Abstract
Aboveground herbivory can impact the root-associated microbiome, while simultaneously different soil microbial communities influence herbivore performance. It is currently unclear how these reciprocal top-down and bottom-up interactions between plants, insects and microbes vary across different soils and over successive plant generations. In this study, we examined top-down impacts of above-ground herbivory on the rhizosphere microbiome across different soils, assessed bottom-up impacts of soil microbial community variation on herbivore performance, and evaluated their respective contributions to soil legacy effects on herbivore performance. We used Macrosiphum euphorbiae (potato aphid) and Solanum pimpinellifolium (wild tomato) to capture pre-domestication microbiome interactions with a specialist pest. First, using 16S rRNA sequencing we compared bacterial communities associated with rhizospheres of aphid-infested and uninfested control plants grown in three different soils over three time points. High aphid infestation impacted rhizosphere bacterial diversity in a soil-dependent manner, ranging from a 22% decrease to a 21% increase relative to uninfested plants and explained 6–7% of community composition differences in two of three soils. We next investigated bottom-up and soil legacy effects of aphid herbivory by growing wild tomatoes in each of the three soils and a sterilized “no microbiome” soil, infesting with aphids (phase one), then planting a second generation (phase two) of plants in the soil conditioned with aphid-infested or uninfested control plants. In the first phase, aphid performance varied across plants grown in different soil sources, ranging from a 20 to 50% increase in aphid performance compared to the “no microbiome” control soil, demonstrating a bottom-up role for soil microbial community. In the second phase, initial soil community, but not previous aphid infestation, impacted aphid performance on plants. Thus, while herbivory altered the rhizosphere microbiome in a soil community-dependent manner, the bottom-up interaction between the microbial community and the plant, not top-down effects of prior herbivore infestation, affected herbivore performance in the following plant generation. These findings suggest that the bottom-up effects of the soil microbial community play an overriding role in herbivore performance in both current and future plant generations and thus are an important target for sustainable control of herbivory in agroecosystems.
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Claims 6
Claim · model-written summary
High aphid infestation changed wild tomato rhizosphere bacterial diversity by 22% depending on soil.
- Taxon
- Tomato
Solanum lycopersicumt0 - Treatment
- High aphid infestatione0
- Interactor
- aphide0pest
- Outcome
- rhizosphere bacterial diversitye0
- Direction
- decreasee0
- Value
- 22%e0
- Comparator
- uninfested plantse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“High aphid infestation impacted rhizosphere bacterial diversity in a soil-dependent manner, ranging from a 22% decrease to a 21% increase relative to uninfested plants and explained 6–7% of community composition differences in two of three soils.”
t0“Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects”
Claim · model-written summary
High aphid infestation changed wild tomato rhizosphere bacterial diversity by 21% depending on soil.
- Taxon
- TomatoSolanum lycopersicumt0
- Treatment
- High aphid infestatione0
- Interactor
- aphide0pest
- Outcome
- rhizosphere bacterial diversitye0
- Direction
- increasee0
- Value
- 21%e0
- Comparator
- uninfested plantse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“High aphid infestation impacted rhizosphere bacterial diversity in a soil-dependent manner, ranging from a 22% decrease to a 21% increase relative to uninfested plants and explained 6–7% of community composition differences in two of three soils.”
t0“Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects”
Claim · model-written summary
Aphid infestation explained 6–7% of rhizosphere community composition differences in two of three soils.
- Taxon
- TomatoSolanum lycopersicumt0
- Treatment
- High aphid infestatione0
- Interactor
- aphide0pest
- Outcome
- community composition differencese0
- Value
- 6–7%e0
Not reportedDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“High aphid infestation impacted rhizosphere bacterial diversity in a soil-dependent manner, ranging from a 22% decrease to a 21% increase relative to uninfested plants and explained 6–7% of community composition differences in two of three soils.”
t0“Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects”
Claim · model-written summary
Aphid performance was 20 to 50% higher across soil sources than in sterilized no microbiome soil.
- Taxon
- TomatoSolanum lycopersicumt0
- Treatment
- different soil sourcese0
- Interactor
- aphide0pest
- Outcome
- aphid performancee0
- Direction
- increasee0
- Value
- 20 to 50%e0
- Comparator
- “no microbiome” control soile0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In the first phase, aphid performance varied across plants grown in different soil sources, ranging from a 20 to 50% increase in aphid performance compared to the “no microbiome” control soil, demonstrating a bottom-up role for soil microbial community.”
t0“Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects”
Claim · model-written summary
Initial soil community affected aphid performance in the second plant generation.
- Taxon
- TomatoSolanum lycopersicumt0
- Treatment
- initial soil communitye0
- Interactor
- aphide0pest
- Outcome
- aphid performancee0
Not reportedDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In the second phase, initial soil community, but not previous aphid infestation, impacted aphid performance on plants.”
t0“Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects”
Claim · model-written summary
Prior aphid infestation did not affect second generation aphid performance.
- Taxon
- TomatoSolanum lycopersicumt0
- Treatment
- previous aphid infestatione0
- Interactor
- aphide0pest
- Outcome
- aphid performancee0
Not reportedComparatorDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In the second phase, initial soil community, but not previous aphid infestation, impacted aphid performance on plants.”
t0“Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects”