Tracking plant virus infections through multiple dimensions: A search for sources of nonpersistent virus vectors and reservoirs at local and regional scales

Gina M Angelella, Purdue University

Abstract

My dissertation explores the ecology of aphid-vectored viruses in Midwestern cucurbits; in particular, it focuses on identifying source populations of vectors and virus reservoirs within fields and interactions of vector aphids with land cover surrounding and within fields. Initially, I identified the most commonly occurring viruses and aphid species associated with virus infections in pumpkin fields located across Indiana. This was done by assaying cucurbit leaf tissue with multiplex-rt-PCR targeting all four aphid-vectored, nonpersistent viruses found in cucurbits (papaya ringspot virus type-W, watermelon mosaic virus type-2, zucchini yellow mosaic virus, cucumber mosaic virus) and concurrently monitoring aphid species alightment in fields throughout Indiana. Watermelon mosaic virus (WMV) was the most common infection, detected in all but one field across both years. Papaya ringspot virus (PRSV) was also detected in many fields, but not zucchini mosaic virus or cucumber mosaic virus. Therioaphis trifolii and Aphis craccivora were positively associated with PRSV, and Aphis nerii with WMV. Rhopalosiphum padi was negatively associated with WMV. No relationship between total aphid or noncolonizing species counts was found with virus infection, and an increase in total colonizing species (Aphis gossypii) trapped in fields predicted a decrease in PRSV infection. Negative relationships between aphid species alightment and virus infection in fields could result from a virus-induced reduction in pumpkin plant quality, thereby reducing abundance of a colonizing species within the field. Other virus-mediated effects in pumpkins could reduce aphid attraction to pumpkin fields as well, such as modification of the olfactory stimuli detectable by airborne aphids. I also inventoried weed species within fields and assayed samples for virus content, to investigate weed cover contributions to vector behavior or as host to virus or vector. Using land cover data from the National Land Cover Database, relationships among virus, aphids and land cover were also analyzed at spatial scales of 1–5 km distance surrounding focal pumpkin fields. A comparison among interactions within each spatial scale indicated relative predictive ability of vector-virus dynamics by surrounding land cover versus within-field weed cover, and the influential factors found at each scale. Although there was evidence for a negative interaction of vector species’ alightment with weed cover, surrounding landscape was consistently a stronger predictor of vector alightment within fields. My focus then narrowed to one aphid species, the cowpea aphid (Aphis craccivora Koch), implicated in virus spread. I collected the species from local and regional source populations (alfalfa and black locust seedlings) and used SNPs to assess their population genetics, and used these data to infer the dispersal patterns of cowpea aphids surrounding focal cucurbit fields, both identifying host-associated source populations and patterns in population structure by spatial distance. Most aphids grouped in one of two host-associated multilocus genotypes (MLGs), and temporal variation in focal field visitation by aphids indicated activity occurred earlier in the season in black locust-associated aphids than in alfalfa-associated aphids. Results also suggest local movement (<10 >km) characterizes most cowpea aphid dispersal. Lastly, I explored host plant-associated endosymbiont effects on cowpea aphid feeding behavior in pumpkins. Interaction effects among host-association (locust/alfalfa), endosymbiont association ( Arsenophonus/Hamiltonella defensa/cured) and virus infections (watermelon mosaic virus) on pumpkins were studied using an electrical penetration graph. I found differential endosymbiont effects on feeding behavior, with one exhibiting depressed frequency of intracellular probes and the other increased frequency. Greater probing frequency on WMV-infected pumpkins occurred across all aphids as a whole. This supports the Vector Manipulation Hypothesis, in which plant viruses mediate changes in plant gustatory and olfactory cues to change vector behavior in ways that enhance likelihood of virus transmission (i.e., increased exploratory intracellular probes). Overall, the dissertation results fill in some of the knowledge gaps existing in aphid-vectored, nonpersistent virus epidemiology using the pumpkin crop system. Hopefully some of the data will prove useful in applications toward aphid-vectored virus management in crops.

Degree

Ph.D.

Advisors

Kaplan, Purdue University.

Subject Area

Entomology

COinS