Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses

Abstract Understanding the responses of insect herbivores to plant chemical defences is pivotal for the management of crops and pests. However, the mechanisms of interaction are not entirely understood. In this study, we compared the whole transcriptome gene expression of the aphid Macrosiphum eupho...

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Main Authors: Rosario Planelló, Lola Llorente, Óscar Herrero, Marta Novo, Lidia Blanco-Sánchez, Juan Antonio Díaz-Pendón, Rafael Fernández-Muñoz, Victoria Ferrero, Eduardo de la Peña
Format: Article
Language:English
Published: Nature Portfolio 2022-11-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-24490-1
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author Rosario Planelló
Lola Llorente
Óscar Herrero
Marta Novo
Lidia Blanco-Sánchez
Juan Antonio Díaz-Pendón
Rafael Fernández-Muñoz
Victoria Ferrero
Eduardo de la Peña
author_facet Rosario Planelló
Lola Llorente
Óscar Herrero
Marta Novo
Lidia Blanco-Sánchez
Juan Antonio Díaz-Pendón
Rafael Fernández-Muñoz
Victoria Ferrero
Eduardo de la Peña
author_sort Rosario Planelló
collection DOAJ
description Abstract Understanding the responses of insect herbivores to plant chemical defences is pivotal for the management of crops and pests. However, the mechanisms of interaction are not entirely understood. In this study, we compared the whole transcriptome gene expression of the aphid Macrosiphum euphorbiae grown on two different varieties of tomato that differ in their inducible chemical defences. We used two isogenic lines of tomato with a shared genetic background that only differ in the presence of type IV glandular trichomes and their associated acylsucrose excretions. This works also reports a de novo transcriptome of the aphid M. euphorbiae. Subsequently, we identified a unique and distinct gene expression profile for the first time corresponding to aphid´s exposure to type IV glandular trichomes and acylsugars. The analysis of the aphid transcriptome shows that tomato glandular trichomes and their associated secretions are highly efficient in triggering stress-related responses in the aphid, and demonstrating that their role in plant defence goes beyond the physical impediment of herbivore activity. Some of the differentially expressed genes were associated with carbohydrate, lipid and xenobiotic metabolisms, immune system, oxidative stress response and hormone biosynthesis pathways. Also, the observed responses are compatible with a starvation syndrome. The transcriptome analysis puts forward a wide range of genes involved in the synthesis and regulation of detoxification enzymes that reveal important underlying mechanisms in the interaction of the aphid with its host plant and provides a valuable genomic resource for future study of biological processes at the molecular level using this aphid.
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spelling doaj.art-737d8635031b467cb4aa05563d68727e2022-12-22T02:55:06ZengNature PortfolioScientific Reports2045-23222022-11-0112111610.1038/s41598-022-24490-1Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responsesRosario Planelló0Lola Llorente1Óscar Herrero2Marta Novo3Lidia Blanco-Sánchez4Juan Antonio Díaz-Pendón5Rafael Fernández-Muñoz6Victoria Ferrero7Eduardo de la Peña8Biology and Environmental Toxicology Group, Faculty of Science, Universidad Nacional de Educación a Distancia (UNED)Biology and Environmental Toxicology Group, Faculty of Science, Universidad Nacional de Educación a Distancia (UNED)Biology and Environmental Toxicology Group, Faculty of Science, Universidad Nacional de Educación a Distancia (UNED)Biodiversity, Ecology and Evolution Department, Complutense University of MadridInstitute for Subtropical and Mediterranean Horticulture (IHSM-UMA-CSIC), Spanish National Research Council (CSIC), Finca Experimental La Mayora, Algarrobo-CostaInstitute for Subtropical and Mediterranean Horticulture (IHSM-UMA-CSIC), Spanish National Research Council (CSIC), Finca Experimental La Mayora, Algarrobo-CostaInstitute for Subtropical and Mediterranean Horticulture (IHSM-UMA-CSIC), Spanish National Research Council (CSIC), Finca Experimental La Mayora, Algarrobo-CostaArea of Botany, Faculty of Biological and Environmental Sciences, University of LeonInstitute for Subtropical and Mediterranean Horticulture (IHSM-UMA-CSIC), Spanish National Research Council (CSIC), Finca Experimental La Mayora, Algarrobo-CostaAbstract Understanding the responses of insect herbivores to plant chemical defences is pivotal for the management of crops and pests. However, the mechanisms of interaction are not entirely understood. In this study, we compared the whole transcriptome gene expression of the aphid Macrosiphum euphorbiae grown on two different varieties of tomato that differ in their inducible chemical defences. We used two isogenic lines of tomato with a shared genetic background that only differ in the presence of type IV glandular trichomes and their associated acylsucrose excretions. This works also reports a de novo transcriptome of the aphid M. euphorbiae. Subsequently, we identified a unique and distinct gene expression profile for the first time corresponding to aphid´s exposure to type IV glandular trichomes and acylsugars. The analysis of the aphid transcriptome shows that tomato glandular trichomes and their associated secretions are highly efficient in triggering stress-related responses in the aphid, and demonstrating that their role in plant defence goes beyond the physical impediment of herbivore activity. Some of the differentially expressed genes were associated with carbohydrate, lipid and xenobiotic metabolisms, immune system, oxidative stress response and hormone biosynthesis pathways. Also, the observed responses are compatible with a starvation syndrome. The transcriptome analysis puts forward a wide range of genes involved in the synthesis and regulation of detoxification enzymes that reveal important underlying mechanisms in the interaction of the aphid with its host plant and provides a valuable genomic resource for future study of biological processes at the molecular level using this aphid.https://doi.org/10.1038/s41598-022-24490-1
spellingShingle Rosario Planelló
Lola Llorente
Óscar Herrero
Marta Novo
Lidia Blanco-Sánchez
Juan Antonio Díaz-Pendón
Rafael Fernández-Muñoz
Victoria Ferrero
Eduardo de la Peña
Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses
Scientific Reports
title Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses
title_full Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses
title_fullStr Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses
title_full_unstemmed Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses
title_short Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses
title_sort transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses
url https://doi.org/10.1038/s41598-022-24490-1
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