Indirect Manipulation Of Plant Induced Defenses By Parasitoids Of Caterpillars
Open Access
- Author:
- Tan, Ching Wen
- Graduate Program:
- Entomology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- February 18, 2019
- Committee Members:
- Gary W. Felton, Dissertation Advisor/Co-Advisor
Gary W. Felton, Committee Chair/Co-Chair
Dawn Luthe, Committee Member
Jared Gregory Ali, Committee Member
Cristina Rosa, Outside Member
Kelli Hoover, Committee Member - Keywords:
- herbivore
parasitoid
tritrophic interaction
host immunigy
plant defense
phytobiome
fitness
saliva
oral secretions - Abstract:
- Almost all plant species are attacked by multiple herbivore species and have evolved various strategies to defend themselves. These plant defense strategies include inducible physical and chemical traits; for example, induced defensive proteins and secondary metabolites can impair herbivore growth and survival. These induced defenses rely on the recognition of herbivore presence. The oral secretions (regurgitant and saliva) of insect herbivores play a crucial role in providing cues that are recognized by plants, which then trigger plant defense responses. However, the interactions between plants and insects are considerably more complex in nature where other trophic levels are involved and can influence these interactions. Microorganisms are abundant in the environment and can impact interactions in many ways including altering the perception of herbivores by plants. Braconid parasitoids are small wasps which lay their eggs inside host caterpillars. These parasitoids possess obligate mutualistic viruses called polydnaviruses (PDVs). PDVs are injected by parasitoids with their eggs into host caterpillars. PDVs suppress caterpillar immune responses and metabolism, thus allowing parasitoid eggs to hatch and develop. In nature, 35-80% of caterpillars are parasitized, depending on locations and host plant species. However, it is not clear how parasitoid/PDVs influence plant and herbivore interactions. The main objective of this study were to: 1. Reveal the mechanism and impacts of the parasitoid and its PDV (Microplitis croceipes) on tomato plant defenses through its host caterpillar (Helicoverpa zea); 2. Evaluate the consequences of parasitoid suppression of induced plant defenses on plant fitness; and 3. Determine if the parasitoid effect on plant defenses are commonly present in other plant and insect systems. These objectives were approached by a series of biochemical, physiological and molecular experiments and results provide solid evidence to support the hypothesis that plants can distinguish between feeding by parasitized and non-parasitized caterpillars, thus altering their defense responses accordingly. Microplitis croceipes parasitized Helicoverpa zea larvae produced lower elicitor activity in their saliva (i.e., glucose oxidase) compared with non-parasitized caterpillars, and significantly downregulated tomato defense-related gene expression and defense protein activities during feeding. The ultimate cause of downregulation of plant defense responses was due to the obligate mutualist PDVs of the parasitoid. PDVs suppressed GOX gene expression and activity in parasitized caterpillar salivary glands thereby downregulating plant defense responses. The lower induced plant defenses benefit the parasitoid by promoting parasitized caterpillar growth performance, producing heavier cocoon mass and overall higher parasitoid survival rate. Besides, tomato plants treated by parasitized caterpillar saliva had significantly higher fitness (increased flower number and fruit weight) compared to those treated by non-parasitized caterpillars. These results support the hypothesis that plants benefit from parasitoids indirectly. This is a previously unidentified benefit of parasitoids on plant productivity/fitness. Two other plant and insect systems were also tested and confirmed that parasitoids can indirectly influence plants perception of insect herbivores. These findings have revealed a novel aspect of microbe-mediated interactions between plants and insects. The symbiotic PDV virus not only alters the phenotype of its primary host (i.e., parasitoid) and secondary host (i.e., caterpillar), but also the host plant of the caterpillar. This is the most extreme example of the extended phenotype known: a virus phenotype that extends across three trophic levels. This work has important implications for the evolutionary ecology of plant-herbivore-parasitoid interactions and points out a new perspective of mutualism between plants and parasitoids.