RNA interference of Argonaute‐1 delays ovarian development in the oriental fruit fly, Bactrocera dorsalis (Hendel)

Abstract

BACKGROUND With the development of rapid resistance, new modes of action for pesticides are needed for insect control, such as RNAi‐based biopesticides targeting essential genes. To explore the function of Argonaute‐1 (Ago‐1) and potential miRNAs in ovarian development of Bactrocera dorsalis, an important agricultural pest, and to develop a novel control strategy for the pest, BdAgo‐1 was first identified in B. dorsalis. RESULTS Spatiotemporal expression analysis indicated that BdAgo‐1 had a relatively high transcriptional level in the ovarian tissues of adult female B. dorsalis during the sexual maturation period. RNA interference (RNAi) experiment showed that BdAgo‐1 knockdown significantly decreased the expression levels of ovarian development‐related genes and delayed ovarian development. Although RNAi‐mediated silencing of Ago‐1 led to a reduced ovary surface area, a subsequent oviposition assay revealed that the influence was minimal over a longer time period. Small RNA libraries were constructed and sequenced from different ovarian developmental stages of B. dorsalis adults. Among 161 identified miRNAs, 84 miRNAs were differentially expressed during the three developmental stages of the B. dorsalis ovary. BdAgo‐1 silencing caused significant down‐regulation of seven differentially expressed miRNAs (DEMs) showing relatively high expression levels (>1000 TPM (Transcripts per kilobase of exon model per million mapped reads)). The expression patterns of these seven core DEMs and their putative target genes were analyzed in the ovaries of B. dorsalis. CONCLUSION The results indicate that Ago‐1 and Ago‐1‐dependent miRNAs are indispensable for normal ovarian development in B. dorsalis and help identify miRNA targets useful for control of this pest.

Argonaute1 and Gawky Are Required for the Development and Reproduction of Melon fly, Zeugodacus cucurbitae

“…Phylogenetic analysis revealed that these proteins are conserved in different fruit fly species, including D. melanogaster . Our findings show that Ago1 has two functional domains, PAZ and PIWI, which are very similar to its homologs in other insects, such as Z. cucurbitae , D. melanogaster , and T. castaneum ( Xu et al, 2013 ; Yang et al, 2021b ). Gawky contains two functional domains, RRM and the M domain.…”

“…The high expression of Ago1 in the ovary and Gawky in the head implies that these genes play important roles in these tissues. Previous studies have shown that Ago1 is highly expressed in Drosophila oocytes, while in B. mori , it is mainly expressed in the ovary, testis, midgut, and head ( Wu et al, 2021 ; Yang et al, 2021 ; Zhao et al, 2021 ). These various expression patterns may be due to the specific functions of Ago1 genes in different insect species.…”

“…We report for the first time that Ago1 silencing at early developmental stages affects ovariole development in Z. cucurbitae . When B. dorsalis adult females were injected with ds Ago1 , the ovarian growth was stopped and both ovaries were substantially smaller but had no effect on ovariole number, shape, or oviposition ( Yang et al, 2021 ). Ago1 knockdown in L. migratoria caused decrease of the vgA transcript in the fat body, which arrests ovary development and oocyte maturation, and results in short terminal oocytes ( Song et al, 2013 ).…”

“…Ago1 mutations cause mitotic abnormalities during early embryogenesis of Drosophila , indicating that it plays a vital role in development ( You et al, 2019b ; Heyt and Thakur 2021 ). The Ago1 studies in Locusta migratoria and Bactrocera dorsalis have shown that loss of Ago1 affects ovarian growth by decreasing vitellogenin expression ( Yang et al, 2021 ). Yet there is no study about the role of Ago1 in the ovary development of Z. cucurbitae .…”

The microRNA pathway core genes are indispensable for development and reproduction in the brown planthopper, Nilaparvata lugens

“…However, some species, such as Schistocerca gregaria (Wynant et al, 2015), contain a DEAD-box RNA helicase domain at the N-terminal, but the domain is not necessary for Dicer activity in vitro and its role remains unknown (Lee et al, 2006). NlAgo1 is a critical effector of miRNA function and is characterised by a domain of DUF1785 and two typical domains, namely, PAZ and Piwi, which exhibit high consistency and homology with the reported insect Ago1 proteins in B. dorsalis (Yang et al, 2021) and L. migratoria (Gao et al, 2020).…”