Improving yield, nutritional value and tolerance to abiotic stress are major targets of current breeding and biotechnological approaches that aim at increasing crop production and ensuring food security. Metabolic engineering of carotenoids, the precursor of vitamin-A and plant hormones that regulate plant growth and response to adverse growth conditions, has been mainly focusing on provitamin A biofortification or the production of high-value carotenoids. Here, we show that the introduction of a single gene of the carotenoid biosynthetic pathway in different tomato cultivars induced profound metabolic alterations in carotenoid, apocarotenoid and phytohormones pathways. Alterations in isoprenoid- (abscisic acid, gibberellins, cytokinins) and non-isoprenoid (auxin and jasmonic acid) derived hormones together with enhanced xanthophyll content influenced biomass partitioning and abiotic stress tolerance (high light, salt, and drought), and it caused an up to 77% fruit yield increase and enhanced fruit's provitamin A content. In addition, metabolic and hormonal changes led to accumulation of key primary metabolites (e.g. osmoprotectants and antiaging agents) contributing with enhanced abiotic stress tolerance and fruit shelf life. Our findings pave the way for developing a new generation of crops that combine high productivity and increased nutritional value with the capability to cope with climate change-related environmental challenges.

Aix Marseille University CEA CNRS UMR7265 BIAM CEA Cadarache F 13108 Saint Paul lez Durance France

Center for Desert Agriculture Biological and Environmental Science and Engineering Division Thuwal Saudi Arabia

Center for Desert Agriculture Biological and Environmental Science and Engineering Division Thuwal Saudi Arabia; Max Planck Institut für Molekulare Pflanzenphysiologie Am Mühlenberg1 D 14476 Potsdam Golm Germany

Institute for Plant Molecular and Cell Biology UPV CSIC 46022 Valencia Spain

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany The Czech Academy of Sciences Šlechtitelů 27 CZ 78371 Olomouc Czech Republic

Max Planck Institut für Molekulare Pflanzenphysiologie Am Mühlenberg1 D 14476 Potsdam Golm Germany

Max Planck Institut für Molekulare Pflanzenphysiologie Am Mühlenberg1 D 14476 Potsdam Golm Germany; Boyce Thompson Institute Cornell University Ithaca NY United States

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