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Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress

Interest in the role of small bioactive molecules (< 500 Da) in plants is on the rise, compelled by plant scientists' attempt to unravel their mode of action implicated in stimulating growth and enhancing tolerance to environmental stressors. The current study aimed at elucidating the morpho...

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Autores principales: Rouphael, Youssef, Raimondi, Giampaolo, Lucini, Luigi, Carillo, Petronia, Kyriacou, Marios C., Colla, Giuseppe, Cirillo, Valerio, Pannico, Antonio, El-Nakhel, Christophe, De Pascale, Stefania
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5835327/
https://www.ncbi.nlm.nih.gov/pubmed/29535755
http://dx.doi.org/10.3389/fpls.2018.00249
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author Rouphael, Youssef
Raimondi, Giampaolo
Lucini, Luigi
Carillo, Petronia
Kyriacou, Marios C.
Colla, Giuseppe
Cirillo, Valerio
Pannico, Antonio
El-Nakhel, Christophe
De Pascale, Stefania
author_facet Rouphael, Youssef
Raimondi, Giampaolo
Lucini, Luigi
Carillo, Petronia
Kyriacou, Marios C.
Colla, Giuseppe
Cirillo, Valerio
Pannico, Antonio
El-Nakhel, Christophe
De Pascale, Stefania
author_sort Rouphael, Youssef
collection PubMed
description Interest in the role of small bioactive molecules (< 500 Da) in plants is on the rise, compelled by plant scientists' attempt to unravel their mode of action implicated in stimulating growth and enhancing tolerance to environmental stressors. The current study aimed at elucidating the morphological, physiological and metabolomic changes occurring in greenhouse tomato (cv. Seny) treated with omeprazole (OMP), a benzimidazole inhibitor of animal proton pumps. The OMP was applied at three rates (0, 10, or 100 μM) as substrate drench for tomato plants grown under nonsaline (control) or saline conditions sustained by nutrient solutions of 1 or 75 mM NaCl, respectively. Increasing NaCl concentration from 1 to 75 mM decreased the tomato shoot dry weight by 49% in the 0 μM OMP treatment, whereas the reduction was not significant at 10 or 100 μM of OMP. Treatment of salinized (75 mM NaCl) tomato plants with 10 and especially 100 μM OMP decreased Na(+) and Cl(−) while it increased Ca(2+) concentration in the leaves. However, OMP was not strictly involved in ion homeostasis since the K(+) to Na(+) ratio did not increase under combined salinity and OMP treatment. OMP increased root dry weight, root morphological characteristics (total length and surface), transpiration, and net photosynthetic rate independently of salinity. Metabolic profiling of leaves through UHPLC liquid chromatography coupled to quadrupole-time-of-flight mass spectrometry facilitated identification of the reprogramming of a wide range of metabolites in response to OMP treatment. Hormonal changes involved an increase in ABA, decrease in auxins and cytokinin, and a tendency for GA down accumulation. Cutin biosynthesis, alteration of membrane lipids and heightened radical scavenging ability related to the accumulation of phenolics and carotenoids were observed. Several other stress-related compounds, such as polyamine conjugates, alkaloids and sesquiterpene lactones, were altered in response to OMP. Although a specific and well-defined mechanism could not be posited, the metabolic processes involved in OMP action suggest that this small bioactive molecule might have a hormone-like activity that ultimately elicits an improved tolerance to NaCl salinity stress.
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spelling pubmed-58353272018-03-13 Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress Rouphael, Youssef Raimondi, Giampaolo Lucini, Luigi Carillo, Petronia Kyriacou, Marios C. Colla, Giuseppe Cirillo, Valerio Pannico, Antonio El-Nakhel, Christophe De Pascale, Stefania Front Plant Sci Plant Science Interest in the role of small bioactive molecules (< 500 Da) in plants is on the rise, compelled by plant scientists' attempt to unravel their mode of action implicated in stimulating growth and enhancing tolerance to environmental stressors. The current study aimed at elucidating the morphological, physiological and metabolomic changes occurring in greenhouse tomato (cv. Seny) treated with omeprazole (OMP), a benzimidazole inhibitor of animal proton pumps. The OMP was applied at three rates (0, 10, or 100 μM) as substrate drench for tomato plants grown under nonsaline (control) or saline conditions sustained by nutrient solutions of 1 or 75 mM NaCl, respectively. Increasing NaCl concentration from 1 to 75 mM decreased the tomato shoot dry weight by 49% in the 0 μM OMP treatment, whereas the reduction was not significant at 10 or 100 μM of OMP. Treatment of salinized (75 mM NaCl) tomato plants with 10 and especially 100 μM OMP decreased Na(+) and Cl(−) while it increased Ca(2+) concentration in the leaves. However, OMP was not strictly involved in ion homeostasis since the K(+) to Na(+) ratio did not increase under combined salinity and OMP treatment. OMP increased root dry weight, root morphological characteristics (total length and surface), transpiration, and net photosynthetic rate independently of salinity. Metabolic profiling of leaves through UHPLC liquid chromatography coupled to quadrupole-time-of-flight mass spectrometry facilitated identification of the reprogramming of a wide range of metabolites in response to OMP treatment. Hormonal changes involved an increase in ABA, decrease in auxins and cytokinin, and a tendency for GA down accumulation. Cutin biosynthesis, alteration of membrane lipids and heightened radical scavenging ability related to the accumulation of phenolics and carotenoids were observed. Several other stress-related compounds, such as polyamine conjugates, alkaloids and sesquiterpene lactones, were altered in response to OMP. Although a specific and well-defined mechanism could not be posited, the metabolic processes involved in OMP action suggest that this small bioactive molecule might have a hormone-like activity that ultimately elicits an improved tolerance to NaCl salinity stress. Frontiers Media S.A. 2018-02-27 /pmc/articles/PMC5835327/ /pubmed/29535755 http://dx.doi.org/10.3389/fpls.2018.00249 Text en Copyright © 2018 Rouphael, Raimondi, Lucini, Carillo, Kyriacou, Colla, Cirillo, Pannico, El-Nakhel and De Pascale. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Rouphael, Youssef
Raimondi, Giampaolo
Lucini, Luigi
Carillo, Petronia
Kyriacou, Marios C.
Colla, Giuseppe
Cirillo, Valerio
Pannico, Antonio
El-Nakhel, Christophe
De Pascale, Stefania
Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress
title Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress
title_full Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress
title_fullStr Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress
title_full_unstemmed Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress
title_short Physiological and Metabolic Responses Triggered by Omeprazole Improve Tomato Plant Tolerance to NaCl Stress
title_sort physiological and metabolic responses triggered by omeprazole improve tomato plant tolerance to nacl stress
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5835327/
https://www.ncbi.nlm.nih.gov/pubmed/29535755
http://dx.doi.org/10.3389/fpls.2018.00249
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