MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalis
In female animals, metabolic homoeostasis and reproductive fitness are critical to population expansion. The trade-off between lipid storage and reproduction inevitably occurs. However, most studies have focused on the complex network of relationships between reproductive and metabolic physiology at...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Taylor & Francis Group
2023-12-01
|
| Series: | RNA Biology |
| Subjects: | |
| Online Access: | http://dx.doi.org/10.1080/15476286.2023.2204579 |
| _version_ | 1827595049475506176 |
|---|---|
| author | Shengfeng Zhang Junfei Xie Rengang Luo Hongyu Zhang Weiwei Zheng |
| author_facet | Shengfeng Zhang Junfei Xie Rengang Luo Hongyu Zhang Weiwei Zheng |
| author_sort | Shengfeng Zhang |
| collection | DOAJ |
| description | In female animals, metabolic homoeostasis and reproductive fitness are critical to population expansion. The trade-off between lipid storage and reproduction inevitably occurs. However, most studies have focused on the complex network of relationships between reproductive and metabolic physiology at the transcriptional level. In this study, we identified a microRNA, miR-2b-2-5p, in a highly invasive quarantine pest, Bactrocera dorsalis. Knockdown of miR-2b-2-5p by antagomiR microinjection impaired ovarian development, reduced fecundity, and decreased triglyceride (TAG) storage in the fat body, whereas overexpression of miR-2b-2-5p by injection of its mimic caused reproductive defects similar to knockdown but increased TAG. Bioinformatics analysis and dual luciferase assay indicated that cyclic AMP response element (CRE)-binding protein (CREB) was the target gene of miR-2b-2-5p. RNAi-mediated knockdown of CREB led to excessive lipid storage and reproductive defects. Further starvation treatment revealed that miR-2b-2-5p functions by fine-tuning CREB expression in response to dietary stimuli. These results suggest that miR-2b-2-5p acts as a monitor to regulate CREB mRNA levels in the fat body, maintaining lipid homoeostasis and keeping the reproductive system on track. Thus, our study not only provides new insights into the interaction between metabolism and reproduction at the posttranscriptional level in B. dorsalis, but also providing a potential eco-friendly control strategy (RNAi-based biopesticides targeting essential miRNAs) for this notorious agricultural pest. |
| first_indexed | 2024-03-09T02:46:10Z |
| format | Article |
| id | doaj.art-432eb7a98b9744b5b4b1eb0ff5479005 |
| institution | Directory Open Access Journal |
| issn | 1547-6286 1555-8584 |
| language | English |
| last_indexed | 2024-03-09T02:46:10Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | RNA Biology |
| spelling | doaj.art-432eb7a98b9744b5b4b1eb0ff54790052023-12-05T16:09:52ZengTaylor & Francis GroupRNA Biology1547-62861555-85842023-12-0120116417610.1080/15476286.2023.22045792204579MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalisShengfeng Zhang0Junfei Xie1Rengang Luo2Hongyu Zhang3Weiwei Zheng4Huazhong Agricultural UniversityHuazhong Agricultural UniversityHuazhong Agricultural UniversityHuazhong Agricultural UniversityHuazhong Agricultural UniversityIn female animals, metabolic homoeostasis and reproductive fitness are critical to population expansion. The trade-off between lipid storage and reproduction inevitably occurs. However, most studies have focused on the complex network of relationships between reproductive and metabolic physiology at the transcriptional level. In this study, we identified a microRNA, miR-2b-2-5p, in a highly invasive quarantine pest, Bactrocera dorsalis. Knockdown of miR-2b-2-5p by antagomiR microinjection impaired ovarian development, reduced fecundity, and decreased triglyceride (TAG) storage in the fat body, whereas overexpression of miR-2b-2-5p by injection of its mimic caused reproductive defects similar to knockdown but increased TAG. Bioinformatics analysis and dual luciferase assay indicated that cyclic AMP response element (CRE)-binding protein (CREB) was the target gene of miR-2b-2-5p. RNAi-mediated knockdown of CREB led to excessive lipid storage and reproductive defects. Further starvation treatment revealed that miR-2b-2-5p functions by fine-tuning CREB expression in response to dietary stimuli. These results suggest that miR-2b-2-5p acts as a monitor to regulate CREB mRNA levels in the fat body, maintaining lipid homoeostasis and keeping the reproductive system on track. Thus, our study not only provides new insights into the interaction between metabolism and reproduction at the posttranscriptional level in B. dorsalis, but also providing a potential eco-friendly control strategy (RNAi-based biopesticides targeting essential miRNAs) for this notorious agricultural pest.http://dx.doi.org/10.1080/15476286.2023.2204579mir-2b-2-5pcrebreproductionmetabolic homoeostasisbactrocera dorsalis |
| spellingShingle | Shengfeng Zhang Junfei Xie Rengang Luo Hongyu Zhang Weiwei Zheng MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalis RNA Biology mir-2b-2-5p creb reproduction metabolic homoeostasis bactrocera dorsalis |
| title | MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalis |
| title_full | MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalis |
| title_fullStr | MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalis |
| title_full_unstemmed | MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalis |
| title_short | MiR-2b-2-5p regulates lipid metabolism and reproduction by targeting CREB in Bactrocera dorsalis |
| title_sort | mir 2b 2 5p regulates lipid metabolism and reproduction by targeting creb in bactrocera dorsalis |
| topic | mir-2b-2-5p creb reproduction metabolic homoeostasis bactrocera dorsalis |
| url | http://dx.doi.org/10.1080/15476286.2023.2204579 |
| work_keys_str_mv | AT shengfengzhang mir2b25pregulateslipidmetabolismandreproductionbytargetingcrebinbactroceradorsalis AT junfeixie mir2b25pregulateslipidmetabolismandreproductionbytargetingcrebinbactroceradorsalis AT rengangluo mir2b25pregulateslipidmetabolismandreproductionbytargetingcrebinbactroceradorsalis AT hongyuzhang mir2b25pregulateslipidmetabolismandreproductionbytargetingcrebinbactroceradorsalis AT weiweizheng mir2b25pregulateslipidmetabolismandreproductionbytargetingcrebinbactroceradorsalis |