A Maternal Gene Regulator CPEB2 Is Involved in Mating-Induced Egg Maturation in the <i>Cnaphalocrocis medinalis</i>
Cytoplasmic polyadenylation element-binding proteins (CPEBs) are critical regulators of maternal mRNA translation during oogenesis, yet their roles in insect reproduction remain underexplored. Here, we characterized CmCPEB2, a CPEB homolog in the rice leaf roller <i>Cnaphalocrocis medinalis<...
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| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2025-06-01
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| Series: | Insects |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2075-4450/16/7/666 |
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| Summary: | Cytoplasmic polyadenylation element-binding proteins (CPEBs) are critical regulators of maternal mRNA translation during oogenesis, yet their roles in insect reproduction remain underexplored. Here, we characterized CmCPEB2, a CPEB homolog in the rice leaf roller <i>Cnaphalocrocis medinalis</i>, a destructive lepidopteran pest insect, and elucidated its role in mating-induced oviposition. The CmCPEB2 protein harbored conserved RNA recognition motifs and a ZZ-type zinc finger domain and was phylogenetically clustered with lepidopteran orthologs. Spatiotemporal expression profiling revealed <i>CmCPEB2</i> was predominantly expressed in ovaries post-mating, peaking at 12 h with a 6.75-fold increase in transcript levels. Liposome-mediated RNA interference targeting <i>CmCPEB2</i> resulted in a 52% reduction in transcript abundance, leading to significant defects in ovarian maturation, diminished vitellogenin deposition, and a 36.7% decline in fecundity. The transcriptomic analysis of RNAi-treated ovaries identified 512 differentially expressed genes, with downregulated genes enriched in chorion formation and epithelial cell development. Tissue culture-based hormonal assays demonstrated the juvenile hormone-dependent regulation of <i>CmCPEB2</i>, as JH treatment induced its transcription, while knockdown of the JH-responsive transcription factor <i>CmKr</i>-h1 in the moths suppressed <i>CmCPEB2</i> expression post-mating. These findings established CmCPEB2 as a juvenile hormone-dependent regulator of mating-induced oviposition that orchestrates vitellogenesis through yolk protein synthesis and ovarian deposition and choriogenesis via transcriptional control of chorion-related genes. This study provides novel evidence of CPEB2-mediated reproductive regulation in Lepidoptera, highlighting its dual role in nutrient allocation and structural eggshell formation during insect oogenesis and oviposition. |
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| ISSN: | 2075-4450 |