A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock Response
Changing the balance between ascorbate, monodehydroascorbate, and dehydroascorbate in plant cells by manipulating the activity of enzymes involved in ascorbate synthesis or recycling of oxidized and reduced forms leads to multiple phenotypes. A systems biology approach including network analysis of...
| Main Authors: | , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2018-02-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/article/10.3389/fpls.2018.00137/full |
| _version_ | 1818929352801255424 |
|---|---|
| author | Rebecca G. Stevens Pierre Baldet Jean-Paul Bouchet Mathilde Causse Catherine Deborde Catherine Deborde Claire Deschodt Mireille Faurobert Cécile Garchery Virginie Garcia Hélène Gautier Barbara Gouble Mickaël Maucourt Mickaël Maucourt Annick Moing Annick Moing David Page Johann Petit Jean-Luc Poëssel Vincent Truffault Christophe Rothan |
| author_facet | Rebecca G. Stevens Pierre Baldet Jean-Paul Bouchet Mathilde Causse Catherine Deborde Catherine Deborde Claire Deschodt Mireille Faurobert Cécile Garchery Virginie Garcia Hélène Gautier Barbara Gouble Mickaël Maucourt Mickaël Maucourt Annick Moing Annick Moing David Page Johann Petit Jean-Luc Poëssel Vincent Truffault Christophe Rothan |
| author_sort | Rebecca G. Stevens |
| collection | DOAJ |
| description | Changing the balance between ascorbate, monodehydroascorbate, and dehydroascorbate in plant cells by manipulating the activity of enzymes involved in ascorbate synthesis or recycling of oxidized and reduced forms leads to multiple phenotypes. A systems biology approach including network analysis of the transcriptome, proteome and metabolites of RNAi lines for ascorbate oxidase, monodehydroascorbate reductase and galactonolactone dehydrogenase has been carried out in orange fruit pericarp of tomato (Solanum lycopersicum). The transcriptome of the RNAi ascorbate oxidase lines is inversed compared to the monodehydroascorbate reductase and galactonolactone dehydrogenase lines. Differentially expressed genes are involved in ribosome biogenesis and translation. This transcriptome inversion is also seen in response to different stresses in Arabidopsis. The transcriptome response is not well correlated with the proteome which, with the metabolites, are correlated to the activity of the ascorbate redox enzymes—ascorbate oxidase and monodehydroascorbate reductase. Differentially accumulated proteins include metacaspase, protein disulphide isomerase, chaperone DnaK and carbonic anhydrase and the metabolites chlorogenic acid, dehydroascorbate and alanine. The hub genes identified from the network analysis are involved in signaling, the heat-shock response and ribosome biogenesis. The results from this study therefore reveal one or several putative signals from the ascorbate pool which modify the transcriptional response and elements downstream. |
| first_indexed | 2024-12-20T03:43:27Z |
| format | Article |
| id | doaj.art-88a87305f01d4fa0903fe3b09ff3aebe |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-20T03:43:27Z |
| publishDate | 2018-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-88a87305f01d4fa0903fe3b09ff3aebe2022-12-21T19:54:40ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-02-01910.3389/fpls.2018.00137318643A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock ResponseRebecca G. Stevens0Pierre Baldet1Jean-Paul Bouchet2Mathilde Causse3Catherine Deborde4Catherine Deborde5Claire Deschodt6Mireille Faurobert7Cécile Garchery8Virginie Garcia9Hélène Gautier10Barbara Gouble11Mickaël Maucourt12Mickaël Maucourt13Annick Moing14Annick Moing15David Page16Johann Petit17Jean-Luc Poëssel18Vincent Truffault19Christophe Rothan20Institut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Villenave d'Ornon, FranceInstitut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Villenave d'Ornon, FrancePlateforme Métabolome du Centre de Génomique Fonctionnelle Bordeaux, Centre Institut National de la Recherche Agronomique de Bordeaux, Villenave d'Ornon, FranceInstitut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Villenave d'Ornon, FranceInstitut National de la Recherche Agronomique, UR1115, Plantes et Systèmes de culture Horticoles, Avignon, FranceInstitut National de la Recherche Agronomique, Université d'Avignon et des Pays du Vaucluse, UMR408 Sécurité et Qualité des Produits d'Origine Végétale, Avignon, FranceInstitut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Villenave d'Ornon, FrancePlateforme Métabolome du Centre de Génomique Fonctionnelle Bordeaux, Centre Institut National de la Recherche Agronomique de Bordeaux, Villenave d'Ornon, FranceInstitut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Villenave d'Ornon, FrancePlateforme Métabolome du Centre de Génomique Fonctionnelle Bordeaux, Centre Institut National de la Recherche Agronomique de Bordeaux, Villenave d'Ornon, FranceInstitut National de la Recherche Agronomique, Université d'Avignon et des Pays du Vaucluse, UMR408 Sécurité et Qualité des Produits d'Origine Végétale, Avignon, FranceInstitut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Villenave d'Ornon, FranceInstitut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, FranceInstitut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Villenave d'Ornon, FranceChanging the balance between ascorbate, monodehydroascorbate, and dehydroascorbate in plant cells by manipulating the activity of enzymes involved in ascorbate synthesis or recycling of oxidized and reduced forms leads to multiple phenotypes. A systems biology approach including network analysis of the transcriptome, proteome and metabolites of RNAi lines for ascorbate oxidase, monodehydroascorbate reductase and galactonolactone dehydrogenase has been carried out in orange fruit