Neuropeptide signaling systems are involved in regulating thermal tolerance in the oriental fruit fly

doi:10.1016/j.jia.2024.04.003

Journal of Integrative Agriculture

2024, Vol. 23

Issue (12): 4147-4160 DOI: 10.1016/j.jia.2024.04.003

Special Issue: 昆虫生理与发育Insect physiology

Plant Protection

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Neuropeptide signaling systems are involved in regulating thermal tolerance in the oriental fruit fly

Yang Yang^{1, 2*}, Hongfei Li^{1, 2*}, Changhao Liang^{1, 2}, Donghai He^{1, 2}, Hang Zhao^{1, 2}, Hongbo Jiang^{1, 2#}, Jinjun Wang^{1, 2#}

¹Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Southwest University, Chongqing 400715, China

²Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, China

Abstract
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摘要

神经肽及其受体参与昆虫各种生理过程的调节。虽然神经肽在重要的农业害虫-东方果实蝇（Bactrocera dorsalis，桔小实蝇）中已被鉴定，但其相应的受体仍然未知。目前尚不清楚神经肽信号系统是否参与调节这种害虫的温度耐受性。本文系统鉴定了44个候选的神经肽受体基因（编码66个蛋白序列），分析了桔小实蝇中神经肽配体及其受体基因的时空表达模式，也分析了它们在两个温度驯化种群中的表达情况。结果显示，在驯化过程中，许多神经肽和受体基因参与了对温度胁迫的响应。特别是短神经肽F（sNPF）的表达量在耐高温种群中显著上调。此外，蛋白质组学数据显示，sNPF在两个温度驯化种群中均上调。基于CRISPR/Cas9的功能验证结果表明，sNPF参与了桔小实蝇对温度耐受性的调节。本研究结果丰富了昆虫神经肽sNPF的功能。此外，该研究完善了桔小实蝇神经肽信号系统以及它们在温度适应性中的作用，有助于更好的解释其在世界各地的快速入侵。

Abstract

Neuropeptides and their receptors are involved in the regulation and coordination of various physiological processes in insects. Although various neuropeptides have been identified previously, the corresponding receptors remain unknown in the oriental fruit fly, Bactrocera dorsalis, an important agricultural insect pest. It is also unclear whether neuropeptide signaling systems are involved in regulating the thermal tolerance of this notorious pest. Here, we systematically identified 44 putative neuropeptide receptor genes which encode 66 protein sequences, and analyzed the spatio-temporal expression patterns of the neuropeptide ligands and their receptor genes in B. dorsalis. We also analyzed changes in their transcript accumulation in two thermo-tolerant populations (heat and cold) of B. dorsalis. The results showed that numerous neuropeptides and receptors participate in responding to thermal stresses during acclimation. In particular, the expression of short neuropeptide F (sNPF) was up-regulated in the heat-tolerant population of B. dorsalis. Moreover, proteomic data showed that sNPF was up-regulated in both thermo-tolerant populations of B. dorsalis. The functional verification based on CRISPR/Cas9 demonstrated that sNPF is involved in regulating the tolerance to thermal stresses. The results of this study enrich our knowledge on the function of neuropeptide sNPF in insects. Moreover, this study demonstrated the role of neuropeptide signaling systems in thermal adaptation, contributing to a better understanding of the rapid invasiveness of B. dorsalis around the world.

Keywords: Bactrocera dorsalis neuropeptide receptors sNPF thermal adaptation CRISPR/Cas9

Received: 08 December 2023 Accepted: 04 March 2024

Fund:

This study was supported by funding from the National Natural Science Foundation of China (U21A20222 and 32072491), the National Key R&D Program of China (2022YFC2601000), the 111 Project, China (B18044) and the earmarked fund for China Agriculture Research System (CARS-26).

About author: #Correspondence Hongbo Jiang, E-mail: jhb8342@swu.edu.cn; Jinjun Wang, E-mail: wangjinjun@swu.edu.cn * These authors contributed equally to this study.

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Yang Yang, Hongfei Li, Changhao Liang, Donghai He, Hang Zhao, Hongbo Jiang, Jinjun Wang. 2024. Neuropeptide signaling systems are involved in regulating thermal tolerance in the oriental fruit fly. Journal of Integrative Agriculture, 23(12): 4147-4160.

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