Drought stress conditions modify source-sink relations, thereby influencing plant growth, adaptive responses, and consequently crop yield. Invertases are key metabolic enzymes regulating sink activity through the hydrolytic cleavage of sucrose into hexose monomers, thus playing a crucial role in plant growth and development. However, the physiological role of invertases during adaptation to abiotic stress conditions is not yet fully understood. Here it is shown that plant adaptation to drought stress can be markedly improved in tomato (Solanum lycopersicum L.) by overexpression of the cell wall invertase (cwInv) gene CIN1 from Chenopodium rubrum. CIN1 overexpression limited stomatal conductance under normal watering regimes, leading to reduced water consumption during the drought period, while photosynthetic activity was maintained. This caused a strong increase in water use efficiency (up to 50%), markedly improving water stress adaptation through an efficient physiological strategy of dehydration avoidance. Drought stress strongly reduced cwInv activity and induced its proteinaceous inhibitor in the leaves of the wild-type plants. However, the CIN1-overexpressing plants registered 3- to 6-fold higher cwInv activity in all analysed conditions. Surprisingly, the enhanced invertase activity did not result in increased hexose concentrations due to the activation of the metabolic carbohydrate fluxes, as reflected by the maintenance of the activity of key enzymes of primary metabolism and increased levels of sugar-phosphate intermediates under water deprivation. The induced sink metabolism in the leaves explained the maintenance of photosynthetic activity, delayed senescence, and increased source activity under drought stress. Moreover, CIN1 plants also presented a better control of production of reactive oxygen species and sustained membrane protection. Those metabolic changes conferred by CIN1 overexpression were accompanied by increases in the concentrations of the senescence-delaying hormone trans-zeatin and decreases in the senescence-inducing ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) in the leaves. Thus, cwInv critically functions at the integration point of metabolic, hormonal, and stress signals, providing a novel strategy to overcome drought-induced limitations to crop yield, without negatively affecting plant fitness under optimal growth conditions.

Centro de Estudios Fotosintéticos y Bioquímicos Universidad Nacional de Rosario Suipacha 531 2000 Rosario Argentina

Departamento de Agroquímica y Bioquímica Facultad de Ciencias Universidad de Alicante 03080 Alicante Spain

Department of Fruit Breeding CEBAS CSIC Campus de Espinardo 30100 Murcia Spain

Department of Molecular Systems Biology Faculty of Life Sciences University of Vienna 1090 Vienna Austria

Department of Plant Nutrition CEBAS CSIC Campus de Espinardo 30100 Murcia Spain

Department of Plant Nutrition CEBAS CSIC Campus de Espinardo 30100 Murcia Spain Institute of Plant Sciences Department of Plant Physiology University of Graz 8010 Graz Austria

Institute of Plant Sciences Department of Plant Physiology University of Graz 8010 Graz Austria

Institute of Plant Sciences Department of Plant Physiology University of Graz 8010 Graz Austria Department of Plant and Environmental Sciences Copenhagen Plant Science Centre University of Copenhagen Højbakkegård Allé 13 DK 2630 Taastrup Denmark

Institute of Plant Sciences Department of Plant Physiology University of Graz 8010 Graz Austria Department of Plant and Environmental Sciences Copenhagen Plant Science Centre University of Copenhagen Højbakkegård Allé 13 DK 2630 Taastrup Denmark Global Change Research Centre Czech Globe AS CR v v i Drásov 470 Cz 664 24 Drásov Czech Republic

Instituto de Bioquímica Vegetal y Fotosíntesis Universidad de Sevilla CSIC 41092 Sevilla Spain

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J Exp Bot. 2015 Jun;66(11):3431-2. doi: 10.1093/jxb/erv134. PubMed

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