Plant-herbivore interactions are often mediated by plant microorganisms, and the "defensive mutualism" of epichloid fungal endophytes of grasses is an example. These endophytes synthesize bioactive alkaloids that generally have detrimental effects on the performance of insect herbivores, but the underlying mechanisms are not well understood. Our objective was to determine whether changes in the physiology and/or behavior of aphids explain the changes in performance of insects feeding on endophytic plants. We studied the interaction between the aphid Rhopalosiphum padi and the annual ryegrass Lolium multiflorum symbiotic (E+) or not symbiotic (E-) with the fungus Epichloë occultans that can synthesize loline alkaloids. We hypothesized that aphids feeding on E+ plants have higher energetic demands for detoxification of fungal alkaloids, thereby negatively impacting the individual performance, population growth, and structure. Aphids growing on E+ plants had lower values in morphometric and functional variables of individual performance, displayed lower birth rate, smaller population size, and dramatic structural changes. However, aphids exhibited lower values of standard metabolic rate (SMR) on E+ plants, which suggests no high costs of detoxification. Behavioral variables during the first 8 h of feeding showed that aphids did not change the phloem sap ingestion with the presence of fungal endophytes. We hypothesize that aphids may maintain phloem sap ingestion according to their fungal alkaloid tolerance capacity. In other words, when alkaloid concentrations overcome tolerance threshold, ingestion of phloem should decrease, which may explain the observed lower values of SMR in E+ feeding aphids.
Myzus persicae Sulzer, like almost all aphids, associates with the endosymbiotic bacterium, Buchnera aphidicola. Although the accepted function of B. aphidicola is to complete the aphid diet with nutrients such as essential amino acids and vitamins, there is evidence that the bacteria may participate in the plant-insect interaction. Moreover, bacterial proteins with potential effector action on the metabolism of the host plant have been identified in the saliva of M. persicae. However, the possible involvement of B. aphidicola in relation to host plant acceptance by aphids needs further investigation. The aim of this study was to evaluate the effect that the disruption of the B. aphidicola-M. persicae symbiosis has on aphid feeding behaviour and on the expression of aphid salivary genes. The antibiotic rifampicin was administrated to adult aphids through artificial diets to disrupt the bacterial primary endosymbionts. Comparisons were made with control aphids, feeding from diet without rifampicin, as well as normal aphids fed on radish plants. Differences were found in the feeding behaviour of aposymbiotic aphids, which had delayed host acceptance and problems during stylet penetration into host plants. It was also found that B. aphidicola disruption down-regulated the expression of the Mp63 salivary protein gene. Together, these results indicate that B. aphidicola plays a role in plant-aphid interactions. The validity of the use of artificial diets in plantaphid studies is also discussed.
The green peach aphid, Myzus persicae Sulzer (Hemiptera: Aphididae) is one of the potato important pests; it is the most efficient vector of potato viruses. Myzus persicae harbors the endosymbiotic bacteria Buchnera aphidicola which supplements their diet. There is increasing evidence that B. aphidicola is involved in plant-aphid interactions and we previously demonstrated that B. aphidicola disruption (aposymbiosis) affected the probing behavior of M. persicae on radish plants, delaying host plant acceptance. In this work, we evaluated the effect of aposymbiosis on the probing behavior of M. persicae on 2 Solanum species with different compatibility with M. persicae, Solanum tuberosum (susceptible) and Solanum stoloniferum (resistant) with the electrical penetration graph technique (EPG). To disrupt B. aphidicola, rifampicin was administered to aphids through artificial diets. Aposymbiotic aphids, on both plant species, showed increased pathway activities, mechanical problems with the stylets, and delayed salivation in the phloem. The extended time in derailed stylet mechanics affected the occurrence of most other probing activities; it delayed the time to the first phloem phase and prevented ingestion from the phloem. The effect of aposymbiosis was more evident in the compatible interaction of M. persicae-S. tuberosum, than in the incompatible interaction with S. stoloniferum, which generated the M. persicae-S. tuberosum interaction to become incompatible. These results confirm that B. aphidicola is involved in the plant-aphid interaction in relation to plant acceptance, presumably through a role in stylets penetration in the plant.
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