Alfred - Al; ZHANG, HONNNNGYU - Huazhong Agricultural University

Submitted to: Insects
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/28/2020
Publication Date: 5/23/2020
Citation: Peng, W., Yu, S., Handler, A.M., Zhang, H. 2020. Transcriptome analysis of the Oriental fruit fly Bactrocera dorsalis early embryos. Insects. 11(5):323. https://doi.org/10.3390/insects11050323.
DOI: https://doi.org/10.3390/insects11050323

Interpretive Summary: The Oriental fruit fly is a major invasive pest insect that has the potential to threaten numerous fruit and vegetable crops in the U.S. Understanding the genetic mechanisms that control sexual differentiation and early embryonic development have provided tools to create genetically modified strains in other pest insects for more effective biological control using the sterile insect technique (SIT). A major advance in SIT for the Oriental fruit fly would be a system that eliminates females early in embryonic development thus avoiding costs of rearing and the need to sterilize and release females along with sterile males. Scientists at Huazhong Agricultural University, China, in collaboration with those at USDA, Agriculture Research Service, Center for Medical, Agricultural and Veterinary Entomology, Gainesville, Florida, conducted a transcriptome sequencing study of the Oriental fruit fly to assess the changes in gene activity that occur at the early stages of embryonic development, and specifically, those genes involved in sex determination and cell formation in the embryos. While changes in gene activity were observed for more than 13,000 genes involved in these processes, twenty-four specific genes were identified for their high levels of expression. These twenty-four genes will be investigated and manipulated to provide new strategies for eliminating females and sterilizing males for more effective SIT in the pest fruit fly species.

Technical 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.