Most known plant viruses are spread from plant to plant by insect vectors. There is strong evidence that non-persistently transmitted viruses manipulate the release of plant volatiles to attract insect vectors, thereby promoting virus spread. The mechanisms whereby aphid settling and feeding is altered on plants infected with these viruses, however, are unclear. Here we employed loss-of-function mutations in cucumber mosaic virus (CMV) and one of its host plants, tobacco (Nicotiana tabacum), to elucidate such mechanisms. We show that, relative to a CMVΔ2b strain with a deletion of the viral suppressor of RNAi (VSR) 2b protein in CMV, plants infected with wild-type CMV produce higher concentrations of the reactive oxygen species (ROS) H2O2 in plant tissues. Aphids on wild-type CMV-infected plants engage in shorter probes, less phloem feeding, and exhibit other changes, as detected by electrical penetration graphing technology, relative to CMVΔ2b-infected plants. Therefore, the frequency of virus acquisition and the virus load per aphid were greater on CMV-infected plants than on CMVΔ2b-infected plants. Aphids also moved away from initial feeding sites more frequently on wild-type CMV infected versus CMVΔ2b-infected plants. The role of H2O2 in eliciting these effects on aphids was corroborated using healthy plants infused with H2O2. Finally, H2O2 levels were not elevated, and aphid behavior was unchanged, on CMV-infected RbohD-silenced tobacco plants, which are deficient in the induction of ROS production. These results suggest that CMV uses its VSR protein to increase plant ROS levels, thereby enhancing its acquisition and transmission by vector insects.

Bacterial symbionts associated with insects are often involved in host development and ecological adaptation. Serratia symbiotica, a common facultative endosymbiont harbored in pea aphids, improves host fitness and heat tolerance, but studies concerning the nutritional metabolism and impact on the aphid host associated with carrying Serratia are limited. In the current study, we showed that Serratia-infected aphids had a shorter nymphal developmental time and higher body weight than Serratia-free aphids when fed on detached leaves. Genes connecting to fatty acid biosynthesis and elongation were up-regulated in Serratia-infected aphids. Specifically, elevated expression of fatty acid synthase 1 (FASN1) and diacylglycerol-o-acyltransferase 2 (DGAT2) could result in accumulation of myristic acid, palmitic acid, linoleic acid, and arachidic acid in fat bodies. Impairing fatty acid synthesis in Serratia-infected pea aphids either by a pharmacological inhibitor or through silencing FASN1 and DGAT2 expression prolonged the nymphal growth period and decreased the aphid body weight. Conversely, supplementation of myristic acid (C14:0) to these aphids restored their normal development and weight gain. Our results indicated that Serratia promoted development and growth of its aphid host through enhancing fatty acid biosynthesis. Our discovery has shed more light on nutritional effects underlying the symbiosis between aphids and facultative endosymbionts.

Interspecific interaction with host plants have important consequences for the host race formation of herbivorous insects. Plant secondary metabolites, particularly those that are involved in host races specializing on plants, warrant the theory of host specialization. Acyrthosiphon pisum comprises various host races that adapt to different Fabaceae plants, which provides an ideal system for determining the behavioral and physiological mechanisms underlying host-adaptive diversification. The current study evaluated the effects of host transfer on population fitness, feeding behavior and the transcriptome-wide gene expression of the two host races of A. pisum, one of which was originally from Medicago sativa and the other from Pisum sativum. The results showed that the Pisum host race of A. pisum had a lower population abundance and feeding efficiency than the Medicago host race in terms of a longer penetration time and shorter duration times of phloem ingestion when fed on M. sativa. In contrast, few differences were found in the population abundance and feeding behavior of A. pisum between the two host races when fed on P. sativum. Meanwhile, of the nine candidate phenolic compounds, only genistein was significantly affected by aphid infestation; higher levels of genistein were detected in M. sativa after feeding by the Pisum host race, but these levels were reduced relative to uninfested controls after feeding by the Medicago host race, which suggested that genistein may be involved in the specialization of the aphid host race on M. sativa. Further exogenous application of genistein in artificial diets showed that the increase in genistein reduced the survival rate of the Pisum host race but had little effect on that of the Medicago host race. The transcriptomic profiles indicated that the transcripts of six genes with functions related to detoxification were up-regulated in the Pisum host race relative to the Medicago host race of A. pisum. These results suggested that the inducible plant phenolics and associated metabolic process in aphids resulted in their differential adaptations to their Fabaceae host.

Plant viruses cause a range of plant diseases symptoms that are often responsible for significant crop production losses and the severity and spread of the symptoms may be affected by climate change. While the increase in anthropogenic activities has caused a critical problem of increased CO₂ levels in the atmosphere, these elevated CO₂ levels have been reported to reduce virus disease severity in some plant species. In such instances, it is not clear if the plant defense mechanisms are being enhanced or virus-mediated mechanisms to overcome plant resistance are being defeated. Additionally, a few studies have been attempted in this area to determine if reduced disease is the norm or the exception under enhanced CO₂ levels. In the present study, the effects of elevated CO₂ levels (750 ppm vs. 390 ppm) on RNAi-mediated resistance of Nicotiana tabacum against the cucumber mosaic virus (CMV), and the activity of viral suppressor of RNAi (VSR) 2b protein of CMV were evaluated. On the one hand, our results showed that elevated CO₂ decreased the transcription of dicer-like protein 2 (DCL2), DCL4, and argonaut 1 (AGO1) genes with functions related to RNAi-mediated resistance when infected by CMV, which is contradictory with the decreased CMV copy numbers under elevated CO₂. On the other hand, we found that elevated CO₂ increased the calcium concentration and expression of the calcium-binding protein rgs-CaM in tobacco plants when infected by CMV, which directly weakened the function of 2b protein, the VSR of CMV, and therefore decreased the infection efficiency of the virus and suppressed the severity of CMV in tobacco plants under elevated CO₂. This study provides molecular insights into the ecological implications underlying the development of prevention strategies against plant virus infection in the context of climate change.