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Koinobiont endoparasitoid wasps whose larvae develop inside a host insect alter several important facets of host physiology, potentially causing cascading effects across multiple trophic levels. For instance, the hijacking of the host immune responses may have effects on how insects interact with host plants and microbial associates. However, the parasitoid regulation of insect–plant–microbiome interactions is still understudied. In this study, we used the fall armyworm (FAW), Spodoptera frugiperda , and the braconid parasitoid Cotesia marginiventris to evaluate impacts of parasitism on the gut microbiome of FAW larvae, and respective maize plant defense responses. The level of reactive oxygen species and the microbial community in larval gut underwent significant changes in response to parasitism, leading to a significant reduction of Enterococcus , while elevating the relative abundance of Pseudomonas . FAW with parasitism had lower glucose oxidase (GOX) activity in salivary glands and triggered lower defense responses in maize plants. These changes corresponded to effects on plants, as Pseudomonas inoculated larvae had lower activity of salivary GOX and triggered lower defense responses in maize plants. Our results demonstrated that parasitism had cascading effects on microbial associates across trophic levels and also highlighted that insect gut bacteria may contribute to complex interrelationships among parasitoids, herbivores, and plants.
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Co‐option of microbial associates by insects and their impact on plant–folivore interactions
Abstract Plants possess a suite of traits that make them challenging to consume by insect herbivores. Plant tissues are recalcitrant, have low levels of protein, and may be well defended by chemicals. Insects use diverse strategies for overcoming these barriers, including co‐opting metabolic activities from microbial associates. In this review, we discuss the co‐option of bacteria and fungi in the herbivore gut. We particularly focus upon chewing, folivorous insects (Coleoptera and Lepidoptera) and discuss the impacts of microbial co‐option on herbivore performance and plant responses. We suggest that there are two components to microbial co‐option: fixed and plastic relationships. Fixed relationships are involved in integral dietary functions and can be performed by microbial enzymes co‐opted into the genome or by stably transferred associates. In contrast, the majority of gut symbionts appear to be looser and perform more facultative, context‐dependent functions. This more plastic, variable co‐option of bacteria likely produces a greater number of insect phenotypes, which interact differently with plant hosts. By altering plant detection of herbivory or mediating insect interactions with plant defensive compounds, microbes can effectively improve herbivore performance in real time within and between generations.
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- Award ID(s):
- 1645548
- PAR ID:
- 10075870
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Plant, Cell & Environment
- Volume:
- 42
- Issue:
- 3
- ISSN:
- 0140-7791
- Page Range / eLocation ID:
- p. 1078-1086
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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