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Molecular determinants of aphid host range

Final Report Summary - APHIDHOST (Molecular determinants of aphid host range)

Aphids are phloem-feeding insects that cause feeding damage and transmit economically important plant viruses to many crops worldwide. Many aphid species are restricted to one or few host plants, while some aphids, many of which are of agricultural importance, can infest a wide range of plant species. An important observation is that aphids spend a considerable time on nonhost species, where they probe the leaf tissue and secrete saliva, but for unknown reasons are unable to ingest phloem sap. These findings suggest that aphids, like plant pathogens, interact with nonhost plants at the molecular level, but potentially are not successful in suppressing plant defences and/or releasing nutrients. Moreover, aphids secreted salivary proteins (effectors) inside host plants that promote susceptibility, but the underlying mechanisms of this remain to be elucidated. The overall aim of the proposed project was to gain insight into the level of cellular host reprogramming that takes place during aphid-host interactions, the cellular processes involved in aphid nonhost resistance, and the role of aphid effectors in determining host range. For this purpose we compared interactions of three economically important aphid species, Myzus persicae (green peach aphid), Myzus cerasi and Rhopalosiphum padi (bird cherry oat aphid), with host and nonhost plants.

Our key findings are:
We generated an overview of plant transcriptional responses to host and non-host interactions with aphids, showing that plants activate immune responses. Moreover, we identified plant genes, in both model and crop plants, with novel roles in host susceptibility and nonhost resistance to aphid pests. Also, our data suggests that nonhost resistance to aphids is complex and involves multiple genes. A further understanding of how these genes impact plant-aphid interactions promises to facilitate crop improvement strategies that protect against infestations.
Aphid gene expression analyses revealed a rather limited transcriptional response when insects were exposed to different plant species and artificial diet. It is possible that aphids do not strongly respond to host versus nonhost plant species. Alternatively, transcriptional responses may occur in specific aphid tissues only, and therefore have been missed in our analyses, which was based on sampling whole aphids.
A combined genomics approach identified an aphid effector pair conserved across different aphid genomes, and tight co-regulation of this pair with a superset of aphid genes, many of which encode effectors. These findings point to a shared control mechanism regulating aphid parasitism genes. Characterization of this mechanism and the regulators involved could unveil novel targets for insecticides development.
We have contributed to the identification of novel candidate effectors from three different aphid species, M. persicae, M. cerasi and R. padi, by using a combination of transcriptomics and saliva proteomics approaches, and used subsequent comparative analyses to identify core and putative species-specific effector-sets in these aphid species. We ectopically expressed a select set of aphid effectors in different plant species and found that several of these proteins enhanced host susceptibility in a species-specific manner. Therefore, aphid effectors likely contribute to and aphid species host range.
In our bid to attribute function to an increasing number of these candidate effectors, the identification of their cellular host targets represents a critical step. We showed, for the first time, that an aphid effector interacts with a host plant protein to promote susceptibility to aphids, thereby allowing extension of the effector paradigm into the plant-aphid interactions field. Importantly, we showed that the effector-host protein interaction is highly specific to the aphid species and its hosts, and likely shaped by plant-aphid co-evolution. We are now well positioned to further explore how aphid effectors promote plant susceptibility, by functionally characterizing the host plant proteins and processes perturbed by aphids. Exploring how to interfere with aphid-mediated susceptibility in future research will inform us on potential novel approaches (knowledge-based breeding/synthetic resistance) to protect crops against aphid infestations.