Respiration climacteric in tomato fruits elucidated by constraint-based modelling

Tomato is a model organism to study the development of fleshy fruit including ripeninginitiation. Unfortunately, few studies deal with the brief phase of accelerated ripeningassociated with the respiration climactericbecause of practical problems involved in measuring fruit respiration. Because constraint-based modelling allows predicting accurate metabolic fluxes, we investigated the respirationand energy dissipation of fruit pericarp at the breaker stage using a detailed stoichiometric model of the respiratory pathway, including alternative oxidaseand 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 CO2 released and an excess of energy dissipated at 40 d post anthesis(DPA) just before the onset of ripeningcoinciding with the respiration climacteric. We demonstrated the unbalanced carbon allocation with the sharp slowdownof 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 respirationand to elucidate the underlying mechanisms of ripening.