Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thaliana

ABSTRACT Plants respond to attack by chewing insects through the recognition of herbivore‐associated molecular patterns (HAMPs) that are present in oral secretions (OS) and released at the wound site, leading to appropriate deployment of plant immune responses. Because insect feeding is accompanied...

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Main Authors: Angel Fernandez Martin, Philippe Reymond
Format: Article
Language:English
Published: Wiley 2025-06-01
Series:Plant Direct
Subjects:
Online Access:https://doi.org/10.1002/pld3.70085
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author Angel Fernandez Martin
Philippe Reymond
author_facet Angel Fernandez Martin
Philippe Reymond
author_sort Angel Fernandez Martin
collection DOAJ
description ABSTRACT Plants respond to attack by chewing insects through the recognition of herbivore‐associated molecular patterns (HAMPs) that are present in oral secretions (OS) and released at the wound site, leading to appropriate deployment of plant immune responses. Because insect feeding is accompanied by severe wounding of the leaf tissue, the specific contribution of HAMPs to defense is not well characterized. Also, OS contain effectors that interfere with the activation of defenses, but the underlying downregulated genes are poorly studied. Here, we analyzed the transcriptome of Arabidopsis thaliana leaves in response to wounding alone or to wounding and application of OS from Spodoptera littoralis or Pieris brassicae. For both insects, OS amplified wound‐induced responses and specifically promoted the activation of stress and hormonal pathways, as well as pathogen‐related responses. In contrast, OS inhibited the expression of genes involved in the regulation and biosynthesis of aliphatic glucosinolates (GS), and cell wall strengthening. In addition, OS‐mediated suppression of wound‐induced ERF114 and wound healing‐related genes uncovered a novel strategy to impair defenses. In support of these findings, we observed an increased performance of S. littoralis and P. brassicae larvae feeding on OS‐treated Arabidopsis plants. Altogether, we highlight a major contribution of OS components to plant response to herbivory and unveil the potential role of conserved OS‐derived effector(s) in inhibiting defenses.
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spelling doaj-art-c491f874fcef4e4282fd9a9e764355e92025-08-20T02:59:35ZengWileyPlant Direct2475-44552025-06-0196n/an/a10.1002/pld3.70085Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thalianaAngel Fernandez Martin0Philippe Reymond1Department of Plant Molecular Biology University of Lausanne Lausanne SwitzerlandDepartment of Plant Molecular Biology University of Lausanne Lausanne SwitzerlandABSTRACT Plants respond to attack by chewing insects through the recognition of herbivore‐associated molecular patterns (HAMPs) that are present in oral secretions (OS) and released at the wound site, leading to appropriate deployment of plant immune responses. Because insect feeding is accompanied by severe wounding of the leaf tissue, the specific contribution of HAMPs to defense is not well characterized. Also, OS contain effectors that interfere with the activation of defenses, but the underlying downregulated genes are poorly studied. Here, we analyzed the transcriptome of Arabidopsis thaliana leaves in response to wounding alone or to wounding and application of OS from Spodoptera littoralis or Pieris brassicae. For both insects, OS amplified wound‐induced responses and specifically promoted the activation of stress and hormonal pathways, as well as pathogen‐related responses. In contrast, OS inhibited the expression of genes involved in the regulation and biosynthesis of aliphatic glucosinolates (GS), and cell wall strengthening. In addition, OS‐mediated suppression of wound‐induced ERF114 and wound healing‐related genes uncovered a novel strategy to impair defenses. In support of these findings, we observed an increased performance of S. littoralis and P. brassicae larvae feeding on OS‐treated Arabidopsis plants. Altogether, we highlight a major contribution of OS components to plant response to herbivory and unveil the potential role of conserved OS‐derived effector(s) in inhibiting defenses.https://doi.org/10.1002/pld3.70085Arabidopsisglucosinolatesherbivorylepidopteraoral secretionstranscriptome
spellingShingle Angel Fernandez Martin
Philippe Reymond
Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thaliana
Plant Direct
Arabidopsis
glucosinolates
herbivory
lepidoptera
oral secretions
transcriptome
title Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thaliana
title_full Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thaliana
title_fullStr Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thaliana
title_full_unstemmed Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thaliana
title_short Impact of Lepidopteran Oral Secretions on the Transcriptome of Arabidopsis thaliana
title_sort impact of lepidopteran oral secretions on the transcriptome of arabidopsis thaliana
topic Arabidopsis
glucosinolates
herbivory
lepidoptera
oral secretions
transcriptome
url https://doi.org/10.1002/pld3.70085
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