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Characterizing the Dual Transcriptomes of Woolly Apple Aphid, Eriosoma lanigerum (Hausmann), and its Host, Malus domestica (Borkh.), Across a Host Resistance Spectrum

Abstract

Aphids are economically important, phloem-feeding insects that can cause substantial feeding damage to crops. The mechanisms underlying plant immunity to aphids are poorly characterized, but recent advances have shown a paradigm exists in plant immune signaling during aphid and pathogen attack. To overcome plant defenses, aphids, like other plant parasites, secrete effectors to modulate host processes that can lead to suppressed immunity. Emerging models of plant immunity combined with powerful sequencing technologies allow in-depth characterization of plant immune responses to aphids. In this thesis, I focus on the transcriptomic response of plants and aphids in the early stages of infestation across a host resistance spectrum to study the genes and processes that underlie plant defense responses. Also, I identify and characterize aphid candidate effectors to reveal insect proteins important for host colonization, and further refine our hypotheses of effector-mediated susceptibility. Through a systems biology approach, this thesis investigates the molecular underpinnings mediating the interaction between the domesticated apple, Malus domestica, and the woolly apple aphid, Eriosoma lanigerum. I found plant signal transduction, primary metabolism, photophosphorylation, cell wall modification and phytohormone mediated signaling were altered by woolly apple aphid feeding, and chloroplastic-ROS production and retrograde signaling may be linked to plant resistance phenotypes. Furthermore, host genes related to gall formation, such as the upregulation of xylogen-like arabinogalactan proteins and proteins involved in cell wall loosening, suggest xylem differentiation and cell expansion occur immediately upon colonization. Salivary gland effector characterization confirmed the presence of aphid effector orthologs such as C002, Shp and Armet. Furthermore, several enzymes possibly involved in reactive oxygen species scavenging and plant cell wall degradation were also identified. Overall, the research improves our understanding of apple transcriptional responses to aphid feeding, identifies woolly apple aphid candidate effectors that likely alter host processes, and provides new hypotheses for the mechanisms of gall induction by this iconic pest of apple.

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