Comparative plant transcriptome profiling of Arabidopsis and Camelina infested withMyzus persicaeaphids acquiring circulative and non-circulative viruses reveals virus- and plant-specific alterations relevant to aphid feeding behavior and transmission

Abstract

Background: Evidence accumulates that plant viruses alter host-plant traits in ways that modify their insect vectors' behavior. These alterations often enhance virus transmission, which has led to the hypothesis that these effects are manipulations caused by viral adaptation. However, the genetic basis of these indirect, plant-mediated effects on vectors and their dependence on the plant host and the mode of virus transmission is hardly known. Results: Transcriptome profiling of Arabidopsis thaliana and Camelina sativa plants infected with turnip yellows virus (TuYV) or cauliflower mosaic virus (CaMV) and infested with the common aphid vector Myzus persicae revealed strong virus- and host-specific differences in the gene expression patterns. CaMV infection caused more severe effects on the phenotype of both plant hosts than did TuYV infection, and the severity of symptoms correlated strongly with the proportion of differentially expressed genes, especially photosynthesis genes. Accordingly, CaMV infection modified aphid behavior and fecundity stronger than did infection with TuYV. Conclusions: Overall, infection with CaMV — relying on the non-circulative transmission mode — tends to have effects on metabolic pathways with strong potential implications for insect-vector / plant-host interactions (e.g. photosynthesis, jasmonic acid, ethylene and glucosinolate biosynthetic processes), while TuYV — using the circulative transmission mode — alters these pathways only weakly. These virus-induced deregulations of genes that are related to plant physiology and defense responses might impact aphid probing and feeding behavior on both infected host plants, with potentially distinct effects on virus transmission. Keywords: Caulimovirus, polerovirus, aphid vector, transmission, feeding behavior, insect-plant interactions, transcriptome profiling, RNA-seq.

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

“…We found that stress-related aphid genes were downregulated in Myzus on both infected plants (regardless of the virus). This suggests that both CaMV and TuYV infections facilitate the establishment of Myzus on the plants, likely by downregulating in the plants expression of genes implicated in anti-herbivore secondary metabolism such as the jasmonic acid pathway as shown in by us in the same experimental setup (Chesnais et al, 2022a). Apart from common transcriptomic changes induced by both viruses, our results indicate that there are also virus-specific gene expression changes, which might be related to the transmission mode.…”

“…This might favor aphid mobility and survival and in turn virus dispersion. Genes involved in stress responses and saliva functions were mostly downregulated (except the saliva protein ACE1 contributing to lifespan), indicating that viral infection facilitates aphid infestation of the host plants, for example by dampening anti-herbivore plant defenses as observed in our previous study (Chesnais et al, 2022a).…”

“…This is evidenced by the higher number of aphid DEGs and stronger deregulations on virus-infected Arabidopsis compared to Camelina, regardless of the virus. It is worth noting that a plant transcriptome analysis revealed a lower number of plant DEGs in Arabidopsis and Camelina infected with TuYV compared to CaMV-infected plants, suggesting a strong virus-specific effect on the two plant hosts (Chesnais et al, 2022a). Thus, the global aphid transcriptome response to plant infection by the two viruses described here does not correlate with the global plant transcriptome response to the virus infection.…”

“…stress-related genes (Table 1). Previously, we demonstrated that plant infection with CaMV and TuYV alters primary and secondary metabolism in Arabidopsis and Camelina strongly (Chesnais et al, 2022a). Consequently, aphids could also be stressed on the infected plants because of these important alterations of the plant composition.…”