Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing, China.
CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China.
PLoS Genet. 2021 Jan 6;17(1):e1009174. doi: 10.1371/journal.pgen.1009174. eCollection 2021 Jan.
Outbreaks of locust plagues result from the long-term accumulation of high-density egg production. The migratory locust, Locusta migratoria, displays dramatic differences in the egg-laid number with dependence on population density, while solitarious locusts lay more eggs compared to gregarious ones. However, the regulatory mechanism for the egg-laid number difference is unclear. Herein, we confirm that oosorption plays a crucial role in the regulation of egg number through the comparison of physiological and molecular biological profiles in gregarious and solitarious locusts. We find that gregarious oocytes display a 15% higher oosorption ratio than solitarious ones. Activinβ (Actβ) is the most highly upregulated gene in the gregarious terminal oocyte (GTO) compared to solitarious terminal oocyte (STO). Meanwhile, Actβ increases sharply from the normal oocyte (N) to resorption body 1 (RB1) stage during oosorption. The knockdown of Actβ significantly reduces the oosorption ratio by 13% in gregarious locusts, resulting in an increase in the egg-laid number. Based on bioinformatic prediction and experimental verification, microRNA-34 with three isoforms can target Actβ. The microRNAs display higher expression levels in STO than those in GTO and contrasting expression patterns of Actβ from the N to RB1 transition. Overexpression of each miR-34 isoform leads to decreased Actβ levels and significantly reduces the oosorption ratio in gregarious locusts. In contrast, inhibition of the miR-34 isoforms results in increased Actβ levels and eventually elevates the oosorption ratio of solitarious locusts. Our study reports an undescribed mechanism of oosorption through miRNA targeting of a TGFβ ligand and provides new insights into the mechanism of density-dependent reproductive adaption in insects.
蝗灾的爆发是长期高密度产卵积累的结果。 飞蝗（Locusta migratoria）的产卵数量存在明显差异，取决于种群密度，群居型飞蝗比散居型飞蝗产卵更多。 然而，产卵数量差异的调节机制尚不清楚。 在此，我们通过比较群居型和散居型飞蝗的生理和分子生物学特征，证实卵吸收在调节产卵数量中起关键作用。 我们发现，群居型卵母细胞的卵吸收比例比散居型高 15%。 与散居型终末卵母细胞（STO）相比，激活素β（Actβ）在群居型终末卵母细胞（GTO）中表达水平最高。 同时，Actβ 在卵吸收过程中从正常卵（N）到吸收体 1（RB1）阶段急剧增加。 Actβ 的敲低使群居型飞蝗的卵吸收比例降低 13%，导致产卵数量增加。 通过生物信息学预测和实验验证，发现具有三种同工型的 microRNA-34 可以靶向 Actβ。 这些 microRNAs 在 STO 中的表达水平高于 GTO，且在 N 到 RB1 过渡过程中与 Actβ 的表达模式相反。 每个 miR-34 同工型的过表达导致 Actβ 水平降低，并使群居型飞蝗的卵吸收比例显著降低。 相反，miR-34 同工型的抑制导致 Actβ 水平升高，最终增加散居型飞蝗的卵吸收比例。 本研究报告了一种通过 microRNA 靶向 TGFβ 配体进行卵吸收的未描述机制，并为昆虫密度依赖生殖适应的机制提供了新的见解。
