Differential gene expression in aphids following virus acquisition from plants or from an artificial medium

Abstract

Background: Poleroviruses, such as turnip yellows virus (TuYV), are plant viruses strictly transmitted by aphids in a persistent and circulative manner. Acquisition of either virus particles or plant material altered by virus infection is expected to induce gene expression deregulation in aphids which may ultimately alter their behavior.

Results: By conducting an RNA-Seq analysis on viruliferous aphids fed either on TuYV-infected plants or on an artificial medium containing purified virus particles, we identified several hundreds of genes deregulated in Myzus persicae, despite non-replication of the virus in the vector. Only a few genes linked to receptor activities and/or vesicular transport were common between the two modes of acquisition with, however, a low level of deregulation. Behavioral studies on aphids after virus acquisition showed that M. persicae locomotion behavior was affected by feeding on TuYV-infected plants, but not by feeding on the artificial medium containing the purified virus particles. Consistent with this, genes potentially involved in aphid behavior were deregulated in aphids fed on infected plants, but not on the artificial medium.

Conclusions: These data show that TuYV particles acquisition alone is associated with a moderate deregulation of a few genes, while higher gene deregulation is associated with aphid ingestion of phloem from TuYV-infected plants. Our data are also in favor of a major role of infected plant components on aphid behavior.

Keywords: Myzus persicae; Polerovirus; RNA-Seq; Vector behavior.

Fig. 1

Venn diagrams of differentially expressed genes (DEGs) in Myzus persicae fed 48 h on TuYV-infected plants or on an artificial medium containing purified TuYV particles. Number of genes deregulated with an FDR ≤ 0.05. a Venn diagram for DESeq2 analysis; b Venn diagram for NOISeq analysis. In red: up-regulated or common up-regulated genes; in green: down-regulated or common down-regulated genes; in yellow: contra-regulated genes (up-regulated genes in one group and down-regulated in the other group)

Fig. 2

Comparison of gene expression analyzed by RNA-Seq or RT-qPCR. Genes are referred to as their annotation on the M. persicae genome. Genes encoding Unknown protein_1, Cytochrome P450-like protein and ACYPI007976 protein were down-regulated genes, and genes encoding the ACYPI45293, Cuticular protein SD and an unknown protein_2 were up-regulated genes in viruliferous vs non-viruliferous aphids. Gene ID, RNA-Seq data, primers used in the RT-qPCR experiments and mean expression of the gene are shown in Additional file 1. Data are presented as the log2 of the ratio: mean expression in viruliferous aphids/mean expression in non-viruliferous aphids

Fig. 3

Significant Gene Ontology (GO) categories of biological processes (BP) among the deregulated genes identified by the NOISeq analysis in the aphid M. persicae following feeding on TuYV-infected or non-infected plants. The percentage of deregulated genes from the total number of genes included in each GO category is indicated on the horizontal axis (% DE); counts: number of genes differentially expressed in the GO term. GO term boxed in blue represents categories potentially implicated in virus uptake and intracellular transport and GO term boxed in red categories potentially involved in aphid behavior and signal perception

Fig. 4

Locomotor activity (number of spatial zones crossed) of viruliferous and non-viruliferous M. persicae fed on plants or on artificial medium. Box plots show median (line), 25–75% percentiles (box) and 10–90% percentiles (whisker). Letters indicate significant differences between aphid status with the GLM followed by multiple comparisons; p-value < 0.05