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,Johann Petit,Jean-Paul Bouchet,Cécile Garchery,Virginie Garcia,Annick Moing,Vincent Truffault,Barbara Gouble,Mathilde Causse,Christophe Rothan,Jean-Luc Poëssel,Pierre Baldet,Claire Deschodt,Hélène Gautier,Mickaël Maucourt,Mireille Faurobert,David Page,Catherine Deborde

doi:10.3389/fpls.2018.00137

Abstract

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.

Highlights

Tomato has emerged as a model fruit for studying the relationships between ascorbate and fruit physiology
The three RNA interference (RNAi) transgenic lines (AO: ascorbate oxidase; GLD: galactonolactone dehydrogenase and MDHAR: monodehydroascorbate reductase) and wild-type plants grown in the greenhouse were subjected to simple phenotypic analyses to measure plant height, growth rate and final leaf area, the duration of fruit ripening and fruit weight were measured
The results for the plant phenotypes are shown in Table 1: AO and GLD RNAi lines had a slower growth rate and a smaller final plant height compared to wild-type plants

Summary

Introduction

Tomato has emerged as a model fruit for studying the relationships between ascorbate and fruit physiology. Studying the interactions between the ascorbate pool and fruit ripening is of particular interest because the vast majority of fresh market tomatoes produced in Europe are harvested at orange or light-red stages, before being fully ripe. At these stages, fruit undergo major modifications in color, firmness, sweetness, acidity, and aroma. Fruit undergo major modifications in color, firmness, sweetness, acidity, and aroma These changes are under developmental and hormonal control and imply profound alterations in the transcriptome, proteome and metabolome (Klee and Giovannoni, 2011). The mechanisms by which ascorbate impinges on fruit physiology remain to be deciphered

Methods

Results

Conclusion