Cucini Claudio, Funari Rebecca, Marturano Giovanni, Cardaioli Elena, Marianelli Leonardo, Paoli Francesco, Carapelli Antonio, Frati Francesco, Nardi Francesco
Department of Life Sciences, University of Siena, Siena, Italy.
National Biodiversity Future Center (NBFC), Palermo, Italy.
BMC Genomics. 2025 Sep 1;26(1):788. doi: 10.1186/s12864-025-11949-4.
The Japanese beetle Popillia japonica is an invasive pest that is creating a major concern due to its spread and damaging potential. Native to Japan, it was introduced in the U.S.A. and the Azores during the twentieth century, and in mainland Europe in 2014. P. japonica is able to attack more than 400 plant species, including some of high economic importance, and the possible losses related to uncontrolled expansion in Europe are substantial. Numerous control measures are being developed to control this pest, with a specific focus on Integrated Pest Management and environmentally safe strategies. Aiming for a genetically informed optimization of the design of these control methods, we studied the gene expression response of the pest following exposure to three different treatments: deltamethrin-coated long lasting insecticidal nets, Bacillus thuringiensis and Metarhizium robertsii spores.
The treatment with insecticidal nets resulted in the differential expression of genes related to Ca transport and CYP-based detoxification. Exposure to B. thuringiensis was associated with enrichment of gene ontology terms related to antimicrobial peptides and immune function, which suggested potential modulation of immune-related processes. Treatment with M. robertsii led to the production of antifungal peptides as well as an up-regulation of the Toll and MAPK pathways.
These findings can be variously interpreted as a response of the insect to minimize the effects of the treatment at the molecular level (e.g. Ca increase), as a direct attempt of the insect to combat the agent (e.g. antimicrobial peptides), or as part of a more complex interplay between the insect and the biological control agent (e.g. modulation of the immune system). In general terms, the response to the insecticidal nets and, partly, to B. thuringiensis, appears to arise from a direct interaction of the insecticide molecule, or toxin, with their targets at the molecular level. On the other hand, multiple gene pathways are modulated in the response to M. robertsii, suggesting a more diversified mode of action that impacts a broader spectrum of biological mechanisms, in line with the notion that the fungus actually grows and reproduces inside the insect host.
日本丽金龟（Popillia japonica）是一种入侵性害虫，因其传播范围和潜在破坏力而备受关注。它原产于日本，20世纪被引入美国和亚速尔群岛，2014年进入欧洲大陆。日本丽金龟能够攻击400多种植物，包括一些具有高度经济重要性的植物，在欧洲，其不受控制的扩散可能造成的损失巨大。目前正在研发多种控制措施来防治这种害虫，特别侧重于综合害虫管理和环境安全策略。为了从基因层面优化这些控制方法的设计，我们研究了该害虫在接触三种不同处理后的基因表达反应：溴氰菊酯涂层长效杀虫网、苏云金芽孢杆菌和罗伯茨绿僵菌孢子。
使用杀虫网处理导致与钙转运和基于细胞色素P450的解毒相关的基因差异表达。接触苏云金芽孢杆菌与抗菌肽和免疫功能相关的基因本体术语富集有关，这表明免疫相关过程可能受到潜在调节。用罗伯茨绿僵菌处理导致抗真菌肽的产生以及Toll和丝裂原活化蛋白激酶（MAPK）途径的上调。
这些发现可以有多种解释，既可以看作是昆虫在分子水平上尽量减少处理影响的反应（例如钙增加），也可以看作是昆虫对抗病原体的直接尝试（例如抗菌肽），或者是昆虫与生物防治剂之间更复杂相互作用的一部分（例如免疫系统的调节）。总体而言，对杀虫网以及部分对苏云金芽孢杆菌的反应，似乎源于杀虫剂分子或毒素在分子水平上与其靶标的直接相互作用。另一方面，在对罗伯茨绿僵菌的反应中，多个基因途径受到调节，这表明其作用方式更加多样化，会影响更广泛的生物学机制，这与真菌实际上在昆虫宿主体内生长和繁殖的观点一致。
