MARA Key Laboratory of Surveillance and Management for Plant Quarantine Pests, College of Plant Protection, China Agricultural University, Beijing, 100193, China; Sanya Institute of China Agricultural University, Sanya, 572025, China.
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China.
Insect Biochem Mol Biol. 2024 Nov;174:104192. doi: 10.1016/j.ibmb.2024.104192. Epub 2024 Oct 12.
Climate change facilitates the rapid invasion of agricultural pests, threatening global food security. The fall armyworm Spodoptera frugiperda is a highly polyphagous migratory pest tolerant to high temperatures, allowing its proliferation in harsh thermal environments. We aimed to demonstrate mechanisms of its high-temperature tolerance, particularly transcriptional and metabolic regulation, which are poorly understood. To achieve the aim, we examined the impact and mechanism of heat events on S. frugiperda by using multiple approaches: ecological measurements, transcriptomics, metabolomics, RNAi, and CRISPR/Cas9 technology. We observed that several physiological indices (larval survival rate, larval period, pupation rate, pupal weight, eclosion rate, and average fecundity) decreased as the temperature increased, with the 32 °C treatment displaying a significant difference from the control group at 26 °C. Significantly upregulated expression of genes encoding endochitinase and chitin deacetylase was observed in the chitin-binding, extracellular region, and carbohydrate metabolic process GO terms of hemolymph, fat body, and brain, exhibiting a tissue-specific pattern. Significantly enriched pathways (e.g., cutin, suberin, and wax biosynthesis; oxidative phosphorylation and cofactor biosynthesis; diverse amino acid biosynthesis and degradation; carbon metabolism; and energy metabolism), all of which are essential for S. frugiperda larvae to tolerate temperature, were found in metabolites that were expressed differently. Successful RNA interference targeting of the three chitin-related genes reduced gene expression levels and larval survival rate. Knockout of the endochitinase gene by using the CRISPR/Cas9 system significantly reduced the relative gene expression and increased sensitivity to high-temperature exposure. On the basis of our findings, theoretical foundations for understanding the high-temperature tolerance of S. frugiperda populations and latent genetic control strategies were established.
气候变化促进了农业害虫的快速入侵，威胁着全球粮食安全。草地贪夜蛾 Spodoptera frugiperda 是一种高度多食性的迁徙性害虫，能耐受高温，使其在恶劣的热环境中繁殖。我们旨在展示其耐高温的机制，特别是转录和代谢调控，这些机制知之甚少。为了实现这一目标，我们采用了多种方法来研究热事件对 S. frugiperda 的影响和机制：生态测量、转录组学、代谢组学、RNAi 和 CRISPR/Cas9 技术。我们观察到，随着温度的升高，几个生理指标（幼虫存活率、幼虫期、化蛹率、蛹重、羽化率和平均产卵量）下降，32°C 处理与 26°C 对照组相比差异显著。在血淋巴、脂肪体和脑中，编码几丁质酶和几丁质脱乙酰酶的基因表达显著上调，在几丁质结合、细胞外区和碳水化合物代谢过程的 GO 术语中，表现出组织特异性模式。在代谢物中发现了显著富集的途径（如角质、栓质和蜡生物合成；氧化磷酸化和辅助因子生物合成；各种氨基酸生物合成和降解；碳代谢；和能量代谢），所有这些途径对于 S. frugiperda 幼虫耐受温度都是必不可少的。成功针对三个几丁质相关基因进行 RNAi 靶向，降低了基因表达水平和幼虫存活率。利用 CRISPR/Cas9 系统敲除内几丁质酶基因，显著降低了相对基因表达水平，提高了对高温暴露的敏感性。基于我们的发现，为理解 S. frugiperda 种群的耐高温性和潜在遗传控制策略奠定了理论基础。
