Nymphal feeding suppresses oviposition-induced indirect plant defense in rice

Abstract Feeding and oviposition by phytophagous insects are both known to trigger defenses in plants. Whether these two defenses functionally interact remains poorly studied, although these interactions are likely important for pests with overlapping generations. Here we investigated the difference...

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Main Authors: Jiancai Li, Xiaoli Liu, Wenhan Xiao, Jiayi Huangfu, Meredith C. Schuman, Ian T. Baldwin, Yonggen Lou
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-55816-y
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author Jiancai Li
Xiaoli Liu
Wenhan Xiao
Jiayi Huangfu
Meredith C. Schuman
Ian T. Baldwin
Yonggen Lou
author_facet Jiancai Li
Xiaoli Liu
Wenhan Xiao
Jiayi Huangfu
Meredith C. Schuman
Ian T. Baldwin
Yonggen Lou
author_sort Jiancai Li
collection DOAJ
description Abstract Feeding and oviposition by phytophagous insects are both known to trigger defenses in plants. Whether these two defenses functionally interact remains poorly studied, although these interactions are likely important for pests with overlapping generations. Here we investigated the differences and interaction between feeding- and oviposition-induced plant defenses triggered by the brown planthopper (BPH, Nilaparvata lugens), which gregariously feeds and oviposits on rice. Analyses of host-plant transcriptomes, phytohormones, and direct and indirect defense compounds all show that BPH gravid females (GFs), but not nymphs and non-gravid females (NFs), strongly induce rice defenses. BPH nymphs and GFs prefer to feed on plants previously infested by nymphs over un-attacked plants, but are repelled by plants previously infested by GFs. Moreover, nymph feeding is found to reduce the attractiveness of rice plants to natural enemies and decrease egg parasitism by suppressing GF-induced volatiles that mediate indirect defenses in both growth chambers and paddies. Intergenerational interactions between oviposition- and feeding-induced plant defenses not only promote the development of the population of pest insects but may also contribute to the aggregation behavior of pest insects by suppressing oviposition-induced indirect plant defenses.
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spelling doaj-art-2ab3cf4a6e2d4c7bbeee84d2860159762025-01-12T12:30:35ZengNature PortfolioNature Communications2041-17232025-01-0116111110.1038/s41467-025-55816-yNymphal feeding suppresses oviposition-induced indirect plant defense in riceJiancai Li0Xiaoli Liu1Wenhan Xiao2Jiayi Huangfu3Meredith C. Schuman4Ian T. Baldwin5Yonggen Lou6State key laboratory of rice biology and breeding & Ministry of Agriculture Key Lab of Agricultural Entomology, Institute of Insect Sciences, Zhejiang UniversityState key laboratory of rice biology and breeding & Ministry of Agriculture Key Lab of Agricultural Entomology, Institute of Insect Sciences, Zhejiang UniversityState key laboratory of rice biology and breeding & Ministry of Agriculture Key Lab of Agricultural Entomology, Institute of Insect Sciences, Zhejiang UniversityState key laboratory of rice biology and breeding & Ministry of Agriculture Key Lab of Agricultural Entomology, Institute of Insect Sciences, Zhejiang UniversityDepartments of Geography and Chemistry, University of ZürichDepartment of Molecular Ecology, Max Planck Institute for Chemical EcologyState key laboratory of rice biology and breeding & Ministry of Agriculture Key Lab of Agricultural Entomology, Institute of Insect Sciences, Zhejiang UniversityAbstract Feeding and oviposition by phytophagous insects are both known to trigger defenses in plants. Whether these two defenses functionally interact remains poorly studied, although these interactions are likely important for pests with overlapping generations. Here we investigated the differences and interaction between feeding- and oviposition-induced plant defenses triggered by the brown planthopper (BPH, Nilaparvata lugens), which gregariously feeds and oviposits on rice. Analyses of host-plant transcriptomes, phytohormones, and direct and indirect defense compounds all show that BPH gravid females (GFs), but not nymphs and non-gravid females (NFs), strongly induce rice defenses. BPH nymphs and GFs prefer to feed on plants previously infested by nymphs over un-attacked plants, but are repelled by plants previously infested by GFs. Moreover, nymph feeding is found to reduce the attractiveness of rice plants to natural enemies and decrease egg parasitism by suppressing GF-induced volatiles that mediate indirect defenses in both growth chambers and paddies. Intergenerational interactions between oviposition- and feeding-induced plant defenses not only promote the development of the population of pest insects but may also contribute to the aggregation behavior of pest insects by suppressing oviposition-induced indirect plant defenses.https://doi.org/10.1038/s41467-025-55816-y
spellingShingle Jiancai Li
Xiaoli Liu
Wenhan Xiao
Jiayi Huangfu
Meredith C. Schuman
Ian T. Baldwin
Yonggen Lou
Nymphal feeding suppresses oviposition-induced indirect plant defense in rice
Nature Communications
title Nymphal feeding suppresses oviposition-induced indirect plant defense in rice
title_full Nymphal feeding suppresses oviposition-induced indirect plant defense in rice
title_fullStr Nymphal feeding suppresses oviposition-induced indirect plant defense in rice
title_full_unstemmed Nymphal feeding suppresses oviposition-induced indirect plant defense in rice
title_short Nymphal feeding suppresses oviposition-induced indirect plant defense in rice
title_sort nymphal feeding suppresses oviposition induced indirect plant defense in rice
url https://doi.org/10.1038/s41467-025-55816-y
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