Differential content of leaf and fruit pigment in tomatoes culminate in a complex metabolic reprogramming without growth impacts

Although significant efforts to produce carotenoid-enriched foods either by biotechnology or traditional breeding strategies have been carried out, our understanding of how changes in the carotenoid biosynthesis might affect overall plant performance remains limited. Here, we investigate how the metabolic machinery of well characterized tomato carotenoid mutant plants [namely crimson (old gold-og), Delta carotene (Del) and tangerine (t)] adjusts itself to varying carotenoid biosynthesis and whether these adjustments are supported by a reprogramming of photosynthetic and central metabolism in the source organs (leaves). We observed that mutations og, Del and t did not greatly affect vegetative growth, leaf anatomy and gas exchange parameters. However, an exquisite metabolic reprogramming was recorded on the leaves, with an increase in levels of amino acids and reduction of organic acids. Taken together, our results show that despite minor impacts on growth and gas exchange, carbon flux is extensively affected, leading to adjustments in tomato leaves metabolism to support changes in carotenoid biosynthesis on fruits (sinks). We discuss these data in the context of our current understanding of metabolic adjustments and carotenoid biosynthesis as well as regarding to improving human nutrition.