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Journal of Integrative Agriculture  2025, Vol. 24 Issue (8): 3155-3168    DOI: 10.1016/j.jia.2024.12.015
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Differential energy pathways are required for rapid long-term memory formation in the oriental fruit fly, Bactrocera dorsalis
Jinxin Yu, Jiayi He, Xuefeng Zhang, Chuxiao LinShiyan Liu, Xin Gong, Xinnian Zeng#, Jiali Liu#

State Key Laboratory of Green Pesticide/Guangdong Engineering Research Center for Insect Behavior Regulation/College of Plant Protection, South China Agricultural University, Guangzhou 510642, China

 Highlights 
Bactrocera dorsalis can rapidly form long-term memory.
Long-term memory formation is  an energy-consuming process.
Early long-term memory formation requires energy from the TCA cycle, while late long-term memory formation requires energy from oxidative phosphorylation.
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摘要  

为了确保获取的信息的可靠性,大多数昆虫在将信息存储为长期记忆之前需要经历多个间隔的体验,这一观点在昆虫的行为和分子层面上均得到证实。近期的研究表明,一些昆虫在一次经历后就能形成长期记忆。然而,单次经历形成长期记忆的机制尚不清楚。因此,了解昆虫快速学习和随后形成偏好的机制至关重要。我们在这里发现了农业害虫桔小实蝇能够迅速形成依赖于蛋白质合成的长期记忆,并且形成长期记忆需要高能量的支持,代价是降低了存活率。此外,我们采用液相色谱-质谱代谢组学方法发现,与长期记忆相关的过程依次与两种能量生成过程相关联,即三羧酸循环和氧化磷酸化。通过阻断这些能量生成过程进一步证实了这一点。我们的研究结果为针对桔小实蝇的能量生成中间代谢物的行为调节剂的开发提供了理论依据,同时也为昆虫快速形成长期记忆提供了新的视角。



Abstract  

To ensure the reliability of learned information, most insects require multiple intervals of experience before storing the information as long-term memory (LTM), and this requirement has been validated in insects from the behavioral to the molecular level.  Recent studies have shown that some insects can form LTM after one-trial experience, although the mechanisms underlying one-trial LTM formation are not well understood.  Therefore, understanding the mechanisms underlying rapid learning and subsequent preference formation in insects is crucial.  Here we show that the agricultural pest Bactrocera dorsalis can rapidly form LTM, which is dependent on protein synthesis, and that the formation of LTM requires high energy support at the cost of reduced survival.  Furthermore, based on a liquid chromatography-mass spectrometry (LC-MS) metabolomics approach, we found that LTM-related processes are sequentially coupled to two processes for energy generation, the TCA cycle and oxidative phosphorylation.  This was further confirmed by blocking these energy generation processes.  Our results provide a theoretical basis for the development of behavioral modulators in oriental fruit flies that target energy generation metabolites, as well as a new perspective on the rapid formation of LTM in insects.

Keywords:  Bactrocera dorsalis       rapid learning       long-term memory       protein synthesis       energy generation  
Received: 24 July 2024   Online: 12 December 2024   Accepted: 11 November 2024
Fund: This study was funded by the National Natural Science Foundation of China (32072486 and 31971424) and the Postdoctoral Fellowship Program of China Postdoctoral Science Foundation (GZC20240511).
About author:  Jinxin Yu, E-mail: jinxinyu1994@163.com; #Correspondence Xinnian Zeng, E-mail: zengxn@scau.edu.cn; Jiali Liu, E-mail: shirley4461@scau.edu.cn

Cite this article: 

Jinxin Yu, Jiayi He, Xuefeng Zhang, Chuxiao Lin, Shiyan Liu, Xin Gong, Xinnian Zeng, Jiali Liu. 2025. Differential energy pathways are required for rapid long-term memory formation in the oriental fruit fly, Bactrocera dorsalis. Journal of Integrative Agriculture, 24(8): 3155-3168.

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