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Tomato-Potato Aphid Interactions: Insights into Plant Defense and the Aphid Pest

Abstract

Aphids cause extensive economic losses to cultivated crops worldwide. Their success as pests is in part due to their complex life cycle, wide host range, and the ability of a female aphid to contain not only the developing embryos of her daughters, but also those of her grand-daughters which develop within her daughters. The latter results in build up of immense populations very quickly. Resistant plants represent an environmental friendly approach to combat aphid pests. Better understanding of plant-aphid interaction will contribute to engineering durable plant resistance. In tomato (Solanum lycopersicum), the Mi-1 gene confers resistance to potato aphid (Macrosiphum euphorbiae), root-knot nematode (RKN) (Meloidogyne sp.), whitefly (Bemisia tabaci), and tomato psyllid (Bactericera cockerelli). This incompatible tomato interaction with RKN is characterized by hypersensitive response and vast transcriptional reprogramming, including differential regulation of transcription factors (TFs). Using gene knock-down approach in Chapter one, a role for SlWRKY70 TF was identified in Mi-1-mediated tomato resistance against potato aphid and RKN. Gene expression analysis showed that the regulation of this TF by Salicylic acid and Jasmonic acid hormones is conserved between tomato and Arabidopsis thaliana. The study of SlWRKY70 revealed that there is no consistent nomenclature for plant WRKY TF family. For this reason a phylogenetic analysis was conducted using sequences from 15 plant species. Chapter two presents the analysis and the established orthologous relationship of WRKY TFs among these plant species. Consequently, this analysis allowed the design of a systemic nomenclature for the WRKY TF family to include the inferred orthology relationships. Chapters three and four pursued another approach to understand plant-aphid interactions. These chapters focused on identifying the aphid effectors and putative lineage-specific set of genes through sequencing the aphid and its salivary gland transcriptomes. In Chapter three sequencing and annotation of the potato aphid transcriptome enabled us to conduct comparative sequence analysis with three other aphid species, as well as seven additional species of insects from different clades and a planktonic crustacean. This analysis identified a set of aphid-specific genes, which may contribute to aphid's unconventional biology. The transcripts of a subset of these aphid-specific genes were expressed in the salivary glands suggesting that they are involved in aphid-host interactions. To study this interaction in more detail, the potato aphid salivary gland transcriptome was sequenced in Chapter four. This enabled identification of secreted proteins based on prediction of secretion signal peptides. In planta functional characterization of eight of these putative aphid secreted proteins identified roles for two, Me10 and Me23, in altering tomato responses to the aphid's advantage.

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