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.
Highlights
Hubbard et al, 2019; Blundell et al, 2020) (Figure 1B)
In contrast to initial predictions that top-down effects of aphid herbivory on the rhizosphere would be similar across soils due to a common “cry for help” response, we observed soildependent effects of herbivory on both the diversity and structure of rhizosphere bacterial communities
We found that high levels of aphid herbivory have a top-down impact on the diversity and composition of the rhizosphere bacterial microbiome of wild tomato
Summary
2019; Blundell et al, 2020) (Figure 1B) Both topdown and bottom-up processes are inherently interconnected, making quantification of plant-insect-microbiome interactions complicated. When aboveground herbivory alters the micSyntax Error (123853): Bad LZW stream - unexpected code robial community surrounding plant roots, these top-down effects can influence bottom-up effects on herbivore performance over time. If soil microbial communities impact plantherbivore interactions, bottom-up effects could lead to variation in responsiveness of the rhizosphere microbiome to top-down effects of herbivore feeding. Top-down effects alter plant stress response and herbivory is hypothesized to elicit a “cry for help” to recruit soil microbes to the rhizosphere that provide protection (Yi et al, 2011; Liu et al, 2020). In addition to topdown effects, “bottom-up” effects of the soil microbiome on herbivore performance can occur through induction of chemical
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