Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids
Microorganisms associated with plant roots significantly impact the quality and quantity of plant defences. However, the bottom-up effects of soil microbes on the aboveground multitrophic interactions remain largely under studied. To address this gap, we investigated the chemically-mediated effects...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-03-01
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| Series: | Heliyon |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2405844024038465 |
| _version_ | 1797224173160890368 |
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| author | Carlos Bustos-Segura Adrienne L. Godschalx Lucas Malacari Fanny Deiss Sergio Rasmann Daniel J. Ballhorn Betty Benrey |
| author_facet | Carlos Bustos-Segura Adrienne L. Godschalx Lucas Malacari Fanny Deiss Sergio Rasmann Daniel J. Ballhorn Betty Benrey |
| author_sort | Carlos Bustos-Segura |
| collection | DOAJ |
| description | Microorganisms associated with plant roots significantly impact the quality and quantity of plant defences. However, the bottom-up effects of soil microbes on the aboveground multitrophic interactions remain largely under studied. To address this gap, we investigated the chemically-mediated effects of nitrogen-fixing rhizobia on legume-herbivore-parasitoid multitrophic interactions. To address this, we initially examined the cascading effects of the rhizobia bean association on herbivore caterpillars, their parasitoids, and subsequently investigated how rhizobia influence on plant volatiles and extrafloral nectar. Our goal was to understand how these plant-mediated effects can affect parasitoids. Lima bean plants (Phaseoulus lunatus) inoculated with rhizobia exhibited better growth, and the number of root nodules positively correlated with defensive cyanogenic compounds. Despite increase of these chemical defences, Spodoptera latifascia caterpillars preferred to feed and grew faster on rhizobia-inoculated plants. Moreover, the emission of plant volatiles after leaf damage showed distinct patterns between inoculation treatments, with inoculated plants producing more sesquiterpenes and benzyl nitrile than non-inoculated plants. Despite these differences, Euplectrus platyhypenae parasitoid wasps were similarly attracted to rhizobia- or no rhizobia-treated plants. Yet, the oviposition and offspring development of E. platyhypenae was better on caterpillars fed with rhizobia-inoculated plants. We additionally show that rhizobia-inoculated common bean plants (Phaseolus vulgaris) produced more extrafloral nectar, with higher hydrocarbon concentration, than non-inoculated plants. Consequently, parasitoids performed better when fed with extrafloral nectar from rhizobia-inoculated plants. While the overall effects of bean-rhizobia symbiosis on caterpillars were positive, rhizobia also indirectly benefited parasitoids through the caterpillar host, and directly through the improved production of high quality extrafloral nectar. This study underscores the importance of exploring diverse facets and chemical mechanisms that influence the dynamics between herbivores and predators. This knowledge is crucial for gaining a comprehensive understanding of the ecological implications of rhizobia symbiosis on these interactions. |
| first_indexed | 2024-04-24T13:48:54Z |
| format | Article |
| id | doaj.art-0c0593684ccf4bb2a8366786d08ef899 |
| institution | Directory Open Access Journal |
| issn | 2405-8440 |
| language | English |
| last_indexed | 2024-04-24T13:48:54Z |
| publishDate | 2024-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Heliyon |
| spelling | doaj.art-0c0593684ccf4bb2a8366786d08ef8992024-04-04T05:06:01ZengElsevierHeliyon2405-84402024-03-01106e27815Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoidsCarlos Bustos-Segura0Adrienne L. Godschalx1Lucas Malacari2Fanny Deiss3Sergio Rasmann4Daniel J. Ballhorn5Betty Benrey6Laboratory of Evolutionary Entomology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland; Sorbonne Université, Institut National de Recherche pour L'Agriculture, L'Alimentation et L'Environnement, CNRS, Institut de Recherche pour le Développement, Université Paris-Est-Créteil-Val-de-Marne, Université Paris Cité, Institut D’Ecologie et des Sciences de L’Environnement de Paris, Versailles, 78026, FranceLaboratory of Functional Ecology, Institute of Biology, University of Neuchâtel, Neuchâtel, SwitzerlandLaboratory of Evolutionary Entomology, Institute of Biology, University of Neuchâtel, Neuchâtel, SwitzerlandLaboratory of Evolutionary Entomology, Institute of Biology, University of Neuchâtel, Neuchâtel, SwitzerlandLaboratory of Functional Ecology, Institute of Biology, University of Neuchâtel, Neuchâtel, SwitzerlandDepartment of Biology, Portland State University, Portland, OR, USALaboratory of Evolutionary Entomology, Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland; Corresponding author.Microorganisms associated with plant roots significantly impact the quality and quantity of plant defences. However, the bottom-up effects of soil microbes on the aboveground multitrophic interactions remain largely under studied. To address this gap, we investigated the chemically-mediated effects of nitrogen-fixing rhizobia on legume-herbivore-parasitoid multitrophic interactions. To address this, we initially examined the cascading effects of the rhizobia bean association on herbivore caterpillars, their parasitoids, and subsequently investigated how rhizobia influence on plant volatiles and extrafloral nectar. Our goal was to understand how these plant-mediated effects can affect parasitoids. Lima bean plants (Phaseoulus lunatus) inoculated with rhizobia exhibited better growth, and the number of root nodules positively correlated with defensive cyanogenic compounds. Despite increase of these chemical defences, Spodoptera latifascia caterpillars preferred to feed and grew faster on rhizobia-inoculated plants. Moreover, the emission of plant volatiles after leaf damage showed distinct patterns between inoculation treatments, with inoculated plants producing more sesquiterpenes and benzyl nitrile than non-inoculated plants. Despite these differences, Euplectrus platyhypenae parasitoid wasps were similarly attracted to rhizobia- or no rhizobia-treated plants. Yet, the oviposition and offspring development of E. platyhypenae was better on caterpillars fed with rhizobia-inoculated plants. We additionally show that rhizobia-inoculated common bean plants (Phaseolus vulgaris) produced more extrafloral nectar, with higher hydrocarbon concentration, than non-inoculated plants. Consequently, parasitoids performed better when fed with extrafloral nectar from rhizobia-inoculated plants. While the overall effects of bean-rhizobia symbiosis on caterpillars were positive, rhizobia also indirectly benefited parasitoids through the caterpillar host, and directly through the improved production of high quality extrafloral nectar. This study underscores the importance of exploring diverse facets and chemical mechanisms that influence the dynamics between herbivores and predators. This knowledge is crucial for gaining a comprehensive understanding of the ecological implications of rhizobia symbiosis on these interactions.http://www.sciencedirect.com/science/article/pii/S2405844024038465RhizobiaPhaseolusBelow-ground interactionsIndirect effectsExtrafloral nectarMultitrophic interactions |
| spellingShingle | Carlos Bustos-Segura Adrienne L. Godschalx Lucas Malacari Fanny Deiss Sergio Rasmann Daniel J. Ballhorn Betty Benrey Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids Heliyon Rhizobia Phaseolus Below-ground interactions Indirect effects Extrafloral nectar Multitrophic interactions |
| title | Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids |
| title_full | Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids |
| title_fullStr | Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids |
| title_full_unstemmed | Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids |
| title_short | Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids |
| title_sort | rhizobia legume symbiosis mediates direct and indirect interactions between plants herbivores and their parasitoids |
| topic | Rhizobia Phaseolus Below-ground interactions Indirect effects Extrafloral nectar Multitrophic interactions |
| url | http://www.sciencedirect.com/science/article/pii/S2405844024038465 |
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