Glutamate–GABA imbalance mediated by miR-8-5p and its STTM regulates phase-related behavior of locusts

Author:

Yang Meiling12,Du Baozhen3ORCID,Xu Lingling2,Wang Huimin12,Wang Yanli4,Lin Ke1,He Guofei1,Kang Le235ORCID

Affiliation:

1. College of Life Sciences, Capital Normal University, Beijing 100048, China

2. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

3. Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing 100101, China

4. Institute of Applied Biology, Shanxi University, Taiyuan, Shanxi 030006, China

5. College of Life Science, Hebei University, Baoding 071002, China

Abstract

The aggregation of locusts from solitary to gregarious phases is crucial for the formation of devastating locust plagues. Locust management requires research on the prevention of aggregation or alternative and greener solutions to replace insecticide use, and insect-derived microRNAs (miRNAs) show the potential for application in pest control. Here, we performed a genome-wide screen of the differential expression of miRNAs between solitary and gregarious locusts and showed that miR-8-5p controls the γ-aminobutyric acid (GABA)/glutamate functional balance by directly targeting glutamate decarboxylase (Gad). Blocking glutamate–GABA neurotransmission by miR-8-5p overexpression or Gad RNAi in solitary locusts decreased GABA production, resulting in locust aggregation behavior. Conversely, activating this pathway by miR-8-5p knockdown in gregarious locusts induced GABA production to eliminate aggregation behavior. Further results demonstrated that ionotropic glutamate/GABA receptors tuned glutamate/GABA to trigger/hamper the aggregation behavior of locusts. Finally, we successfully established a transgenic rice line expressing the miR-8-5p inhibitor by short tandem target mimic (STTM). When locusts fed on transgenic rice plants, Gad transcript levels in the brain increased greatly, and aggregation behavior was lost. This study provided insights into different regulatory pathways in the phase change of locusts and a potential control approach through behavioral regulation in insect pests.

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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