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其组织的植食性昆虫的生存表现具有关键性调控作用。部分昆虫已演化出对植物次生代谢物的专食适应性，甚至可利用此类物质实现自身获益，比如抵御天敌。然而，植物病原菌侵染会显著改变植食性昆虫与宿主植物间的互作关系。本研究旨在探究植物次生代谢物——环烯醚萜苷（iridoid glycosides, IGs）对植食性昆虫生存表现与免疫应答的调控作用，是否会受到植物病原菌的影响。本研究以专食环烯醚萜苷的格纹蛱蝶（*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——白粉菌（*Phodosphaera plantaginis*）为研究模型。实验将预滞育期幼虫分别饲养于携带高、低水平环烯醚萜苷的长叶车前植株上，同时设置白粉菌侵染与未侵染两组处理。幼虫的生存表现通过生长速率、滞育前存活率以及免疫投资水平进行评估。本研究通过细菌攻毒后的酚氧化酶（phenoloxidase, PO）活性，以及7个预先筛选的昆虫免疫基因的定量PCR（qPCR）表达量，来评估幼虫的免疫状态。实验结果显示，本底表达的叶片环烯醚萜苷可促进幼虫生长，但其有益效应会因白粉菌侵染而显著削弱。此外，白粉菌侵染会下调幼虫免疫应答的一个组分——酚氧化酶活性，这表明在非最优环境下，昆虫的免疫投资会产生生理代价。但取食白粉菌侵染的叶片则会上调两种免疫基因的表达：溶菌酶（lysozyme）与酚氧化酶原（prophenoloxidase）。本研究结果表明，植物病原菌可显著调控次生代谢物对植食性昆虫生长的影响。此外，本研究证实植物病原菌可对昆虫免疫功能产生截然相反的调控效应。我们推测，昆虫针对植物病原菌侵染激活免疫系统的行为可能并不具有适应性，但该病原菌对幼虫的实际侵染性仍需进一步实验验证。