pericarp of tomato (Solanum lycopersicum). The transcriptome of the RNAi ascorbate oxidase lines is inversed compared to the monodehydroascorbate reductase and galactonolactone dehydrogenase lines. Differentially expressed genes are involved in ribosome biogenesis and translation. This transcriptome inversion is also seen in response to different stresses in Arabidopsis. The transcriptome response is not well correlated with the proteome which, with the metabolites, are correlated to the activity of the ascorbate redox enzymes—ascorbate oxidase and monodehydroascorbate reductase. Differentially accumulated proteins include metacaspase, protein disulphide isomerase, chaperone DnaK and carbonic anhydrase and the metabolites chlorogenic acid, dehydroascorbate and alanine. The hub genes identified from the network analysis are involved in signaling, the heat-shock response and ribosome biogenesis. The results from this study therefore reveal one or several putative signals from the ascorbate pool which modify the transcriptional response and elements downstream.http://journal.frontiersin.org/article/10.3389/fpls.2018.00137/fullascorbatecellular signalingheat-shock responseredoxribosome biogenesistranslation |
| spellingShingle | Rebecca G. Stevens Pierre Baldet Jean-Paul Bouchet Mathilde Causse Catherine Deborde Catherine Deborde Claire Deschodt Mireille Faurobert Cécile Garchery Virginie Garcia Hélène Gautier Barbara Gouble Mickaël Maucourt Mickaël Maucourt Annick Moing Annick Moing David Page Johann Petit Jean-Luc Poëssel Vincent Truffault Christophe Rothan A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock Response Frontiers in Plant Science ascorbate cellular signaling heat-shock response redox ribosome biogenesis translation |
| title | A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock Response |
| title_full | A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock Response |
| title_fullStr | A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock Response |
| title_full_unstemmed | A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock Response |
| title_short | A Systems Biology Study in Tomato Fruit Reveals Correlations between the Ascorbate Pool and Genes Involved in Ribosome Biogenesis, Translation, and the Heat-Shock Response |
| title_sort | systems biology study in tomato fruit reveals correlations between the ascorbate pool and genes involved in ribosome biogenesis translation and the heat shock response |
| topic | ascorbate cellular signaling heat-shock response redox ribosome biogenesis translation |
| url | http://journal.frontiersin.org/article/10.3389/fpls.2018.00137/full |
| work_keys_str_mv | AT rebeccagstevens asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT pierrebaldet asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT jeanpaulbouchet asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mathildecausse asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT catherinedeborde asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT catherinedeborde asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT clairedeschodt asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mireillefaurobert asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT cecilegarchery asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT virginiegarcia asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT helenegautier asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT barbaragouble asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mickaelmaucourt asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mickaelmaucourt asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT annickmoing asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT annickmoing asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT davidpage asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT johannpetit asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT jeanlucpoessel asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT vincenttruffault asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT christopherothan asystemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT rebeccagstevens systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT pierrebaldet systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT jeanpaulbouchet systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mathildecausse systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT catherinedeborde systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT catherinedeborde systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT clairedeschodt systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mireillefaurobert systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT cecilegarchery systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT virginiegarcia systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT helenegautier systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT barbaragouble systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mickaelmaucourt systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT mickaelmaucourt systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT annickmoing systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT annickmoing systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT davidpage systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT johannpetit systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT jeanlucpoessel systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT vincenttruffault systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse AT christopherothan systemsbiologystudyintomatofruitrevealscorrelationsbetweentheascorbatepoolandgenesinvolvedinribosomebiogenesistranslationandtheheatshockresponse |