Abstract
Herbivory affects subsequent herbivores, mainly regulated by the phytohormones jasmonic (JA) and salicylic acid (SA). Additionally, organisms such as soil microbes belowground or parasitoids that develop inside their herbivorous hosts aboveground, can change plant responses to herbivory. However, it is not yet well known how organisms of trophic levels other than herbivores, below- and above-ground, alter the interactions between insect species sharing a host plant. Here, we investigated whether the parasitoid Aphidius colemani and different soil microbial communities (created through plant-soil feedbacks) affect the JA and SA signalling pathways in response to the aphid Myzus persicae and the thrips Frankliniella occidentalis, as well as subsequent thrips performance. Our results show that the expression of the JA-responsive gene CaPINII in sweet pepper was more suppressed by aphids than by parasitised aphids. However, parasitism did not affect the expression of CaPAL1, a biosynthetic gene of SA. Furthermore, aphid feeding enhanced thrips performance compared with uninfested plants, but this was not observed when aphids were parasitised. Soils where different plant species were previously grown, did not affect plant responses or the interaction between herbivores. Our study shows that members of the third trophic level can modify herbivore interactions by altering plant physiology.
Highlights
Plants have evolved sophisticated strategies to defend themselves against pathogens and herbivorous insects
The concept of plant-soil feedbacks” (PSF) can be applied to create distinct soil microbiomes by growing different plant species in a given soil, which results in different effects on above-ground herbivores that feed on plants that are subsequently grown in these soils[26,30]
In order to thest these hypothesis, we addressed two main research questions: (i) Does parasitism of aphids or PSF influence the induction of marker genes of the JA and salicylic acid (SA) defensive signalling pathways in pepper plants?; (ii) Do these effects of PSF and/or parasitism on plant responses affect the later performance of F. occidentalis? By using a model system of agricultural interest we highlight the potential relevance of parasitism at modulating plant responses to aphids and their interaction with thrips
Summary
Plants have evolved sophisticated strategies to defend themselves against pathogens and herbivorous insects. Maranello (sweet pepper), the phloem feeding aphid Myzus persicae (Sulzer, 1776) (Sternorrhyncha, Aphididae), which is commonly used as a model of SA-inducer, and the cell content feeding thrips Frankliniella occidentalis (Pergande, 1895) (Thysanoptera, Tripidae), which is known to induce and be sensitive to JA-regulated defences in Arabidopsis and tomato[31,32,33,34]. Both aphids and thrips, are generalist insects and major pests in sweet pepper plants, and in many other crops worldwide. At the third trophic level, we used the parasitoid Aphidius colemani (Dalman, 1820) (Hymenoptera, Braconidae), parasitising the aphid M. persicae, in the described plant-herbivore system
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