Abstract

Aphids are economically important pests that display exceptional variation in host range. The determinants of diverse aphid host ranges are not well understood, but it is likely that molecular interactions are involved. With significant progress being made towards understanding host responses upon aphid attack, the mechanisms underlying non-host resistance remain to be elucidated. Here, we investigated and compared Arabidopsis thaliana host and non-host responses to aphids at the transcriptional level using three different aphid species, Myzus persicae, Myzus cerasi and Rhopalosiphum pisum. Gene expression analyses revealed a high level of overlap in the overall gene expression changes during the host and non-host interactions with regards to the sets of genes differentially expressed and the direction of expression changes. Despite this overlap in transcriptional responses across interactions, there was a stronger repression of genes involved in metabolism and oxidative responses specifically during the host interaction with M. persicae. In addition, we identified a set of genes with opposite gene expression patterns during the host versus non-host interactions. Aphid performance assays on Arabidopsis mutants that were selected based on our transcriptome analyses identified novel genes contributing to host susceptibility, host defences during interactions with M. persicae as well to non-host resistance against R. padi. Understanding how plants respond to aphid species that differ in their ability to infest plant species, and identifying the genes and signaling pathways involved, is essential for the development of novel and durable aphid control in crop plants.

Highlights

  • Aphids are hemipteran insects that display exceptional variation in host range

  • While most aphid species are restricted to one or few host plants, some aphids can infest a wide range of plant species

  • To test whether Myzus cerasi and Rhopalosiphum padi probe the leaf surface during the interaction with Arabidopsis we assessed leaves challenged with these aphid species as well as Myzus persicae for the presence of autofluorescence, indicative of damaged epidermal cells

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Summary

Introduction

Aphids are hemipteran insects that display exceptional variation in host range. While some aphid species, such as Myzus persicae (green peach aphid), are able to infest plants in over 40 families, including many important crops, closely related Myzus cerasi (black cherry aphid) is only able to infest a limited number of hosts within one or two plant families [1]. It has been reported that aphids exhibit probing behavior regardless of the plant species they land on, and regardless of host suitability [3,4,5,6]. It has been suggested that aphids have increased probing rates in nonhost interactions, which explains the higher virus transmission rates by aphids reported on non-host plant species [2]. These observations imply that there is an opportunity for molecular interactions to take place during both aphid-host and non-host interactions. Perhaps as a results of these molecular interactions, aphids are either unable to reach the phloem or unable to successfully feed from the phloem of non-host plants

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