Transcriptome responses of the aphid vectorMyzus persicaeare shaped by identities of the host plant and the virus

Abstract

Background: Numerous studies document modifications in vector orientation behavior, settling and feeding behavior, and/or performance due to virus infection in host plants. These alterations are often expected to enhance virus transmission, which has led to the hypothesis that such effects are manipulations caused by virus adaptations. However, until now, the genetic basis of these effects on vectors that can be direct (effects that occur following acquisition and retention of virions) or indirect (plant-mediated effects) are mostly unknown. Results: Transcriptome profiling of Myzus persicae aphids feeding on turnip yellows virus (TuYV) and cauliflower mosaic virus (CaMV) infected Arabidopsis thaliana and Camelina sativa revealed a substantial proportion of commonly deregulated genes, revealing general players in plant-virus-aphid interactions. We identified also aphid genes specifically deregulated by CaMV or TuYV infection, which might be related to the viral transmission mode. Furthermore, we observed strong host-specific differences in the gene expression patterns with plant virus infection causing more deregulations of aphid genes on Arabidopsis than on Camelina, likely related to the differences in susceptibility of the plant hosts to these viruses. Finally, stress-related aphid genes were downregulated in Myzus on both infected plants, regardless of the virus. Conclusions: TuYV - relying on the circulative persistent mode of transmission - tends to affect developmental genes, which could increase the proportion of alate aphids in TuYV viruliferous aphids, but also contribute to their locomotion, neuronal activity, and lifespan, while CaMV - using the non-circulative non-persistent mode of transmission - had a strong impact on feeding-related genes and in particular those related to salivary proteins. In general, these transcriptome alterations target pathways that seem to be particularly adapted to the transmission mode of the corresponding virus and could be evidence of manipulation caused by viral adaptation. Keywords: Caulimovirus, polerovirus, aphid vector, insect-plant interactions, transmission, transcriptome profiling, RNA-seq

A Review of Interactions between Plants and Whitefly-Transmitted Begomoviruses

“…Additionally, the Janus kinase/signal transducer and activator of transcription (JAK/STAT) signaling pathway plays a role in balancing vector fitness and virus transmission, with the virus inhibiting the pathway, while the vector protects itself through it [3]. Furthermore, virus infection can alter vector orientation behavior, settling and feeding behavior, fecundity, and survival, potentially enhancing virus transmission [57,58]. Moreover, the pre-infestation of plants by vector or non-vector insects can affect subsequent viral transmission and infection, with different insect mouthparts activating different plant signaling pathways that impact virus replication and movement [59].…”