Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato

Author(s)
Alfonso Albacete, Elena Cantero-Navarro, Dominik K. Großinsky, Cintia L. Arias, Maria Encarnation Balibrea, Roque Bru, Lena Fragner, Michael E. Ghanem, Maria de la Cruz Gonzalez, Jose A. Hernandez, Cristina Martinez-Andujar, Eric van der Graaff, Wolfram Weckwerth, Günther Zellnig, Francisco Perez-Alfocea, Thomas Roitsch
Abstract

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.

Organisation(s)
External organisation(s)
Karl-Franzens-Universität Graz, Centro de Edafologia y Biologia Aplicada del Segura, Universidad Nacional de Rosario, Universidad de Alicante, Universidad de Sevilla
Journal
Journal of Experimental Botany
Volume
66
Pages
863-878
No. of pages
16
ISSN
0022-0957
DOI
https://doi.org/10.1093/jxb/eru448
Publication date
02-2015
Peer reviewed
Yes
Austrian Fields of Science 2012
106002 Biochemistry, 106031 Plant physiology, 106030 Plant ecology
Keywords
ASJC Scopus subject areas
Physiology, Plant Science
Portal url
https://ucris.univie.ac.at/portal/en/publications/ectopic-overexpression-of-the-cell-wall-invertase-gene-cin1-leads-to-dehydration-avoidance-in-tomato(0aa0c738-242c-4fa7-9089-a09bba230965).html