miR-309a is a regulator of ovarian development in the oriental fruit fly Bactrocera dorsalis

Zhang, Qiang; Dou, Wei; Taning, Clauvis Nji Tizi; Yu, Su; Yuan, Guangjie; Shang, Feng; Smagghe, Guy; Wang, Jinjun

doi:10.1371/journal.pgen.1010411

Cited by 15 publications

(17 citation statements)

References 47 publications

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“…Studies have shown that miRNAs were engaged in the regulation of insect physiology including body weight [ 28 , 29 , 30 ]. Fang et al [ 30 ] found that injection of miR-982490 agomir into 5th instar Grapholita molesta larvae resulted in increased trehalose and triglyceride levels in hemolymph, and decreased pupation success and pupa weight.…”

Section: Discussionmentioning

confidence: 99%

ame-miR-34 Modulates the Larval Body Weight and Immune Response of Apis mellifera Workers to Ascosphara apis Invasion

Guo

Fan

et al. 2023

IJMS

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MiRNAs are critical regulators of numerous physiological and pathological processes. Ascosphaera apis exclusively infects bee larvae and causes chalkbrood disease. However, the function and mechanism of miRNAs in the bee larval response to A. apis infection is poorly understood. Here, ame-miR-34, a previously predicted miRNA involved in the response of Apis mellifera larvae to A. apis invasion, was subjected to molecular validation, and overexpression and knockdown were then conducted to explore the regulatory functions of ame-miR-34 in larval body weight and immune response. Stem-loop RT-PCR and Sanger sequencing confirmed the authenticity of ame-miR-34 in the larval gut of A. mellifera. RT-qPCR results demonstrated that compared with that in the uninfected larval guts, the expression level of ame-miR-34 was significantly downregulated (p < 0.001) in the guts of A. apis-infected 4-, 5-, and 6-day-old larvae, indicative of the remarkable suppression of host ame-miR-34 due to A. apis infection. In comparison with the corresponding negative control (NC) groups, the expression level of ame-miR-34 in the larval guts in the mimic-miR-34 group was significantly upregulated (p < 0.001), while that in the inhibitor-miR-34 group was significantly downregulated (p < 0.01). Similarly, effective overexpression and knockdown of ame-miR-34 were achieved. In addition, the body weights of 5- and 6-day-old larvae were significantly increased compared with those in the mimic-NC group; the weights of 5-day-old larvae in the inhibitor-miR-34 group were significantly decreased in comparison with those in the inhibitor-NC group, while the weights of 4- and 6-day-old larvae in the inhibitor-miR-34 group were significantly increased, indicating the involvement of ame-miR-34 in modulating larval body weight. Furthermore, the expression levels of both hsp and abct in the guts of A. apis-infected 4-, 5-, and 6-day-old larvae were significantly upregulated after ame-miR-34 overexpression. In contrast, after ame-miR-34 knockdown, the expression levels of the aforementioned two key genes in the A. apis-infected 4-, 5-, and 6-day-old larval guts were significantly downregulated. Together, the results demonstrated that effective overexpression and knockdown of ame-miR-34 in both noninfected and A. apis-infected A. mellifera larval guts could be achieved by the feeding method, and ame-miR-34 exerted a regulatory function in the host immune response to A. apis invasion through positive regulation of the expression of hsp and abct. Our findings not only provide a valuable reference for the functional investigation of bee larval miRNAs but also reveal the regulatory role of ame-miR-34 in A. mellifera larval weight and immune response. Additionally, the results of this study may provide a promising molecular target for the treatment of chalkbrood disease.

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Section: Discussionmentioning

confidence: 99%

ame-miR-34 Modulates the Larval Body Weight and Immune Response of Apis mellifera Workers to Ascosphara apis Invasion

Guo

Fan

et al. 2023

IJMS

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“…In our recent study, the expression level of Bdpnr was relatively high during early ovarian development and it induced the Vg-related genes expression; in contrast, during late ovarian development, the high expression of miR-309a inhibited the expression of Bdpnr to avoid excessive transcription of Vg-related genes. 24 Indirect evidence in vivo (overexpression of miR-309a repressed the Vg-related genes expression) and direct evidence in vitro (pnr interaction with Vg-related genes by luciferase reporter assays) indicated that pnr regulates Vg-related gene expression to control ovarian development in B. dorsalis. 24 The current study provides the direct evidence in vivo.…”

Section: Discussionmentioning

confidence: 99%

“…24 Indirect evidence in vivo (overexpression of miR-309a repressed the Vg-related genes expression) and direct evidence in vitro (pnr interaction with Vg-related genes by luciferase reporter assays) indicated that pnr regulates Vg-related gene expression to control ovarian development in B. dorsalis. 24 The current study provides the direct evidence in vivo. Importantly, the evidence of Bdpnr interacted with the BdVgR was proved for the first time in vivo.…”

