Undercover operation: belowground herbivory modifies systemic plant defense and repels aboveground foraging herbivores

Authors: THOMPSON, MORGAN - Texas A&M University; GRUNSEICH, JOHN - Texas A&M University; MARMOLEJO, LAURA - Texas A&M University; ARGUIRRE, NATALIE - Texas A&M University; BRADICICH, PIUS - Texas A&M University; BEHMER, SPENCER - Texas A&M University; Suh, Charles; HELMS, ANJEL - Texas A&M University

Submitted to: Frontiers in Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/24/2022
Publication Date: 11/10/2022
Citation: Thompson, M.N., Grunseich, J.M., Marmolejo, L.O., Arguirre, N.M., Bradicich, P., Behmer, S.T., Suh, C.P., Helms, A.M. 2022. Undercover operation: belowground herbivory modifies systemic plant defense and repels aboveground foraging herbivores. Frontiers in Ecology and Evolution. Article 1033730. https://doi.org/10.3389/fevo.2022.1033730.
DOI: https://doi.org/10.3389/fevo.2022.1033730

Interpretive Summary: There is increasing evidence that insect pests feeding on one type of plant structure can alter the profile of defensive chemicals produced in other parts of the plant. This phenomenon is known as "cross-compartment systemic response" but little is known about the impacts of this systemic response on above- and below-ground insect pest communities that share a common host. We discovered striped cucumber beetle larval feeding on roots of zucchini squash altered the nutrient content in leaves, enhanced above ground plant defenses, and repelled key above-ground insect pests such as adult striped cucumber beetles and squash bugs. However, feeding by these adults on above-ground tissue had no impact on the development of striped cucumber beetle larvae or root damage. These findings suggest root-feeding larvae may manipulate above-ground defenses for their own benefit, while zucchini squash plants benefit from enhanced defenses against multiple above-ground insect pests. Overall, our findings provide new insight on the indirect interactions between above- and below-ground insect pests as mediated by cross-compartment systemic response of a shared host plant.

Technical Abstract: Plants attacked by insects may induce defenses locally in attacked plant tissues and/or systemically in non-attacked tissues, such as aboveground herbivory affecting belowground roots or belowground herbivory modifying aboveground tissues (i.e., cross-compartment systemic defense). Through induced systemic plant defenses, above- and belowground insect herbivores indirectly interact when feeding on a shared host plant. However, determining the systemic effects of herbivory on cross-compartment plant tissues and cascading consequences for herbivore communities remains underexplored. The goal of this study was to determine how belowground striped cucumber beetle (Acalymma vittatum) larval herbivory alters aboveground zucchini squash (Cucurbita pepo subsp. pepo) defenses and interactions with herbivores, including adult cucumber beetles and squash bugs (Anasa tristis). To explore this question, field and greenhouse experiments were conducted to compare responses of aboveground herbivores to belowground larvae-damaged plants and non-damaged control plants. We also characterized changes in defensive chemicals and nutritional content of aboveground plant structures following belowground herbivory. We discovered belowground herbivory enhanced aboveground plant resistance and deterred aboveground foraging herbivores. We also found that larvae-damaged plants emitted higher amounts of a key volatile compound, (E)-ß-ocimene, compared to non-damaged controls. Further investigation suggests that other mechanisms, such as plant nutrient content may additionally contribute to aboveground herbivore foraging decisions. Collectively, our findings underscore connections between above- and belowground herbivore communities as mediated through induced systemic defenses of a shared host plant. Specifically, these findings indicate that belowground larval herbivory systemically enhances plant defenses in zucchini squash and deters a suite of respective aboveground insect herbivores, suggesting larvae may manipulate aboveground plant defenses for their own benefit, while plants may benefit from enhanced systemic defenses against multi-herbivore attack.