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Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing

The most abundant phenolic compound in Solanaceous plants is chlorogenic acid (CGA), which possesses protective properties such as antimicrobial and antioxidant activities. These properties are particularly relevant when plants are under adverse conditions, such as pathogen attack, excess light, or...

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Autores principales: D’Orso, Fabio, Hill, Lionel, Appelhagen, Ingo, Lawrenson, Tom, Possenti, Marco, Li, Jie, Harwood, Wendy, Morelli, Giorgio, Martin, Cathie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10102458/
https://www.ncbi.nlm.nih.gov/pubmed/37063176
http://dx.doi.org/10.3389/fpls.2023.1124959
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author D’Orso, Fabio
Hill, Lionel
Appelhagen, Ingo
Lawrenson, Tom
Possenti, Marco
Li, Jie
Harwood, Wendy
Morelli, Giorgio
Martin, Cathie
author_facet D’Orso, Fabio
Hill, Lionel
Appelhagen, Ingo
Lawrenson, Tom
Possenti, Marco
Li, Jie
Harwood, Wendy
Morelli, Giorgio
Martin, Cathie
author_sort D’Orso, Fabio
collection PubMed
description The most abundant phenolic compound in Solanaceous plants is chlorogenic acid (CGA), which possesses protective properties such as antimicrobial and antioxidant activities. These properties are particularly relevant when plants are under adverse conditions, such as pathogen attack, excess light, or extreme temperatures that cause oxidative stress. Additionally, CGA has been shown to absorb UV-B light. In tomato and potato, CGA is mainly produced through the HQT pathway mediated by the enzyme hydroxycinnamoyl-CoA:quinate hydroxycinnamoyl transferase. However, the absence of natural or induced mutants of this gene has made it unclear whether other pathways contribute to CGA production and accumulation. To address this question, we used CRISPR technology to generate multiple knock-out mutant lines in the tomato HQT gene. The resulting slhqt plants did not accumulate CGA or other caffeoylquinic acids (CQAs) in various parts of the plant, indicating that CQA biosynthesis depends almost entirely on the HQT pathway in tomato and, likely, other Solanaceous crops. We also found that the lack of CGA in slhqt plants led to higher levels of hydroxycinnamoyl-glucose and flavonoids compared to wild-type plants. Gene expression analysis revealed that this metabolic reorganization was partly due to flux redirection, but also involved modulation of important transcription factor genes that regulate secondary metabolism and sense environmental conditions. Finally, we investigated the physiological role of CGA in tomato and found that it accumulates in the upper epidermis where it acts as a protector against UV-B irradiation.
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spelling pubmed-101024582023-04-15 Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing D’Orso, Fabio Hill, Lionel Appelhagen, Ingo Lawrenson, Tom Possenti, Marco Li, Jie Harwood, Wendy Morelli, Giorgio Martin, Cathie Front Plant Sci Plant Science The most abundant phenolic compound in Solanaceous plants is chlorogenic acid (CGA), which possesses protective properties such as antimicrobial and antioxidant activities. These properties are particularly relevant when plants are under adverse conditions, such as pathogen attack, excess light, or extreme temperatures that cause oxidative stress. Additionally, CGA has been shown to absorb UV-B light. In tomato and potato, CGA is mainly produced through the HQT pathway mediated by the enzyme hydroxycinnamoyl-CoA:quinate hydroxycinnamoyl transferase. However, the absence of natural or induced mutants of this gene has made it unclear whether other pathways contribute to CGA production and accumulation. To address this question, we used CRISPR technology to generate multiple knock-out mutant lines in the tomato HQT gene. The resulting slhqt plants did not accumulate CGA or other caffeoylquinic acids (CQAs) in various parts of the plant, indicating that CQA biosynthesis depends almost entirely on the HQT pathway in tomato and, likely, other Solanaceous crops. We also found that the lack of CGA in slhqt plants led to higher levels of hydroxycinnamoyl-glucose and flavonoids compared to wild-type plants. Gene expression analysis revealed that this metabolic reorganization was partly due to flux redirection, but also involved modulation of important transcription factor genes that regulate secondary metabolism and sense environmental conditions. Finally, we investigated the physiological role of CGA in tomato and found that it accumulates in the upper epidermis where it acts as a protector against UV-B irradiation. Frontiers Media S.A. 2023-03-31 /pmc/articles/PMC10102458/ /pubmed/37063176 http://dx.doi.org/10.3389/fpls.2023.1124959 Text en Copyright © 2023 D’Orso, Hill, Appelhagen, Lawrenson, Possenti, Li, Harwood, Morelli and Martin https://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(s) 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
D’Orso, Fabio
Hill, Lionel
Appelhagen, Ingo
Lawrenson, Tom
Possenti, Marco
Li, Jie
Harwood, Wendy
Morelli, Giorgio
Martin, Cathie
Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing
title Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing
title_full Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing
title_fullStr Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing
title_full_unstemmed Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing
title_short Exploring the metabolic and physiological roles of HQT in S. lycopersicum by gene editing
title_sort exploring the metabolic and physiological roles of hqt in s. lycopersicum by gene editing
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10102458/
https://www.ncbi.nlm.nih.gov/pubmed/37063176
http://dx.doi.org/10.3389/fpls.2023.1124959
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