Section: Discussionmentioning

confidence: 99%

“…16 However, Plutella xylostella PxGA-TAd contributes to BtCry1Ac resistance by reducing PxmALP expression. 17 In our very recent study, there is evidence that the B. dorsalis pnr gene (Bdpnr) regulates ovarian development 24 and could thus be suitable as a target in control strategies for this species and other tephritid pests. However, RNA interference (RNAi) is limited to transcribed genes in B. dorsalis and its efficiency varies significantly depending on the target.…”

Section: Introductionmentioning

confidence: 99%

“…However, RNA interference (RNAi) is limited to transcribed genes in B. dorsalis and its efficiency varies significantly depending on the target. [25][26][27] We have been unable to suppress Bdpnr expression effectively using RNAi, 24 therefore direct evidence of pnr regulating the fly ovarian development is still lacking. In contrast, genome editing using clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPRassociated protein 9 (Cas9) allows the efficient generation of knockout mutations in B. dorsalis, 25,28 so here we used CRISPR/ Cas9 to target the Bdpnr gene.…”

Section: Introductionmentioning

confidence: 99%

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Pannier is a key regulator of embryogenesis, pupal development and female reproduction in the insect pest Bactrocera dorsalis

Zhang

Dou

et al. 2022

Pest Management Science

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Background: Most arthropods are famous for their large reproductive capacity, with the ovary playing a vital role in the process.The study of the regulatory mechanisms of ovarian development may have the potential for a reproduction-based pest management strategy. GATA-binding transcription factors (GATAs) as important regulatory factors mediate many physiological processes, including development, immunity, insecticide resistance and reproduction. The Pannier (pnr), a member of GATA family, was confirmed to be involved in ovarian development of Bactrocera dorsalis in our previous study. However, the direct evidence of pnr regulating the fly ovarian development is still lacking.Results: We used CRISPR/Cas9 to create Bdpnr loss-of-function mutations. Homozygous Bdpnr −/− mutants were nonviable, with most individuals dying during embryogenesis, some surviving to the larval stages, and the remaining few dying during pupation. In contrast, heterozygous individuals reached the adult stage, but ovarian development was disrupted, with concomitant decreases in egg laying and hatching rates. We also found that two genes encoding vitellogenin proteins (BdVg1 and BdVg2) and the vitellogenin receptor (BdVgR) were significantly down-regulated in heterozygous mutants compared to wild-type controls.Conclusion: These results indicate that Bdpnr is required for embryonic and post-embryonic development, including the formation of ovaries. Bdpnr could therefore be considered as a molecular target for tephritid fly pest control.

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MicroRNA PC‐5p‐3991_515 mediates triflumezopyrim susceptibility in the small brown planthopper through regulating the post‐transcriptional expression of P450 CYP417A2

Yang,

Wang,

Xue

et al. 2023

Pest Management Science

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BACKGROUNDCytochrome P450 monooxygenases (P450s) are recognized as a major contributor to metabolic resistance in insects to most insecticides, through gene overexpressions and protein mutations. MicroRNA (miRNA), an important post‐transcriptional regulator, has been reported to promote insecticide resistance by mediating the expression of detoxification enzyme genes.RESULTSIn the present study, we reported that a novel microRNA PC‐5p‐3991_515 was involved in the post‐transcriptional regulation of CYP417A2 and mediated the triflumezopyrim susceptibility in the small brown planthopper (SBPH), Laodelphax striatellus (Fallén). The tissue expression profiles showed that CYP417A2 was highly expressed in fat body. CYP417A2 was significantly up‐regulated at 12, 36, 60, 84 and 108 h after the triflumezopyrim treatment. RNA interference (RNAi) against CYP417A2 significantly increased triflumezopyrim susceptibility in SBPH. According to the prediction by miRanda and TargetScan software, three miRNAs were indicated to bind to CYP417A2. However, when oversupply of agomir, only two miRNAs, PC‐3p‐625_4405 and PC‐5p‐3991_515, significantly increased the susceptibility to triflumezopyrim and decreased CYP417A2 levels. Furthermore, PC‐5p‐3991_515 was confirmed to be involved in the post‐transcriptional regulation of CYP417A2 by dual luciferase reporter assay. Meanwhile, PC‐5p‐3991_515 was co‐localized with CYP417A2 in the midgut in situ hybridization.CONCLUSIONOur findings revealed that the novel microRNA, PC‐5p‐3991_515, post‐transcriptionally regulated CYP417A2 expression, which then mediated the triflumezopyrim susceptibility in SBPH. © 2023 Society of Chemical Industry.

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miR-309a is a regulator of ovarian development in the oriental fruit fly Bactrocera dorsalis

Cited by 15 publications

References 47 publications

ame-miR-34 Modulates the Larval Body Weight and Immune Response of Apis mellifera Workers to Ascosphara apis Invasion

ame-miR-34 Modulates the Larval Body Weight and Immune Response of Apis mellifera Workers to Ascosphara apis Invasion

Pannier is a key regulator of embryogenesis, pupal development and female reproduction in the insect pest Bactrocera dorsalis

MicroRNA PC‐5p‐3991_515 mediates triflumezopyrim susceptibility in the small brown planthopper through regulating the post‐transcriptional expression of P450 CYP417A2

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