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High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber
Nowadays open field and protected vegetable cultivation practices require and use genotypes which are precisely tailored to their intended growth environments. Variability of this kind provides a rich source of material to uncover molecular mechanisms supporting the necessarily divergent physiologic...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10051573/ https://www.ncbi.nlm.nih.gov/pubmed/36986979 http://dx.doi.org/10.3390/plants12061292 |
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author | Hesari, Neda Szegő, Anita Mirmazloum, Iman Pónya, Zsolt Kiss-Bába, Erzsébet Kolozs, Henriett Gyöngyik, Márta Vasas, Dominika Papp, István |
author_facet | Hesari, Neda Szegő, Anita Mirmazloum, Iman Pónya, Zsolt Kiss-Bába, Erzsébet Kolozs, Henriett Gyöngyik, Márta Vasas, Dominika Papp, István |
author_sort | Hesari, Neda |
collection | PubMed |
description | Nowadays open field and protected vegetable cultivation practices require and use genotypes which are precisely tailored to their intended growth environments. Variability of this kind provides a rich source of material to uncover molecular mechanisms supporting the necessarily divergent physiological traits. In this study, typical field-optimized and glasshouse-cultivated cucumber F1 hybrids were investigated, and displayed slower growth (‘Joker’) and faster growth (‘Oitol’) in seedlings. Antioxidant capacity was lower in ‘Joker’ and higher in ‘Oitol’, pointing to a potential redox regulation of growth. The growth response of seedlings to paraquat treatment indicated stronger oxidative stress tolerance in the fast-growing ‘Oitol’. To test whether protection against nitrate-induced oxidative stress was also different, fertigation with increasing potassium nitrate content was applied. This treatment did not change growth but decreased the antioxidant capacities of both hybrids. Bioluminescence emission revealed stronger lipid peroxidation triggered by high nitrate fertigation in the leaves of ‘Joker’ seedlings. To explore the background of the more effective antioxidant protection of ‘Oitol’, levels of ascorbic acid (AsA), as well as transcriptional regulation of relevant genes of the Smirnoff–Wheeler biosynthetic pathway and ascorbate recycling, were investigated. Genes related to AsA biosynthesis were strongly upregulated at an elevated nitrate supply in ‘Oitol’ leaves only, but this was only reflected in a small increase in total AsA content. High nitrate provision also triggered expression of ascorbate–glutathion cycle genes with stronger or exclusive induction in ‘Oitol’. AsA/dehydro–ascorbate ratios were higher in ‘Oitol’ for all treatments, with a more pronounced difference at high nitrate levels. Despite strong transcriptional upregulation of ascorbate peroxidase genes (APX) in ‘Oitol’, APX activity only increased significantly in ‘Joker’. This suggests potential inhibition of APX enzyme activity specifically in ‘Oitol’ at a high nitrate supply. Our results uncover an unexpected variability in redox stress management in cucumbers, including nitrate inducibility of AsA biosynthetic and recycling pathways in certain genotypes. Possible connections between AsA biosynthesis, recycling and nitro-oxidative stress protection are discussed. Cucumber hybrids emerge as an excellent model system for studying the regulation of AsA metabolism and the roles of AsA in growth and stress tolerance. |
format | Online Article Text |
id | pubmed-10051573 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-100515732023-03-30 High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber Hesari, Neda Szegő, Anita Mirmazloum, Iman Pónya, Zsolt Kiss-Bába, Erzsébet Kolozs, Henriett Gyöngyik, Márta Vasas, Dominika Papp, István Plants (Basel) Article Nowadays open field and protected vegetable cultivation practices require and use genotypes which are precisely tailored to their intended growth environments. Variability of this kind provides a rich source of material to uncover molecular mechanisms supporting the necessarily divergent physiological traits. In this study, typical field-optimized and glasshouse-cultivated cucumber F1 hybrids were investigated, and displayed slower growth (‘Joker’) and faster growth (‘Oitol’) in seedlings. Antioxidant capacity was lower in ‘Joker’ and higher in ‘Oitol’, pointing to a potential redox regulation of growth. The growth response of seedlings to paraquat treatment indicated stronger oxidative stress tolerance in the fast-growing ‘Oitol’. To test whether protection against nitrate-induced oxidative stress was also different, fertigation with increasing potassium nitrate content was applied. This treatment did not change growth but decreased the antioxidant capacities of both hybrids. Bioluminescence emission revealed stronger lipid peroxidation triggered by high nitrate fertigation in the leaves of ‘Joker’ seedlings. To explore the background of the more effective antioxidant protection of ‘Oitol’, levels of ascorbic acid (AsA), as well as transcriptional regulation of relevant genes of the Smirnoff–Wheeler biosynthetic pathway and ascorbate recycling, were investigated. Genes related to AsA biosynthesis were strongly upregulated at an elevated nitrate supply in ‘Oitol’ leaves only, but this was only reflected in a small increase in total AsA content. High nitrate provision also triggered expression of ascorbate–glutathion cycle genes with stronger or exclusive induction in ‘Oitol’. AsA/dehydro–ascorbate ratios were higher in ‘Oitol’ for all treatments, with a more pronounced difference at high nitrate levels. Despite strong transcriptional upregulation of ascorbate peroxidase genes (APX) in ‘Oitol’, APX activity only increased significantly in ‘Joker’. This suggests potential inhibition of APX enzyme activity specifically in ‘Oitol’ at a high nitrate supply. Our results uncover an unexpected variability in redox stress management in cucumbers, including nitrate inducibility of AsA biosynthetic and recycling pathways in certain genotypes. Possible connections between AsA biosynthesis, recycling and nitro-oxidative stress protection are discussed. Cucumber hybrids emerge as an excellent model system for studying the regulation of AsA metabolism and the roles of AsA in growth and stress tolerance. MDPI 2023-03-13 /pmc/articles/PMC10051573/ /pubmed/36986979 http://dx.doi.org/10.3390/plants12061292 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Hesari, Neda Szegő, Anita Mirmazloum, Iman Pónya, Zsolt Kiss-Bába, Erzsébet Kolozs, Henriett Gyöngyik, Márta Vasas, Dominika Papp, István High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber |
title | High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber |
title_full | High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber |
title_fullStr | High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber |
title_full_unstemmed | High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber |
title_short | High-Nitrate-Supply-Induced Transcriptional Upregulation of Ascorbic Acid Biosynthetic and Recycling Pathways in Cucumber |
title_sort | high-nitrate-supply-induced transcriptional upregulation of ascorbic acid biosynthetic and recycling pathways in cucumber |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10051573/ https://www.ncbi.nlm.nih.gov/pubmed/36986979 http://dx.doi.org/10.3390/plants12061292 |
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