Foliar Aphid Herbivory Alters the Tomato Rhizosphere Microbiome, but Initial Soil Community Determines the Legacy Effects

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.

Shoot and root insect herbivory change the plant rhizosphere microbiome and affects cabbage–insect interactions through plant–soil feedback

“…Plants were additionally fertilized twice per week with 50 ml of Hyponex solution (nitrogen, phosphorus and potassium (NPK) = 7 : 6 : 19, electrical conductivity = 1.6). As the staring soil can be important in PSF experiments (French et al ., 2021 ), we used the same batch of soil throughout the experiment. Seedling and potting soil from the conditioning phase was bagged and stored at 4°C for use in the feedback phase (Fig.…”

Host Plant Species Influences the Composition of Milkweed and Monarch Microbiomes

“…Interestingly, our results show monarch feeding does not impose large top-down effects on microbial communities associated with host plant roots or leaves (Figure 4). In contrast, previous studies show aboveground herbivore feeding by both sap-sucking and chewing herbivores can induce changes in plant associated microbial communities (Humphrey and Whiteman, 2020;French et al, 2021;Malacrinò et al, 2021). For example, aphids can prime systemic plant defense responses, leading to increases in beneficial microbes and reductions in pathogens in the rhizosphere (Lee et al, 2012).…”

Soil microbiota and herbivory drive the assembly of plant-associated microbial communities through different mechanisms

“…Herbivory driven changes in microbiome composition could also be plant mediated or passive, and our data contributes to parsing out support for these hypotheses as well. Other studies have also shown that herbivory drives changes in shoot (Humphrey and Whiteman, 2020), root (Ourry et al ., 2018), and rhizosphere (Kong et al ., 2016; French et al ., 2021; Malacrinò, Wang, et al ., 2021) microbiome composition. These studies posit that changes in composition are driven by changes in metabolites, physiology, and root exudates.…”

“…Similarly, the effect driven by herbivores can be generated by active mechanisms (changes in plant metabolism) or by passive mechanisms (e.g., transfer of microorganisms between compartments via excrements or honeydew). Although both soil- and herbivory-driven effects on the plant and herbivore microbiota have been previously reported (Hannula et al ., 2019; Humphrey and Whiteman, 2020; Tkacz et al ., 2020; French et al ., 2021; Malacrinò, Karley, et al ., 2021), to the best of our knowledge, no previous study tested whether this effect is driven by active (via plant) or passive (via microbial spillover) mechanisms.…”