Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness
Herbivore feeding often increases secondary metabolite production in plants. These herbivore-induced plant proteins might end up in honeydew excreted by phloem-feeding insects. This is important because honeydew is one of the most abundant and accessible carbohydrate sources for natural enemies in m...
| Autores principales: | , , , , |
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| Formato: | article |
| Lenguaje: | Inglés |
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Wiley
2024
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| Acceso en línea: | https://hdl.handle.net/20.500.11939/8974 https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2435.14605 |
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| author | Urbaneja-Bernat, Pablo Rodríguez-Saona, César Valero, M. Luz González-Cabrera, Joel Tena, Alejandro |
| author_browse | González-Cabrera, Joel Rodríguez-Saona, César Tena, Alejandro Urbaneja-Bernat, Pablo Valero, M. Luz |
| author_facet | Urbaneja-Bernat, Pablo Rodríguez-Saona, César Valero, M. Luz González-Cabrera, Joel Tena, Alejandro |
| author_sort | Urbaneja-Bernat, Pablo |
| collection | ReDivia |
| description | Herbivore feeding often increases secondary metabolite production in plants. These herbivore-induced plant proteins might end up in honeydew excreted by phloem-feeding insects. This is important because honeydew is one of the most abundant and accessible carbohydrate sources for natural enemies in many agroecosystems and these proteins can thus mediate many tri-trophic interactions.
Here, we hypothesized that defensive metabolites induced in the phloem by herbivory accumulate in the honeydew excreted by phloem-feeding insects and, consequently, affect the fitness of the herbivores' natural enemies that feed on it.
We used a tri-trophic system consisting of citrus plants, the mealybug Planococcus citri and its primary parasitoid Anagyrus vladimiri. First, we assessed A. vladimiri fitness when fed on P. citri honeydew. We then collected honeydew of seven phloem-feeding insects, including P. citri, and analysed their protein content. Finally, we analysed the effect of superoxide dismutase (SOD), an antioxidant enzyme associated with plant defences that was commonly found in the analysed honeydews, on A. vladimiri fitness.
The fitness of A. vladimiri increased when fed on honeydew compared to a sucrose-based diet, demonstrating that honeydew can contain compounds that benefit natural enemies. Proteomic analyses showed that defence-related plant proteins were present in honeydew of seven phloem-feeding insects analysed. Among these, the enzyme SOD was present in honeydew of all of them. Moreover, the levels of SOD were 10-fold higher in the phloem of plants infested by P. citri than in that of uninfested plants. SOD was also actively excreted in P. citri honeydew, and we proved that it increases the fecundity of the parasitoid A. vladimiri.
We conclude that enzymatic proteins induced by herbivory in the phloem and involved in plant defence, accumulate in the honeydew excreted by phloem-feeding insects and, contrary to the current paradigm, at least some of these can have positive effects on the third trophic level. |
| format | article |
| id | ReDivia8974 |
| institution | Instituto Valenciano de Investigaciones Agrarias (IVIA) |
| language | Inglés |
| publishDate | 2024 |
| publishDateRange | 2024 |
| publishDateSort | 2024 |
| publisher | Wiley |
| publisherStr | Wiley |
| record_format | dspace |
| spelling | ReDivia89742025-04-25T14:49:36Z Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness Urbaneja-Bernat, Pablo Rodríguez-Saona, César Valero, M. Luz González-Cabrera, Joel Tena, Alejandro Honeydew Induced-plant-defence Parasitoid fitness Plant-derives food source Superoxide dismutase (SOD) Tri-trophic interactions H10 Pests of plants Herbivore feeding often increases secondary metabolite production in plants. These herbivore-induced plant proteins might end up in honeydew excreted by phloem-feeding insects. This is important because honeydew is one of the most abundant and accessible carbohydrate sources for natural enemies in many agroecosystems and these proteins can thus mediate many tri-trophic interactions. Here, we hypothesized that defensive metabolites induced in the phloem by herbivory accumulate in the honeydew excreted by phloem-feeding insects and, consequently, affect the fitness of the herbivores' natural enemies that feed on it. We used a tri-trophic system consisting of citrus plants, the mealybug Planococcus citri and its primary parasitoid Anagyrus vladimiri. First, we assessed A. vladimiri fitness when fed on P. citri honeydew. We then collected honeydew of seven phloem-feeding insects, including P. citri, and analysed their protein content. Finally, we analysed the effect of superoxide dismutase (SOD), an antioxidant enzyme associated with plant defences that was commonly found in the analysed honeydews, on A. vladimiri fitness. The fitness of A. vladimiri increased when fed on honeydew compared to a sucrose-based diet, demonstrating that honeydew can contain compounds that benefit natural enemies. Proteomic analyses showed that defence-related plant proteins were present in honeydew of seven phloem-feeding insects analysed. Among these, the enzyme SOD was present in honeydew of all of them. Moreover, the levels of SOD were 10-fold higher in the phloem of plants infested by P. citri than in that of uninfested plants. SOD was also actively excreted in P. citri honeydew, and we proved that it increases the fecundity of the parasitoid A. vladimiri. We conclude that enzymatic proteins induced by herbivory in the phloem and involved in plant defence, accumulate in the honeydew excreted by phloem-feeding insects and, contrary to the current paradigm, at least some of these can have positive effects on the third trophic level. 2024-09-06T11:44:55Z 2024-09-06T11:44:55Z 2024 article publishedVersion Urbaneja‐Bernat, P., Rodriguez‐Saona, C., Valero, M. L., González‐Cabrera, J., & Tena, A. (2024). Not just candy: A herbivore‐induced defence‐related plant protein in honeydew enhances natural enemy fitness. Functional Ecology, 38(8), 1822-1834. 1365-2435 https://hdl.handle.net/20.500.11939/8974 10.1111/1365-2435.14605 https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2435.14605 en This research was partially funded by the projects: EUR2020-112293 funded MCIN and IVIA-GVA 52202 funded by IVIA (this project is susceptible of being cofinanced by the European Union through the ERDF Program 2021–2027). info:eu-repo/grantAgreement/ERDF/PCV 2021-2027/52202/ES/Control biológico de plagas y enfermedades como pieza clave en el impulso de la Sostenibilidad de los cultivos agrarios de la Comunidad Valenciana/SOSTENIBLE Attribution-NonCommercial-NoDerivatives 4.0 Internacional http://creativecommons.org/licenses/by-nc-nd/4.0/ openAccess Wiley electronico |
| spellingShingle | Honeydew Induced-plant-defence Parasitoid fitness Plant-derives food source Superoxide dismutase (SOD) Tri-trophic interactions H10 Pests of plants Urbaneja-Bernat, Pablo Rodríguez-Saona, César Valero, M. Luz González-Cabrera, Joel Tena, Alejandro Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness |
| title | Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness |
| title_full | Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness |
| title_fullStr | Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness |
| title_full_unstemmed | Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness |
| title_short | Not just candy: A herbivore-induced defence-related plant protein in honeydew enhances natural enemy fitness |
| title_sort | not just candy a herbivore induced defence related plant protein in honeydew enhances natural enemy fitness |
| topic | Honeydew Induced-plant-defence Parasitoid fitness Plant-derives food source Superoxide dismutase (SOD) Tri-trophic interactions H10 Pests of plants |
| url | https://hdl.handle.net/20.500.11939/8974 https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2435.14605 |
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