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Characterizing host plant-virus-vector interactions of the potato virus Y and aphid pathosystem

Abstract

Aphid-transmitted potato virus Y (PVY) is one of the most damaging pathogens of potato worldwide. Plant virus prevalence is influenced by landscape composition, host-use patterns of vectors, and the range of capable vector species. Regarding these influences, there are important knowledge gaps that remain within the PVY-aphid pathosystem. The overall goal of this research was to better understand host-virus-vector interactions within the PVY-aphid pathosystem at multiple levels of ecological organization. There is limited information on the effect of landscape-scale crop diversity on prevalence of insect-vectored viruses. In my dissertation, I investigate how landscape composition of crops (Shannon diversity of crops, percent crop cover) affects aphid vector communities and prevalence of aphid-transmitted PVY. I conducted a two-year field study in the San Luis Valley in Colorado where I sampled aphid communities with pan traps, quantified PVY incidence in potato crops with ELISA, and determined the association with landscape variables (Shannon diversity index of crops and percent crop cover) surrounding sampling sites. Crop diversity negatively influenced aphid species richness, but positively influenced PVY incidence. The negative association of crop diversity with aphid species richness could have been due to differences in management between crops and/or increased predation/parasitization of aphids. The positive association between crop diversity and PVY is likely because PVY has a wide host range and increasing crop diversity may positively influence PVY incidence due to increased inoculum in the landscape. Additionally, there was a positive association of potato (virus host) and a negative association of barley (virus non-host) with PVY incidence. In summary, I found that crop species diversity influenced both PVY prevalence and aphid communities, and that the virus host/non-host status of crops likely modulates this effect. Aphid vectors frequently probe upon various plants within a landscape, but the host use patterns of aphid vectors has not been adequately described. It would be useful to identify plants that aphid vectors are probing upon within a landscape in order to identify 1) vector movement within a landscape and 2) potential sources of aphid-transmitted virus inoculum. I used high throughput molecular gut content analysis (GCA) to characterize plant-aphid vector associations within a major potato producing region, the San Luis Valley, CO, where aphid-transmitted potato virus Y (PVY) is a major issue for potato production. Aphids were trapped weekly with suction traps during the growing seasons of 2020 and 2021. Plant-specific DNA in 200 individual aphids representing 9 vector species of PVY (Acyrthosiphon kondoi, A. pisum, Capitophorus elaeagni, Diuraphis noxia, Hayhurstia atriplicis, Myzus persicae, Phorodon cannabis, Protaphis middletonii, and Rhopalosiphum padi) were amplified by PCR, sequenced with the PacBio sequencing platform, and sequences were identified to genus using NCBI BLASTn. I found that all species of aphid vectors probed on plant genera that are outside of their reported host ranges, with Solanum, Medicago, Populus, Brassica, and Glycine as the most frequently detected plant genera. Moreover, aphids probed on many plant genera likely to be PVY host plants. These findings provide information that is essential to develop sustainable and effective management strategies to reduce PVY spread. With the increasing acreage of hemp (Cannabis sativa L.) (Rosales: Cannabaceae) in the United States, I was interested to know whether the cannabis aphid (Phorodon cannabis Passerini) (Hemiptera: Aphididae) is a potential vector of PVY. I conducted transmission assays and used the electrical penetration graph (EPG) technique to determine whether cannabis aphids can transmit PVY to hemp (host) and potato (non-host) (Solanum tuberosum L.) (Solanales: Solanaceace). I showed, for the first time, that the cannabis aphid is an efficient vector of PVY to both hemp (96% transmission rate) and potato (91%) using cohorts of cannabis aphids. In contrast, individual aphids transmitted the virus more efficiently to hemp (63%) compared to potato (19%). During the initial 15 min of EPG recordings, aphids performed fewer intracellular punctures and spent less time performing intracellular punctures on potato compared to hemp, which may in part explain low virus transmission to potato using individual aphids. During the entire 8-hour recording, viruliferous aphids spent less time ingesting phloem compared to non-viruliferous aphids on hemp. This reduced host acceptance could potentially cause viruliferous aphids to disperse thereby increasing virus transmission. Overall, my study shows that cannabis aphid is an efficient vector of PVY and that virus infection and host plant suitability affect feeding behaviors of the cannabis aphid in ways which may increase virus transmission.

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epidemiology
landscape ecology
plant-insect interactions
hemp
aphids
plant virus

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