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Journal of Integrative Agriculture  2024, Vol. 23 Issue (04): 1285-1299    DOI: 10.1016/j.jia.2023.10.022
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Development and formation of wing cuticle based on transcriptomic analysis in Locusta migratoria during metamorphosis

Jing Zhang1, 2, Zhaochen Wu1, 2, Shuo Li2, He Huang2, Suning Liu3, Weimin Liu1, Xiaoming Zhao1#, Jianzhen Zhang1#

1Shanxi Key Laboratory of Nucleic Acid Biopesticides, Institute of Applied Biology, Shanxi University, Taiyuan 030006, China

2 College of Life Science, Shanxi University, Taiyuan 030006, China

3 Guangmeiyuan R&D Center/Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, South China Normal University, Meizhou 514779, China

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摘要  

翅是昆虫重要的飞行器官。翅的发育是一个由一系列基因控制的复杂过程。在若虫到成虫的蜕变过程中,无飞行功能的翅芽转变为具有迁徙飞行功能的成熟。然而,飞蝗翅形态发生的机制尚不清楚。本研究对飞蝗羽化前和羽化后翅的微观结构进行了分析,并进行了比较转录组分析。RNA-seq鉴定出25,334Unigenes,其中有3,430个差异表达基因(Differentially Expressed Genes, DEGs)包括1,907个上调基因和1,523个下调基因DEGs主要包括表皮发育相关基因(LmACPs)、几丁质代谢相关基因(LmIdgf4)、脂质代谢相关基因、细胞粘附基因(Integrin)、锌指转录因子编码基因(LmSalmLmZF593LmZF521)等。基于RNA干扰和H&E染色的功能分析表明,这3个编码锌指转录因子的基因对飞蝗翅表皮的形成和形态维持至关重要。最后,研究发现LmSalm在羽化前调控翅芽LmACPs的表达,LmZF593LmZF521调控羽化后翅中LmIntegrin/LmIdgf4/LmHMT420的表达。本研究揭示了飞蝗若虫期和成虫期控制翅形态的分子调控轴,为研究不完全变态昆虫翅发育机制提供了理论依据。



Abstract  

Wings are an important flight organ of insects.  Wing development is a complex process controlled by a series of genes.  The flightless wing pad transforms into a mature wing with the function of migratory flight during the nymph-to-adult metamorphosis.  However, the mechanism of wing morphogenesis in locusts is still unclear.  This study analyzed the microstructures of the locust wing pads at pre-eclosion and the wings after eclosion and performed the comparative transcriptome analysis.  RNA-seq identified 25,334 unigenes  and 3,430 differentially expressed genes (DEGs) (1,907 up-regulated and 1,523 down-regulated).  The DEGs mainly included cuticle development (LmACPs), chitin metabolism (LmIdgf4), lipid metabolism-related genes, cell adhesion (Integrin), zinc finger transcription factors (LmSalm, LmZF593 and LmZF521), and others.  Functional analysis based on RNA interference and hematoxylin and eosin (H&E) staining showed that the three genes encoded zinc finger transcription factors are essential for forming wing cuticle and maintaining morphology in Locusta migratoria.  Finally, the study found that the LmSalm regulates the expression of LmACPs in the wing pads at pre-eclosion, and LmZF593 and LmZF521 regulate the expression of LmIntegrin/LmIdgf4/LmHMT420 in the wings after eclosion.  This study revealed that the molecular regulatory axis controls wing morphology in nymphal and adult stages of locusts, offering a theoretical basis for the study of wing development mechanisms in hemimetabolous insects.

Keywords:  Locusta migratoria       wing development        metamorphosis        RNA-seq
  
Received: 21 July 2023   Accepted: 28 September 2023
Fund: This work was supported by the National Key R&D Program of China (2022YFD1700200), the National Natural Science Foundation of China (31970469), earmarked fund for Modern Agro-industry Technology Research System, China (2023CYJSTX01-20), the Fund for Shanxi “1331 Project”, China, and the Scientific and Technological Innovation Programs of Higher Education Institutions in Shanxi, China (2022Y032).
About author:  Jing Zhang, E-mail: 1265725529@qq.com; #Correspondence Xiaoming Zhao, E-mail: zxming@sxu.edu.cn; Jianzhen Zhang, E-mail: zjz@sxu.edu.cn

Cite this article: 

Jing Zhang, Zhaochen Wu, Shuo Li, He Huang, Suning Liu, Weimin Liu, Xiaoming Zhao, Jianzhen Zhang. 2024.

Development and formation of wing cuticle based on transcriptomic analysis in Locusta migratoria during metamorphosis . Journal of Integrative Agriculture, 23(04): 1285-1299.

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