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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 Rebecca Stevens, Pierre Baldet, Jean-Paul Bouchet, Mathilde Causse, Catherine Deborde, Claire Deschodt, Mireille Faurobert, Cecile Garchery, Virginie Garcia, Hélène Gautier, et al. To cite this version: Rebecca Stevens, Pierre Baldet, Jean-Paul Bouchet, Mathilde Causse, Catherine Deborde, et al.. 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, Frontiers, 2018, 9 (137), 16 p. 10.3389/fpls.2018.00137. hal-01721265 HAL Id: hal-01721265 https://hal.archives-ouvertes.fr/hal-01721265 Submitted on 1 Mar 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License ORIGINAL RESEARCH published: 14 February 2018 doi: 10.3389/fpls.2018.00137 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 Rebecca G. Stevens 1*, Pierre Baldet 2, Jean-Paul Bouchet 1, Mathilde Causse 1, Catherine Deborde 2,3, Claire Deschodt 1, Mireille Faurobert 1, Cécile Garchery 1, Virginie Garcia 2, Hélène Gautier 4, Barbara Gouble 5, Mickaël Maucourt 2,3, Annick Moing 2,3, David Page 5, Johann Petit 2, Jean-Luc Poëssel 1, Vincent Truffault 1 and Christophe Rothan 2 1 Institut National de la Recherche Agronomique, UR1052, Génétique et Amélioration des Fruits et Légumes, Montfavet, France, 2 Institut National de la Recherche Agronomique, Université de Bordeaux, UMR1332, Biologie du Fruit et Pathologie, Edited by: Villenave d’Ornon, France, 3 Plateforme Métabolome du Centre de Génomique Fonctionnelle Bordeaux, Centre Institut Atsushi Fukushima, National de la Recherche Agronomique de Bordeaux, Villenave d’Ornon, France, 4 Institut National de la Recherche RIKEN, Japan Agronomique, UR1115, Plantes et Systèmes de culture Horticoles, Avignon, France, 5 Institut National de la Recherche Reviewed by: Agronomique, Université d’Avignon et des Pays du Vaucluse, UMR408 Sécurité et Qualité des Produits d’Origine Végétale, Victoriano Valpuesta, Avignon, France University of Málaga, Spain Jedrzej Jakub Szymanski, Changing the balance between ascorbate, monodehydroascorbate, and Weizmann Institute of Science, Israel dehydroascorbate in plant cells by manipulating the activity of enzymes involved *Correspondence: Rebecca G. Stevens in ascorbate synthesis or recycling of oxidized and reduced forms leads to [email protected] multiple phenotypes. A systems biology approach including network analysis of the transcriptome, proteome and metabolites of RNAi lines for ascorbate oxidase, Specialty section: This article was submitted to monodehydroascorbate reductase and galactonolactone dehydrogenase has been Plant Systems and Synthetic Biology, carried out in orange fruit pericarp of tomato (Solanum lycopersicum). The transcriptome a section of the journal Frontiers in Plant Science of the RNAi ascorbate oxidase lines is inversed compared to the monodehydroascorbate Received: 09 October 2017 reductase and galactonolactone dehydrogenase lines. Differentially expressed genes are Accepted: 24 January 2018 involved in ribosome biogenesis and translation. This transcriptome inversion is also seen Published: 14 February 2018 in response to different stresses in Arabidopsis. The transcriptome response is not well Citation: correlated with the proteome which, with the metabolites, are correlated to the activity Stevens RG, Baldet P, Bouchet J-P, Causse M, Deborde C, Deschodt C, of the ascorbate redox enzymes—ascorbate oxidase and monodehydroascorbate Faurobert M, Garchery C, Garcia V, reductase. Differentially accumulated proteins include metacaspase, protein disulphide Gautier H, Gouble B, Maucourt M, Moing A, Page D, Petit J, Poëssel J-L, isomerase, chaperone DnaK and carbonic anhydrase and the metabolites chlorogenic Truffault V and Rothan C (2018) A acid, dehydroascorbate and alanine. The hub genes identified from the network analysis Systems Biology Study in Tomato Fruit are involved in signaling, the heat-shock response and ribosome biogenesis. The results Reveals Correlations between the Ascorbate Pool and Genes Involved in from this study therefore reveal one or several putative signals from the ascorbate pool Ribosome Biogenesis, Translation, which modify the transcriptional response and elements downstream. and the Heat-Shock Response. Front. Plant Sci. 9:137. Keywords: ascorbate, cellular signaling, heat-shock