Phytoplasma-mediated manipulation of plant-herbivore interactions in the American cranberry
Creators: name: Pradit, Nakorn
Publisher: name: No Publisher Supplied
Year: 2019

description: The transmission of insect-borne pathogens mainly relies on the foraging and feeding behavior of their insect vectors. Changes in phytochemicals, especially volatiles, nutrients and chemical defenses, of host plants from pathogen infection can facilitate the performance and preference of insect vectors. Moreover, in the ecosystem, these changes in infected host plants can also affect non-vector herbivorous insects. In the American cranberry, Vaccinium macrocarpon Ait., false blossom disease is caused by a phytoplasma that requires the blunt-nosed leafhopper, Limotettix vaccinii Van Duzee, as a vector. In this study, we hypothesized that (1) phytoplasma infection enhances L. vaccinii performance and preference on infected plants, (2) phytoplasma infection enhances the performance of three non-vector leaf feeders, and (3) phytoplasma infection alters levels of phytochemicals and expression of gene related to primary (i.e., nutrients) and secondary (i.e., plant defenses) metabolism in cranberries. Phytoplasma infection had conflicting effects on its vector. L. vaccinii had similar survival rates on infected and uninfected cranberries; however, nymphs developed more slowly and adults had higher mass on infected plants than on uninfected plants, indicative of a short-term positive effect. In contrast, female L. vaccinii laid less eggs on infected plants than uninfected plants, indicative of a potential negative long-term effect on population size. In no-choice tests, L. vaccinii preferred volatiles from uninfected plants; uninfected plants emit higher volatile emissions than infected plants. Besides these effects on the vector, larvae of three common non-vector herbivores: spotted fireworm (Choristoneura parallela Robinson), Sparganothis fruitworm (Sparganothis sulfureana Clemens), and gypsy moth (Lymantria dispar L.) had 2-3 times higher mass, and damaged 1.5-3.5 times more leaves, when feeding on infected vs. uninfected plants. Larval survival of S. sulfurena and L. dispar also improved on infected plants. Nutrient levels were higher in infected plants, while defensive proanthocyanidins were lower, which may explain the short-term benefits in performance by vector and non-vector herbivores. Phytoplasma infection induced expression of 132 genes and suppressed expression of 225 genes in cranberries. Expression of genes associated with nutrient metabolism (i.e., carbohydrate) were up-regulated, while those associated with defensive pathways were down-regulated, in the phytoplasma-infected plants. Our study suggests that phytoplasma-infected plants may rely on visual cues and volatiles from neighboring uninfected plants to attract its vector L. vaccinii. After attraction, L. vaccinii feeding might be facilitated through elevated nutrient and reduced defensive metabolite levels in infected plants. These findings support the "vector manipulation hypothesis." This vector facilitation also benefits other, non-vector, herbivores in the cranberry community. A better understanding of the mechanisms underlying tri-partite interactions among plants, pathogens, and herbivores could help in the development of ways to reduce disease transmission by improving host-plant resistance against diseases and pests of crops.