Data from: A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore

Host plant chemical composition critically shapes the performance of insect herbivores feeding on them. Some insects have become specialized on plant secondary metabolites, and even use them to their own advantage such as defense against predators. However, infection by plant pathogens can seriously alter the interaction between herbivores and their host plants. We tested whether the effects of the plant secondary metabolites, iridoid glycosides (IGs), on the performance and immune response of an insect herbivore are modulated by a plant pathogen. We used the IG-specialized Glanville fritillary butterfly (Melitaea cinxia), its host plant Plantago lanceolata, and the naturally occurring plant pathogen, powdery mildew (Phodosphaera plantaginis), as model system. Pre-diapause larvae were fed on P. lanceolata host plants selected to contain either high or low IGs, in the presence or absence of powdery mildew. Larval performance was measured by growth rate, survival until diapause, and by investment in immunity. We assessed immunity after a bacterial challenge in terms of phenoloxidase (PO) activity and the expression of seven pre-selected insect immune genes (qPCR). We found that the beneficial effects of constitutive leaf IGs, that improved larval growth, were significantly reduced by mildew infection. Moreover, mildew presence downregulated one component of larval immune response (PO activity), suggesting a physiological cost of investment in immunity under suboptimal conditions. Yet, feeding on mildew infected leaves caused an upregulation of two immune genes, lysozyme and prophenoloxidase. Our findings indicate that a plant pathogen can significantly modulate the effects of secondary metabolites on the growth of an insect herbivore. Furthermore, we show that a plant pathogen can induce contrasting effects on insect immune function. We suspect that the activation of the immune system toward a plant pathogen infection may be maladaptive, but the actual infectivity on the larvae should be tested.宿主植物的化学成分对取食它们的植食性昆虫的生长表现具有关键调控作用。部分昆虫已特化适应植物次生代谢物，甚至能利用这些物质实现自身获益，例如抵御天敌。然而，植物病原菌侵染会严重改变植食性昆虫与其宿主植物之间的互作关系。本研究旨在探究植物次生代谢物环烯醚萜苷（iridoid glycosides, IGs）对植食性昆虫生长表现与免疫响应的影响，是否会受到植物病原菌的调控。我们以特化依赖IGs的格纹蛱蝶（Melitaea cinxia）、其宿主植物长叶车前（Plantago lanceolata），以及天然存在的植物病原菌白粉病菌（Phodosphaera plantaginis）作为模式系统开展实验。将滞育前幼虫分别置于含有高、低水平IGs的长叶车前植株上饲养，同时设置存在或不存在白粉病菌侵染的处理组。通过生长速率、滞育前存活率以及免疫投入量来衡量幼虫的生长表现。在细菌攻毒试验后，以酚氧化酶（phenoloxidase, PO）活性以及7个预先筛选出的昆虫免疫基因的表达量（实时定量聚合酶链反应, qPCR检测）来评估幼虫的免疫状态。研究结果显示，能够提升幼虫生长速率的组成型叶片IGs的有益效应，会因白粉病菌的侵染而显著减弱。此外，白粉病菌的存在会下调幼虫免疫响应的一个组分——PO活性，这暗示在次优环境下投入免疫防御存在生理代价。但取食被白粉病菌侵染的叶片，会使两个免疫基因（溶菌酶与酚氧化酶原）的表达量上调。我们的研究结果表明，植物病原菌能够显著调控次生代谢物对植食性昆虫生长的影响。此外，本研究还显示植物病原菌可对昆虫免疫功能产生截然不同的调控效应。我们推测，针对植物病原菌侵染激活免疫系统可能存在适应不良性，但需进一步开展实验验证幼虫实际受侵染的情况。