response, redox, ribosome biogenesis, translation, tomato doi: 10.3389/fpls.2018.00137 (Solanum lycopersicum) Frontiers in Plant Science | www.frontiersin.org 1 February 2018 | Volume 9 | Article 137 Stevens et al. Ascorbate Signaling in Tomato Fruit INTRODUCTION These enzymes are dioxygenases and therefore this is an example of a role for ascorbate as an electron donor to iron-dependent Tomato has emerged as a model fruit for studying the oxidoreductases. Ascorbate is also involved in oxidative protein relationships between ascorbate and fruit physiology. In addition folding in the endoplasmic reticulum and therefore plays a role to its nutritional value, ascorbate is a major antioxidant that in protein maturation (Banhegyi et al., 2003; Zito et al., 2012; contributes to fruit tolerance to biotic and abiotic stresses Szarka and Lorincz, 2014). Dehydroascorbate has been shown (Malacrida et al., 2006; Davey et al., 2007; Stevens et al., to have a role in neuronal energy metabolism via activation 2008). Studying the interactions between the ascorbate pool of glucose-6-phosphate dehydrogenase thus increasing flux and fruit ripening is of particular interest because the vast through the pentose phosphate pathway (Puskas et al., 2000; majority of fresh market tomatoes produced in Europe are Cisternas et al., 2014). Furthermore, ascorbate has been identified harvested at orange or light-red stages, before being fully ripe. as a kinase inhibitor (Carcamo et al., 2004) as well as an inhibitor At these stages, fruit undergo major modifications in color, of hexokinase (Fiorani et al., 2000) and its oxidized form can firmness, sweetness, acidity, and aroma. These changes are inhibit glyceraldehyde 3-phosphate dehydrogenase leading to an under developmental and hormonal control and imply profound energetic crisis and cell death in cancer cells which uptake more alterations in the transcriptome, proteome and metabolome dehydroascorbate via glucose transporters (Yun et al., 2015). (Klee and Giovannoni, 2011). In a previous study, we showed These examples have not been shown in plants: the study of ◦ that chilling stress conditions (<10 C) that can prevail during ascorbate in non-photosynthetic tissues may be key to revealing postharvest transport and storage affect fruit firmness, and that additional functions for the molecule; fruit is an ideal tissue, this effect is correlated with the ascorbate oxidation status particularly in advanced ripening stages when photosynthetic (Stevens et al., 2008). However, the mechanisms by which activity is low. ascorbate impinges on fruit physiology remain to be deciphered. Ascorbate’s functions are profoundly affected by the oxidation Ripening fruit are non-photosynthetic sink tissues relying state of the ascorbate pool: ascorbate is oxidized to the on import of sucrose for providing reducing power, ATP, and monodehydroascorbate radical, a relatively stable radical, which precursor molecules necessary for synthesis of fruit-specific can regain an electron to regenerate ascorbate, or lose a second metabolites or proteins. The conversion of sucrose into hexose- electron to become dehydroascorbate; these three forms are phosphates is the starting point for glycolysis, the TCA cycle in equilibrium (Bors and Buettner, 1997). Plants also possess and the oxidative pentose phosphate pathway which provide ascorbate oxidase enzymes which have roles in oxygen removal the tissue with its metabolic and energetic requirements. The and signaling (De Tullio et al., 2007; De Tullio, 2012). Ascorbate fruit therefore represents a complex biological system built on oxidase activity has also been shown to have links with sugar multi-layered interactions between metabolites, proteins and metabolism and yield (Garchery et al., 2013), in a similar way genes which form a network characteristic of the tissue. Induced to an isoform of monodehydroascorbate reductase (MDHAR), genetic modifications are a good way of perturbing the system except that the phenotypes are inverted (Truffault et al., 2016): by varying the level of a gene and its corresponding protein plants with reduced MDHAR activity show reduced growth and/or metabolites (network nodes) to evaluate the new steady and yield and lower levels of sugars (sucrose and hexose) state of the network, thus pinpointing the interactions that