MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts

MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts
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MicroRNA-276通过上调蝗虫的brm促进卵孵化同步

DOI:
10.1073/pnas.1521098113
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发表时间:
2016-01-19
影响因子:
11.1
通讯作者:
Kang, Le
Kang, Le
中科院分区:
综合性期刊1区
文献类型:
--
作者:
He, Jing;Chen, Qianquan;Kang, Le

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发育的同步性,减少个体发育速率的波动,对集群动物的群集,迁移和社会关系至关重要。然而,同步发育的分子调控因子知之甚少。飞蝗在高密度群居和低密度独居之间过渡,高密度群居性成熟更同步。在这里,我们确定了一个microRNA(miRNA),miR-276,在雌性蝗虫卵巢介导后代卵孵化同步上调其目标brahma(brm),转录辅激活基因。此外,这种上调依赖于brm RNA的二级结构。我们的研究表明了一种非经典的miRNA介导的基因调控机制,并提供了蝗虫相变的重要特征,为可能预测鼠疫爆发提供了线索。发育同步性是群居动物适应环境变化的重要策略,是群居动物群体一致性群集、迁移和性成熟的基础。然而,发育同步性的分子机制在很大程度上是未知的。飞蝗的性成熟和迁飞的同步性强于群居个体和独居个体。结果表明,群居蝗虫卵的孵化时间比独居蝗虫卵的孵化时间更均匀,且microRNA-276(miR-276)在群居蝗虫卵巢和卵中的表达量显著高于独居蝗虫。有趣的是,在群居雌性中抑制miR-276和在独居雌性中过表达miR-276分别导致后代卵的异时和同步孵化。此外,miR-276直接靶向转录辅激活因子基因brahma(brm),导致其上调。BRM基因的敲除不仅导致群居蝗虫卵的异步孵化,而且还削弱了miR-276诱导的独居蝗虫卵的同步孵化。从机制上讲,miR-276以依赖于brm二级结构的方式介导brm活化,即miR-276结合位点周围的茎环。总的来说,我们的研究结果揭示了miR-276增强brm表达以促进发育同步的机制,并为发育稳态和与生物同步密切相关的种群维持的调节提供了见解。
Significance Developmental synchrony, resulting from reduced fluctuation in individual development rate, is critical for swarming, migration, and social relationships of colonial animals. However, the molecular regulators of synchronous development are poorly understood. The migratory locust transits between high-density gregarious and low-density solitarious phases, with the former displaying more synchronous sexual maturation. Here, we identify a microRNA (miRNA), miR-276, expressed in the ovaries of female locusts mediating progeny egg-hatching synchrony by up-regulating its target brahma (brm), a transcription coactivator gene. Moreover, this up-regulation was dependent on the secondary structure of brm RNA. Our study demonstrates a noncanonical mechanism of miRNA-mediated gene regulation and provides important traits of locust phase transition for clues of possible prediction of pest plague outbreaks. Developmental synchrony, the basis of uniform swarming, migration, and sexual maturation, is an important strategy for social animals to adapt to variable environments. However, the molecular mechanisms underlying developmental synchrony are largely unexplored. The migratory locust exhibits polyphenism between gregarious and solitarious individuals, with the former displaying more synchronous sexual maturation and migration than the latter. Here, we found that the egg-hatching time of gregarious locusts was more uniform compared with solitarious locusts and that microRNA-276 (miR-276) was expressed significantly higher in both ovaries and eggs of gregarious locusts than in solitarious locusts. Interestingly, inhibiting miR-276 in gregarious females and overexpressing it in solitarious females, respectively, caused more heterochronic and synchronous hatching of progeny eggs. Moreover, miR-276 directly targeted a transcription coactivator gene, brahma (brm), resulting in its up-regulation. Knockdown of brm not only resulted in asynchronous egg hatching in gregarious locusts but also impaired the miR-276–induced synchronous egg hatching in solitarious locusts. Mechanistically, miR-276 mediated brm activation in a manner that depended on the secondary structure of brm, namely, a stem-loop around the binding site of miR-276. Collectively, our results unravel a mechanism by which miR-276 enhances brm expression to promote developmental synchrony and provide insight into regulation of developmental homeostasis and population sustaining that are closely related to biological synchrony.