All Aphid Effectors on DEK

In recent years it has become clear that cross-kingdom RNA plays a key role in mediating host-parasite interactions. Research on cross-kingdom RNA has mostly focused on microbial parasites and small RNAs. However, we showed in a recent publication that aphid insect pests use long non-coding RNAs (lncRNAs) as virulence factors, i.e. the peach-potato aphid/green peach aphid (GPA) Myzus persicae, which is a global pest, translocates at least one long lncRNA virulence factor, named Ya1, into divergent plant species, including crops. We show that Ya1 migrates systemically throughout these plant species and promotes GPA colonization on plants.

Aphids are sap-sucking insects that are vectors of a range of viruses and bacterial plant pathogens, and also transmit viroids, which consists of only nucleic acid without a protein coat. Our finding that aphids translocate their own nucleic acids that modulate plant processes is novel and mechanisms involved could contribute to the reasons of these sap-sucking insects being such efficient pathogen vectors.

In this proposal, we wish to further understand what the aphid nucleic acids do in plants and how they interfere with plant processes. We will focus on aphid lncRNA Ya1 and then also study at least two other aphid lncRNA virulence factors in plants. Data so far suggest that the aphid RNAs interfere with aspects of nucleus-chloroplast communications, including plant defense responses to biotic stress, that so far are still poorly understood. We will use the aphid RNAs to further dissect these processes.

We also found that the aphid Ya lncRNAs migrate away from aphid feeding site to distal locations of plants. It has been known for a while that nucleic acids, including those of aphid-transmitted viruses and viroids, migrate throughout plants, but the mechanisms involved have remained largely obscure. In this proposal, we will also use the aphid lncRNAs to better understand processes involved in long-distance migration of nucleic acids in plants.

The proposed research will focus on dissecting fundamental plant processes that are likely to play important roles in the ability of aphids to colonize plants and the efficiency of virus/viroid transmission by these insects. In the longer term, we anticipate that this research project will provide the basis for future research that is focused on identification of benign methods to manage outbreaks of aphids and aphid-transmitted pathogens in crops.

The long-term goal of research in the Hogenhout lab is to identify key processes in plant-microbe and plant-insect interactions that enable pathogens and insects to colonize plants. The objective of this project is to further dissect the role of aphid lncRNAs, and specifically Ya genes, in aphid-plant interactions. The proposed research is based on a recent publication (Chen et al., 2020. PNAS) showing that the peach-potato aphid/green peach aphid (GPA) Myzus persicae translocates the Ya1 long non-coding RNA (lncRNA) into plants and that this lncRNA migrates systemically and promotes aphid fecundity. In this project we want to further investigate if GPA Ya1 and other Ya lncRNA form complexes with another GPA effector, MpC002. Moreover, we will investigate if MpC002-Ya complexes interact with plant non-histone DNA-binding chromatin factors and interfere with the splicing of specific transcripts leading to altered JA, SA signaling and nucleus-chloroplast communications and promotion of aphid colonization. Finally, we will investigate whether MpC002 and Ya lncRNAs migrate as complexes via interactions with specific plant proteins. The proposed work will improve our knowledge of (i) the functions of cross-kingdom RNAs; (ii) molecular aspects that mediate plant-insect interactions, (iii) the functions of plant DEK proteins in mRNA splicing and regulation of plant defence, and (iv) mechanisms involved in systemic spread of RNA-protein complexes in plants. All these areas involve basic biological processes that are not yet well understood. We anticipate that, in the long term, the research will contribute to translational/applied science projects. To make sure we maximize opportunities for impact, we will build on our existing network and experience in translational science projects to plan regular meetings with (current) industrial collaborators, and engage with stakeholders, (under)graduate students, and the (inter)national research community.