circRNAs derived from a nuclear hormone receptor act differentially on insect metamorphosis and reproduction

Lulu Gao; Qiang Yan; Ying Qu; Wanwan Li; Jiasheng Song; Shutang Zhou

doi:10.1016/j.jgg.2025.10.001

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circRNAs derived from a nuclear hormone receptor act differentially on insect metamorphosis and reproduction

doi: 10.1016/j.jgg.2025.10.001

State Key Laboratory of Cotton Bio-breeding and Integrated Utilization, School of Life Sciences, Henan University, Kaifeng, Henan 475001, China

Funds:

This work was supported by the National Natural Science Foundation of China (32070489 and U22A20482) and the National Key R&

D Program of China (2022YFD1400500).

Received Date: 2025-06-11
Accepted Date: 2025-10-02
Rev Recd Date: 2025-09-29

Available Online: 2025-10-10

Abstract

Abstract

Insects are the most diverse group on earth, partially owing to their metamorphosis and strong fecundity. Circular RNAs (circRNAs) are stable molecules implicated in a broad range of biological processes. However, the regulatory roles of circRNAs in insect metamorphosis and reproduction are unclear. Methoprene-tolerant (Met) is the nuclear receptor of juvenile hormone (JH) that plays dual roles of inhibiting precocious metamorphosis and promoting reproduction. Here, we report that locust Met generates two circRNAs, circMet1 and circMet2, respectively. While circMet1 is highly expressed in the cuticle of late final instar, circMet2 is more abundant in the corpora allata, brain, and fat body of early vitellogenic adults. Interestingly, circMet2 is generated by complementary pairing of Penelope-like remnants across the introns of Met. Moreover, circMet2 functions as a miRNA sponge of four species-specific miRNAs that downregulate Met translation. siRNA-mediated knockdown of circMet1 causes the delay of metamorphosis and retarded vitellogenesis. Loss of circMet2 results in significantly decreased vitellogenin synthesis, along with blocked ovarian growth. These results reveal the differential roles of circMet1 and circMet2 in modulating insect metamorphosis and female reproduction. This study advances our understanding of how circRNAs derived from a single gene exert distinct roles in insect life history.
- circRNA,
- ceRNA,
- Transposon,
- Insect metamorphosis,
- Vitellogenesis,
- Oogenesis

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