In nature, most insects do not exhibit nurturing behavior. That is to say, when insect mothers leave their offspring in the form of laying eggs, they quietly die. So, as swarm insects, what can locusts do for their offspring? On May 21, the recreation team of the academicians of the CAS Member published a research paper entitled Parental experiences or strategic location egg hatching synchronization by regulating nuclear export of precursor miRNA online on Nature Communications, which clarified the signal transmission mechanism of female insects' high population density experience regulating the synchronous hatching of their offspring locust eggs to pre adapt to the high population density experienced by their mothers.

The cross generational effect induced by parental environment is a common phenomenon in nature. At present, research on cross generational effects focuses on the molecular signaling pathways of small RNAs in the reproductive system that regulate post representational types, while there is little research on how small RNAs in the reproductive system respond to external environmental signals. Research has found that the high population density of locusts experiences a molecular mechanism by regulating the transcription factor FOXN1 and RNA binding protein PTBP1 in terminal oocytes to induce miR-276 expression, thereby promoting synchronous hatching of offspring eggs. This fills the gap in the mechanism by which the reproductive system responds to external environmental signals and generates intergenerational effects.

In the early stage, the team found that locusts responded to high population density by regulating the high expression of miR-276 in the ovaries, thereby mediating synchronous hatching of offspring eggs. This study detected products from different stages of the miR-276 synthesis process and determined the population density changes in response to the pre miR-276 precursor's nuclear transport. Furthermore, the study confirmed through pre miR-276 RNA pull down experiments, combined with in vivo interference and in vitro overexpression experiments, that the RNA binding protein PTBP1 in high-density locusts promotes the nucleation and maturation of pre miR-276. Research has shown that the high expression of PTBP1 in social locusts is caused by the activation of transcription factor FOXN1, which responds to population density changes at the protein level. To analyze the mechanism of PTBP1 regulating pre miR-276 nucleation, the study conducted in vitro and in vivo protein interaction experiments as well as protein RNA interaction experiments. It was found that PTBP1 promotes pre miR-276 nucleation by recruiting the necessary nuclear transporter protein Exportin-5 (XPO5) for pre miRNA nucleation transport. In addition, research has found that the "CU motifs" on pre miR-276 are the "tags" recognized by PTBP1 for pre miR-276, which enables PTBP1 to specifically bind to pre miR-276 to promote pre miR-276 nucleation, leading to high expression of miR-276 and inducing synchronous hatching of offspring eggs.



Research has found that under high population density, the transcription factor FOXN1 and RNA binding protein PTBP1 are highly expressed in the terminal oocytes of locusts; PTBP1 induces PTBP1 by recognizing the "tag" on pre miR-276 and binds to it, recruiting more XPO5 to promote efficient nucleation of pre miR-276 and induce miR-276 mediated synchronous hatching of offspring eggs. Meanwhile, The mechanism by which PTBP1 promotes pre miR-276 nucleation is conserved in insects.



This study combines the life experiences of animals with the micro molecular regulatory pathways in organisms, proposing new ideas and insights on miRNA synthesis and processing, as well as how to respond to the environment, deepening the understanding of the cross generational effect mechanism mediated by the environment. Especially, the high population density of locusts undergoes synchronous hatching of their offspring eggs, laying the foundation for future larval aggregation and large-scale migration of adults. Parents arrange their offspring's life history strategies in advance based on their own life experiences, which helps them adapt to the environment in which their mother once lived.



The research work has been supported by the National Natural Science Foundation of China and the National Key Research and Development Program.



Paper link





The mode of action of FOXN1-PTBP1-miR-276 in response to high population density regulation of synchronized hatching of offspring eggs