Respiration climacteric in tomato fruits elucidated by constraint-based modelling.

Sophie Colombié,Bertrand Beauvoit,Benoit Biais,Camille Bénard,Yves Gibon,Mickaël Maucourt,Martine Dieuaide‐Noubhani,Sophie Le Gall,Jean‐Pierre Mazat,Stéphane Bernillon,Annick Moing,Christine Nazaret,Cécile Cabasson,Gilles Vercambre

doi:10.1111/nph.14301

Abstract

Summary Tomato is a model organism to study the development of fleshy fruit including ripening initiation. Unfortunately, few studies deal with the brief phase of accelerated ripening associated with the respiration climacteric because of practical problems involved in measuring fruit respiration.Because constraint‐based modelling allows predicting accurate metabolic fluxes, we investigated the respiration and energy dissipation of fruit pericarp at the breaker stage using a detailed stoichiometric model of the respiratory pathway, including alternative oxidase and uncoupling proteins. Assuming steady‐state, a metabolic dataset was transformed into constraints to solve the model on a daily basis throughout tomato fruit development.We detected a peak of CO 2 released and an excess of energy dissipated at 40 d post anthesis (DPA) just before the onset of ripening coinciding with the respiration climacteric. We demonstrated the unbalanced carbon allocation with the sharp slowdown of accumulation (for syntheses and storage) and the beginning of the degradation of starch and cell wall polysaccharides. Experiments with fruits harvested from plants cultivated under stress conditions confirmed the concept.We conclude that modelling with an accurate metabolic dataset is an efficient tool to bypass the difficulty of measuring fruit respiration and to elucidate the underlying mechanisms of ripening.

Highlights

Due to its agronomic importance, tomato (Solanum lycopersicum) has been studied intensively with respect to genetics, physiology and biochemistry, and became an important model for fruit development
The flux-balance model used in this study, which is based on previous work (Beurton-Aimar et al, 2011; Colombie et al, 2015), is a medium-scale knowledge-based model describing central metabolism of heterotrophic plant cells
It simulates the functioning of the tomato fruit pericarp during fruit development, that is, with breakdown and transformation of nutriments to produce energy and metabolic precursors of biomass components

Summary

Introduction

Due to its agronomic importance, tomato (Solanum lycopersicum) has been studied intensively with respect to genetics, physiology and biochemistry, and became an important model for fruit development. It has been reported that for climacteric fruits, such as tomato, mango and kiwifruit, the conversion of starch into soluble sugars is one of the most important events during ripening. These fruits store imported photosynthates in the form of starch in amyloplasts and, as ripening proceeds, this carbon is exported to the cytosol and is thought to be converted into sugars and CO2 (Moing et al, 2001; Han & Kawabata, 2002). At the physiological scale, respiration is defined as the release of CO2, whereas at the biochemical level, the focus tends to be an oxidative metabolism

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