Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores
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 s...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-11-01
|
| Series: | Frontiers in Ecology and Evolution |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fevo.2022.1033730/full |
| _version_ | 1798023081357213696 |
|---|---|
| author | Morgan N. Thompson John M. Grunseich Laura O. Marmolejo Laura O. Marmolejo Natalie M. Aguirre Pius A. Bradicich Spencer T. Behmer Spencer T. Behmer Charles P.-C. Suh Anjel M. Helms Anjel M. Helms |
| author_facet | Morgan N. Thompson John M. Grunseich Laura O. Marmolejo Laura O. Marmolejo Natalie M. Aguirre Pius A. Bradicich Spencer T. Behmer Spencer T. Behmer Charles P.-C. Suh Anjel M. Helms Anjel M. Helms |
| author_sort | Morgan N. Thompson |
| collection | DOAJ |
| description | 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 laboratory 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)-β-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 and deters a suite of aboveground herbivores, suggesting larvae may manipulate aboveground plant defenses for their own benefit, while plants may benefit from enhanced systemic defenses against multi-herbivore attack. |
| first_indexed | 2024-04-11T17:40:21Z |
| format | Article |
| id | doaj.art-d1ac9b17a6804573925a1e88e405f1ab |
| institution | Directory Open Access Journal |
| issn | 2296-701X |
| language | English |
| last_indexed | 2024-04-11T17:40:21Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Ecology and Evolution |
| spelling | doaj.art-d1ac9b17a6804573925a1e88e405f1ab2022-12-22T04:11:31ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2022-11-011010.3389/fevo.2022.10337301033730Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivoresMorgan N. Thompson0John M. Grunseich1Laura O. Marmolejo2Laura O. Marmolejo3Natalie M. Aguirre4Pius A. Bradicich5Spencer T. Behmer6Spencer T. Behmer7Charles P.-C. Suh8Anjel M. Helms9Anjel M. Helms10Department of Entomology, Texas A&M University, College Station, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesDepartment of Entomology, Michigan State University, East Lansing, MI, United StatesEcology and Evolutionary Biology Program, Texas A&M University, College Station, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesEcology and Evolutionary Biology Program, Texas A&M University, College Station, TX, United StatesUSDA, ARS, Southern Plains Agricultural Research Center, College Station, TX, United StatesDepartment of Entomology, Texas A&M University, College Station, TX, United StatesEcology and Evolutionary Biology Program, Texas A&M University, College Station, TX, United StatesPlants 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 laboratory 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)-β-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 and deters a suite of aboveground herbivores, suggesting larvae may manipulate aboveground plant defenses for their own benefit, while plants may benefit from enhanced systemic defenses against multi-herbivore attack.https://www.frontiersin.org/articles/10.3389/fevo.2022.1033730/fullabove-belowground interactionsinsect herbivoryherbivore-induced plant volatilesphytohormonessystemic plant defense |
| spellingShingle | Morgan N. Thompson John M. Grunseich Laura O. Marmolejo Laura O. Marmolejo Natalie M. Aguirre Pius A. Bradicich Spencer T. Behmer Spencer T. Behmer Charles P.-C. Suh Anjel M. Helms Anjel M. Helms Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores Frontiers in Ecology and Evolution above-belowground interactions insect herbivory herbivore-induced plant volatiles phytohormones systemic plant defense |
| title | Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores |
| title_full | Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores |
| title_fullStr | Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores |
| title_full_unstemmed | Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores |
| title_short | Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores |
| title_sort | undercover operation belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores |
| topic | above-belowground interactions insect herbivory herbivore-induced plant volatiles phytohormones systemic plant defense |
| url | https://www.frontiersin.org/articles/10.3389/fevo.2022.1033730/full |
| work_keys_str_mv | AT morgannthompson undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT johnmgrunseich undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT lauraomarmolejo undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT lauraomarmolejo undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT nataliemaguirre undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT piusabradicich undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT spencertbehmer undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT spencertbehmer undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT charlespcsuh undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT anjelmhelms undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores AT anjelmhelms undercoveroperationbelowgroundinsectherbivorymodifiessystemicplantdefenseandrepelsabovegroundforaginginsectherbivores |