Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i>
Tomato plants are attacked by a variety of herbivore pests and among them, the leafminer <i>Tuta absoluta</i>, which is currently a major threat to global tomato production. Although the commercial tomato is susceptible to <i>T. absoluta</i> attacks, a better understanding of...
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MDPI AG
2022-05-01
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| Series: | Metabolites |
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| Online Access: | https://www.mdpi.com/2218-1989/12/6/484 |
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| author | Marwa Roumani Jacques Le Bot Michel Boisbrun Florent Magot Arthur Péré Christophe Robin Frédérique Hilliou Romain Larbat |
| author_facet | Marwa Roumani Jacques Le Bot Michel Boisbrun Florent Magot Arthur Péré Christophe Robin Frédérique Hilliou Romain Larbat |
| author_sort | Marwa Roumani |
| collection | DOAJ |
| description | Tomato plants are attacked by a variety of herbivore pests and among them, the leafminer <i>Tuta absoluta</i>, which is currently a major threat to global tomato production. Although the commercial tomato is susceptible to <i>T. absoluta</i> attacks, a better understanding of the defensive plant responses to this pest will help in defining plant resistance traits and broaden the range of agronomic levers that can be used for an effective integrated pest management strategy over the crop cycle. In this study, we developed an integrative approach combining untargeted metabolomic and transcriptomic analyses to characterize the local and systemic metabolic responses of young tomato plants to <i>T. absoluta</i> larvae herbivory. From metabolomic analyses, the tomato response appeared to be both local and systemic, with a local response in infested leaves being much more intense than in other parts of the plant. The main response was a massive accumulation of phenolamides with great structural diversity, including rare derivatives composed of spermine and dihydrocinnamic acids. The accumulation of this family of specialized metabolites was supported by transcriptomic data, which showed induction of both phenylpropanoid and polyamine precursor pathways. Moreover, our transcriptomic data identified two genes strongly induced by <i>T. absoluta</i> herbivory, that we functionally characterized as putrescine hydroxycinnamoyl transferases. They catalyze the biosynthesis of several phenolamides, among which is caffeoylputrescine. Overall, this study provided new mechanistic clues of the tomato/<i>T. absoluta</i> interaction. |
| first_indexed | 2024-03-09T23:05:28Z |
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| institution | Directory Open Access Journal |
| issn | 2218-1989 |
| language | English |
| last_indexed | 2024-03-09T23:05:28Z |
| publishDate | 2022-05-01 |
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| record_format | Article |
| series | Metabolites |
| spelling | doaj.art-f7d4f916221c4074a44d32f8ac85d80c2023-11-23T17:55:25ZengMDPI AGMetabolites2218-19892022-05-0112648410.3390/metabo12060484Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i>Marwa Roumani0Jacques Le Bot1Michel Boisbrun2Florent Magot3Arthur Péré4Christophe Robin5Frédérique Hilliou6Romain Larbat7UMR1121 Laboratoire Agronomie et Environnement (LAE), Université de Lorraine, INRAE, F-54000 Nancy, FranceINRAE, UR1115 Plantes et Systèmes de Culture Horticole, 84000 Avignon, FranceCNRS, L2CM, Université de Lorraine, F-54000 Nancy, FranceUMR1121 Laboratoire Agronomie et Environnement (LAE), Université de Lorraine, INRAE, F-54000 Nancy, FranceINRAE, Institut Sophia Agrobiotech, Université Côte D’Azur, CNRS, F-06903 Sophia Antipolis, FranceUMR1121 Laboratoire Agronomie et Environnement (LAE), Université de Lorraine, INRAE, F-54000 Nancy, FranceINRAE, Institut Sophia Agrobiotech, Université Côte D’Azur, CNRS, F-06903 Sophia Antipolis, FranceUMR1121 Laboratoire Agronomie et Environnement (LAE), Université de Lorraine, INRAE, F-54000 Nancy, FranceTomato plants are attacked by a variety of herbivore pests and among them, the leafminer <i>Tuta absoluta</i>, which is currently a major threat to global tomato production. Although the commercial tomato is susceptible to <i>T. absoluta</i> attacks, a better understanding of the defensive plant responses to this pest will help in defining plant resistance traits and broaden the range of agronomic levers that can be used for an effective integrated pest management strategy over the crop cycle. In this study, we developed an integrative approach combining untargeted metabolomic and transcriptomic analyses to characterize the local and systemic metabolic responses of young tomato plants to <i>T. absoluta</i> larvae herbivory. From metabolomic analyses, the tomato response appeared to be both local and systemic, with a local response in infested leaves being much more intense than in other parts of the plant. The main response was a massive accumulation of phenolamides with great structural diversity, including rare derivatives composed of spermine and dihydrocinnamic acids. The accumulation of this family of specialized metabolites was supported by transcriptomic data, which showed induction of both phenylpropanoid and polyamine precursor pathways. Moreover, our transcriptomic data identified two genes strongly induced by <i>T. absoluta</i> herbivory, that we functionally characterized as putrescine hydroxycinnamoyl transferases. They catalyze the biosynthesis of several phenolamides, among which is caffeoylputrescine. Overall, this study provided new mechanistic clues of the tomato/<i>T. absoluta</i> interaction.https://www.mdpi.com/2218-1989/12/6/484tomatoleafminer<i>Tuta absoluta</i>phenolamidemetabolomicstranscriptomics |
| spellingShingle | Marwa Roumani Jacques Le Bot Michel Boisbrun Florent Magot Arthur Péré Christophe Robin Frédérique Hilliou Romain Larbat Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i> Metabolites tomato leafminer <i>Tuta absoluta</i> phenolamide metabolomics transcriptomics |
| title | Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i> |
| title_full | Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i> |
| title_fullStr | Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i> |
| title_full_unstemmed | Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i> |
| title_short | Transcriptomics and Metabolomics Analyses Reveal High Induction of the Phenolamide Pathway in Tomato Plants Attacked by the Leafminer <i>Tuta absoluta</i> |
| title_sort | transcriptomics and metabolomics analyses reveal high induction of the phenolamide pathway in tomato plants attacked by the leafminer i tuta absoluta i |
| topic | tomato leafminer <i>Tuta absoluta</i> phenolamide metabolomics transcriptomics |
| url | https://www.mdpi.com/2218-1989/12/6/484 |
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