Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato.
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.
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.
Alfonso
A
Albacete
Department of Plant Nutrition, CEBAS-CSIC, Campus de Espinardo, 30100 Murcia, Spain.
Elena
E
Cantero-Navarro
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.
Dominik K
DK
Großkinsky
Centro de Estudios Fotosintéticos y Bioquímicos, Universidad Nacional de Rosario, Suipacha 531, 2000 Rosario, Argentina.
Cintia L
CL
Arias
Department of Plant Nutrition, CEBAS-CSIC, Campus de Espinardo, 30100 Murcia, Spain.
María Encarnación
ME
Balibrea
Departamento de Agroquímica y Bioquímica, Facultad de Ciencias, Universidad de Alicante, 03080 Alicante, Spain.
Roque
R
Bru
Department of Molecular Systems Biology, Faculty of Life Sciences, University of Vienna, 1090 Vienna, Austria.
Lena
L
Fragner
Department of Plant Nutrition, CEBAS-CSIC, Campus de Espinardo, 30100 Murcia, Spain.
Michel E
ME
Ghanem
Instituto de Bioquímica Vegetal y Fotosíntesis, Universidad de Sevilla, CSIC, 41092 Sevilla, Spain.
María de la Cruz
Mde L
González
Department of Fruit Breeding, CEBAS-CSIC, Campus de Espinardo, 30100 Murcia, Spain.
Jose A
JA
Hernández
Department of Plant Nutrition, CEBAS-CSIC, Campus de Espinardo, 30100 Murcia, Spain.
Cristina
C
Martínez-Andújar
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.
Eric
E
van der Graaff
Department of Molecular Systems Biology, Faculty of Life Sciences, University of Vienna, 1090 Vienna, Austria.
Wolfram
W
Weckwerth
Institute of Plant Sciences, Department of Plant Physiology, University of Graz, 8010 Graz, Austria.
Günther
G
Zellnig
Department of Plant Nutrition, CEBAS-CSIC, Campus de Espinardo, 30100 Murcia, Spain alfocea@cebas.csic.es.
Francisco
F
Pérez-Alfocea
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.
Thomas
T
Roitsch
D002473:Cell Wall / Q000201:enzymology*; D027462:Chenopodium / Q000235:genetics* / Q000378:metabolism; D055864:Droughts; D000066630:Ectopic Gene Expression; D018506:Gene Expression Regulation, Plant; D018551:Solanum lycopersicum / Q000201:enzymology / Q000235:genetics / Q000502:physiology*; D010788:Photosynthesis; D018515:Plant Leaves / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D030821:Plants, Genetically Modified / Q000235:genetics / Q000378:metabolism; D043324:beta-Fructofuranosidase / Q000235:genetics* / Q000378:metabolism
D010940:Plant Proteins; D043324:beta-Fructofuranosidase
Cell wall invertase; cytokinins; drought stress; ethylene; source–sink relationships; tomato.