Viral Infection Induces Changes to the Metabolome, Immune Response and Development of a Generalist Insect Herbivore.

IF 2.2 3区 环境科学与生态学 Q4 BIOCHEMISTRY & MOLECULAR BIOLOGY
Journal of Chemical Ecology Pub Date : 2024-04-01 Epub Date: 2024-02-14 DOI:10.1007/s10886-024-01472-3
Marilia Elias Gallon, Nadya Dougherty Muchoney, Angela Marie Smilanich
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Abstract

Host plant consumption and pathogen infection commonly influence insect traits related to development and immunity, which are ultimately reflected in the behavior and physiology of the insect. Herein, we explored changes in the metabolome of a generalist insect herbivore, Vanessa cardui (Lepidoptera: Nymphalidae), in response to both dietary variation and pathogen infection in order to gain insight into tritrophic interactions for insect metabolism and immunity. Caterpillars were reared on two different host plants, Plantago lanceolata (Plantaginaceae) and Taraxacum officinale (Asteraceae) and subjected to a viral infection by Junonia coenia densovirus (JcDV), along with assays to determine the insect immune response and development. Richness and diversity of plant and caterpillar metabolites were evaluated using a liquid chromatography-mass spectrometry approach and showed that viral infection induced changes to the chemical content of V. cardui hemolymph and frass dependent upon host plant consumption. Overall, the immune response as measured by phenoloxidase (PO) enzymatic activity was higher in individuals feeding on P. lanceolata compared with those feeding on T. officinale. Additionally, infection with JcDV caused suppression of PO activity, which was not host plant dependent. We conclude that viral infection combined with host plant consumption creates a unique chemical environment, particularly within the insect hemolymph. Whether and how these metabolites contribute to defense against viral infection is an open question in chemical ecology.

Abstract Image

病毒感染诱导综合食草昆虫的代谢组、免疫反应和发育发生变化
寄主植物的消耗和病原体的感染通常会影响昆虫与发育和免疫有关的性状,这些性状最终会反映在昆虫的行为和生理上。在此,我们探讨了食草昆虫Vanessa cardui(鳞翅目:蛱蝶科)的代谢组对食物变化和病原体感染的响应变化,以深入了解昆虫代谢和免疫的三营养相互作用。毛虫在两种不同的寄主植物(车前子(Plantaginaceae)和蒲公英(Asteraceae))上饲养,并受到Junonia coenia densovirus(JcDV)的病毒感染,同时进行昆虫免疫反应和发育测定。采用液相色谱-质谱法评估了植物和毛虫代谢物的丰富性和多样性,结果表明病毒感染会导致V. cardui血淋巴和胎粪中的化学成分发生变化,这取决于寄主植物的消耗量。总体而言,以酚氧化酶(PO)酶活性衡量的免疫反应在摄食 P. lanceolata 的个体中高于摄食 T. officinale 的个体。此外,感染 JcDV 会抑制 PO 活性,这与寄主植物无关。我们的结论是,病毒感染与宿主植物消耗相结合会产生一种独特的化学环境,尤其是在昆虫血淋巴中。这些代谢物是否有助于抵御病毒感染以及如何抵御病毒感染是化学生态学中的一个未决问题。
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来源期刊
Journal of Chemical Ecology
Journal of Chemical Ecology 环境科学-生化与分子生物学
CiteScore
5.10
自引率
4.30%
发文量
58
审稿时长
4 months
期刊介绍: Journal of Chemical Ecology is devoted to promoting an ecological understanding of the origin, function, and significance of natural chemicals that mediate interactions within and between organisms. Such relationships, often adaptively important, comprise the oldest of communication systems in terrestrial and aquatic environments. With recent advances in methodology for elucidating structures of the chemical compounds involved, a strong interdisciplinary association has developed between chemists and biologists which should accelerate understanding of these interactions in nature. Scientific contributions, including review articles, are welcome from either members or nonmembers of the International Society of Chemical Ecology. Manuscripts must be in English and may include original research in biological and/or chemical aspects of chemical ecology. They may include substantive observations of interactions in nature, the elucidation of the chemical compounds involved, the mechanisms of their production and reception, and the translation of such basic information into survey and control protocols. Sufficient biological and chemical detail should be given to substantiate conclusions and to permit results to be evaluated and reproduced.
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