Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system

Societal Impact Statement Arbuscular mycorrhizal fungi (AMF) impact the relationships between plants, aphids (insects that feed on plant phloem), and their natural enemies (insects that prey on or parasitize aphids). The presence of AMF influences the growth and population of different aphid species...

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Main Authors: Pasquale Cascone, Luigi Iodice, Liberata Gualtieri, Assunta Russo, Patrizia Cesaro, Zekun Yang, Michelina Ruocco, Maurilia Maria Monti, Nadia Massa, Guido Lingua, Emilio Guerrieri
Format: Article
Language:English
Published: Wiley 2024-11-01
Series:Plants, People, Planet
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Online Access:https://doi.org/10.1002/ppp3.10493
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author Pasquale Cascone
Luigi Iodice
Liberata Gualtieri
Assunta Russo
Patrizia Cesaro
Zekun Yang
Michelina Ruocco
Maurilia Maria Monti
Nadia Massa
Guido Lingua
Emilio Guerrieri
author_facet Pasquale Cascone
Luigi Iodice
Liberata Gualtieri
Assunta Russo
Patrizia Cesaro
Zekun Yang
Michelina Ruocco
Maurilia Maria Monti
Nadia Massa
Guido Lingua
Emilio Guerrieri
author_sort Pasquale Cascone
collection DOAJ
description Societal Impact Statement Arbuscular mycorrhizal fungi (AMF) impact the relationships between plants, aphids (insects that feed on plant phloem), and their natural enemies (insects that prey on or parasitize aphids). The presence of AMF influences the growth and population of different aphid species and affects the development of aphid‐killing wasps and their attraction to plants. This research has been conducted also considering the insects' feeding strategy and their feeding specialization. This study provides novel perspectives on how these fungi shape interactions in the natural world, offering potential insights for the development of sustainable pest management strategies in agriculture. Summary Arbuscular mycorrhizal fungi (AMF) are major root symbionts regulating plant physiology. Their presence affects the performance of aboveground insect herbivores in relation to their feeding strategy and their feeding specialization. For example, the effect of the arbuscular mycorrhizal (AM) symbiosis on chewing insects, positive for specialists and negative for generalists, has been previously demonstrated. Conversely, the impact of AMF on phloem‐suckers with relatively different levels of specialization remains unexplored. We tested the influence of the AM Funneliformis mosseae on the fitness of the specialist aphid Acyrthosiphon pisum and the generalist aphid Myzus persicae on Vicia faba plants. Further, we investigated the effects of AMF on the higher trophic level, the aphid parasitoids Aphidius ervi (specialist) and Aphidius colemani (generalist), by evaluating plant attractiveness and parasitoid fitness. To support the results of behavioral and biological bioassays we characterized the photosynthetic parameters, the volatilome and the transcriptome of tested plants. Mycorrhizal plants proved unsuitable for the generalist M. persicae but enhanced the fitness of the specialist A. pisum. The AM symbiosis had no effects on the behavioral response of A. colemani and enhanced the attraction and fitness of A. ervi. Volatilome and transcriptome profiling corroborated the results of bioassay highlighting a bottom‐up effect of the AMF across a plant–aphid–parasitoid system.
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spelling doaj-art-376ddc1173b64cf5a39e540e8787ee962025-08-20T02:10:32ZengWileyPlants, People, Planet2572-26112024-11-01661299131310.1002/ppp3.10493Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid systemPasquale Cascone0Luigi Iodice1Liberata Gualtieri2Assunta Russo3Patrizia Cesaro4Zekun Yang5Michelina Ruocco6Maurilia Maria Monti7Nadia Massa8Guido Lingua9Emilio Guerrieri10Institute for Sustainable Plant Protection (IPSP) National Research Council of Italy Portici Naples ItalyInstitute for Sustainable Plant Protection (IPSP) National Research Council of Italy Portici Naples ItalyInstitute for Sustainable Plant Protection (IPSP) National Research Council of Italy Portici Naples ItalyInstitute for Sustainable Plant Protection (IPSP) National Research Council of Italy Portici Naples ItalyDipartimento di Scienze e Innovazione Tecnologica Università del Piemonte Orientale Alessandria ItalyDepartment of Agronomy, Food, Natural Resources, Animals and Environment (DAFNAE) University of Padova Padova ItalyInstitute for Sustainable Plant Protection (IPSP) National Research Council of Italy Portici Naples ItalyInstitute for Sustainable Plant Protection (IPSP) National Research Council of Italy Portici Naples ItalyDipartimento di Scienze e Innovazione Tecnologica Università del Piemonte Orientale Alessandria ItalyDipartimento di Scienze e Innovazione Tecnologica Università del Piemonte Orientale Alessandria ItalyInstitute for Sustainable Plant Protection (IPSP) National Research Council of Italy Portici Naples ItalySocietal Impact Statement Arbuscular mycorrhizal fungi (AMF) impact the relationships between plants, aphids (insects that feed on plant phloem), and their natural enemies (insects that prey on or parasitize aphids). The presence of AMF influences the growth and population of different aphid species and affects the development of aphid‐killing wasps and their attraction to plants. This research has been conducted also considering the insects' feeding strategy and their feeding specialization. This study provides novel perspectives on how these fungi shape interactions in the natural world, offering potential insights for the development of sustainable pest management strategies in agriculture. Summary Arbuscular mycorrhizal fungi (AMF) are major root symbionts regulating plant physiology. Their presence affects the performance of aboveground insect herbivores in relation to their feeding strategy and their feeding specialization. For example, the effect of the arbuscular mycorrhizal (AM) symbiosis on chewing insects, positive for specialists and negative for generalists, has been previously demonstrated. Conversely, the impact of AMF on phloem‐suckers with relatively different levels of specialization remains unexplored. We tested the influence of the AM Funneliformis mosseae on the fitness of the specialist aphid Acyrthosiphon pisum and the generalist aphid Myzus persicae on Vicia faba plants. Further, we investigated the effects of AMF on the higher trophic level, the aphid parasitoids Aphidius ervi (specialist) and Aphidius colemani (generalist), by evaluating plant attractiveness and parasitoid fitness. To support the results of behavioral and biological bioassays we characterized the photosynthetic parameters, the volatilome and the transcriptome of tested plants. Mycorrhizal plants proved unsuitable for the generalist M. persicae but enhanced the fitness of the specialist A. pisum. The AM symbiosis had no effects on the behavioral response of A. colemani and enhanced the attraction and fitness of A. ervi. Volatilome and transcriptome profiling corroborated the results of bioassay highlighting a bottom‐up effect of the AMF across a plant–aphid–parasitoid system.https://doi.org/10.1002/ppp3.10493arbuscular mycorrhizal fungiintegrated pest managementmulti‐trophic interactionsspecialist and generalist aphidsVicia faba
spellingShingle Pasquale Cascone
Luigi Iodice
Liberata Gualtieri
Assunta Russo
Patrizia Cesaro
Zekun Yang
Michelina Ruocco
Maurilia Maria Monti
Nadia Massa
Guido Lingua
Emilio Guerrieri
Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system
Plants, People, Planet
arbuscular mycorrhizal fungi
integrated pest management
multi‐trophic interactions
specialist and generalist aphids
Vicia faba
title Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system
title_full Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system
title_fullStr Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system
title_full_unstemmed Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system
title_short Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system
title_sort feeding specialization shapes the bottom up effect of arbuscular mycorrhizal fungi across a plant aphid parasitoid system
topic arbuscular mycorrhizal fungi
integrated pest management
multi‐trophic interactions
specialist and generalist aphids
Vicia faba
url https://doi.org/10.1002/ppp3.10493
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