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Are saliva proteins key determinants of host plant specificity in the pea aphid complex?

Final Report Summary - APHISPIT (Are saliva proteins key determinants of host plant specificity in the pea aphid complex?)

Most of the herbivorous insects are specialized to feed on a few plant species and cannot feed on others. This project examines the molecular mechanisms that are involved in the process of plant specialization using the pea aphid, Acyrthosiphon pisum. A. pisum forms at least 15 biotypes that are genetically distinct and each of which is specialized to feed on one or a few legume species. Interestingly, each biotype is associated with one or a few facultative bacterial symbionts, and their involvement in host plant adaptation is speculated. In this project, we focused on the interface of plant and aphid interactions to understand the mechanisms of host specialization. We examined the functions of aphid saliva, which contains numerous proteins that might interact and manipulate plant biology.

We hypothesized that the salivary genes that have biotype specific expression patterns or biotype specific polymorphism are involved in aphid host specialization. Catalogues of A.pisum salivary proteins have been published in the past, but none of them seemed to be complete. To improve A. pisum salivary protein catalogue, we have dissected salivary glands of A. pisum reference line and conducted RNAseq. The analysis of the data identified approximately 700 candidate salivary proteins. Further analyses of the salivary gene sequences in comparison to other aphid genomes revealed that some salivary genes are under diversifying selection while others are under purifying selection and some have been multiplicated only in A. pisum. These salivary genes may be involved in the host specialization in A. pisum. We have also examined gene expression pattern of A.pisum biotypes and found that each biotype shows specific gene expression pattern. Importantly, we saw enrichment of salivary genes and chemosensory genes among the genes that show biotype specific expression patterns. In addition, our re-sequenced genome data of 11 biotypes showed that some salivary genes have biotype specific polymorphism, again supporting the hypothesis that salivary genes are involved in host plant adaptation. Based on these results, we have created the list of the candidate salivary genes that may be involved in host plant adaptation, and started functional characterization of those genes.

Strong association between each aphid biotype and specific facultative symbionts indicates involvement of the symbionts in host plant adaptation. Therefore, we examined the influence of Regiella insecticola strains on aphid fecundity but observed no clear impact. In parallel, we examined distribution of facultative symbionts in aphid organs and identified the bacteria in salivary glands of A.pisum. This indicates the possibility of the transmission of bacteria or bacterial proteins to plant; therefore, we initiated the proteomics of aphid saliva.

The outcomes from this project certainly extended our knowledge on plant-aphid-symbiont interactions at a molecular level. The knowledge on the mechanism of aphid specialization to host plants will contribute to develop new pest management strategies and to select/construct aphid resistant crops. Therefore, the results of this project might be of interest of agriculture industry.
The fellow obtained a permanent position in the host research institute and is developing the research program on plant-aphid-symbiont interactions.