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Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1

Plants respond to high temperatures with global changes of the transcriptome, proteome, and metabolome. Heat stress transcription factors (Hsfs) are the core regulators of transcriptome responses as they control the reprogramming of expression of hundreds of genes. The thermotolerance-related functi...

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Autores principales: Paupière, Marine Josephine, Tikunov, Yury, Schleiff, Enrico, Bovy, Arnaud, Fragkostefanakis, Sotirios
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7785825/
https://www.ncbi.nlm.nih.gov/pubmed/33424907
http://dx.doi.org/10.3389/fpls.2020.610599
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author Paupière, Marine Josephine
Tikunov, Yury
Schleiff, Enrico
Bovy, Arnaud
Fragkostefanakis, Sotirios
author_facet Paupière, Marine Josephine
Tikunov, Yury
Schleiff, Enrico
Bovy, Arnaud
Fragkostefanakis, Sotirios
author_sort Paupière, Marine Josephine
collection PubMed
description Plants respond to high temperatures with global changes of the transcriptome, proteome, and metabolome. Heat stress transcription factors (Hsfs) are the core regulators of transcriptome responses as they control the reprogramming of expression of hundreds of genes. The thermotolerance-related function of Hsfs is mainly based on the regulation of many heat shock proteins (HSPs). Instead, the Hsf-dependent reprogramming of metabolic pathways and their contribution to thermotolerance are not well described. In tomato (Solanum lycopersicum), manipulation of HsfB1, either by suppression or overexpression (OE) leads to enhanced thermotolerance and coincides with distinct profile of metabolic routes based on a metabolome profiling of wild-type (WT) and HsfB1 transgenic plants. Leaves of HsfB1 knock-down plants show an accumulation of metabolites with a positive effect on thermotolerance such as the sugars sucrose and glucose and the polyamine putrescine. OE of HsfB1 leads to the accumulation of products of the phenylpropanoid and flavonoid pathways, including several caffeoyl quinic acid isomers. The latter is due to the enhanced transcription of genes coding key enzymes in both pathways, in some cases in both non-stressed and stressed plants. Our results show that beyond the control of the expression of Hsfs and HSPs, HsfB1 has a wider activity range by regulating important metabolic pathways providing an important link between stress response and physiological tomato development.
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spelling pubmed-77858252021-01-07 Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1 Paupière, Marine Josephine Tikunov, Yury Schleiff, Enrico Bovy, Arnaud Fragkostefanakis, Sotirios Front Plant Sci Plant Science Plants respond to high temperatures with global changes of the transcriptome, proteome, and metabolome. Heat stress transcription factors (Hsfs) are the core regulators of transcriptome responses as they control the reprogramming of expression of hundreds of genes. The thermotolerance-related function of Hsfs is mainly based on the regulation of many heat shock proteins (HSPs). Instead, the Hsf-dependent reprogramming of metabolic pathways and their contribution to thermotolerance are not well described. In tomato (Solanum lycopersicum), manipulation of HsfB1, either by suppression or overexpression (OE) leads to enhanced thermotolerance and coincides with distinct profile of metabolic routes based on a metabolome profiling of wild-type (WT) and HsfB1 transgenic plants. Leaves of HsfB1 knock-down plants show an accumulation of metabolites with a positive effect on thermotolerance such as the sugars sucrose and glucose and the polyamine putrescine. OE of HsfB1 leads to the accumulation of products of the phenylpropanoid and flavonoid pathways, including several caffeoyl quinic acid isomers. The latter is due to the enhanced transcription of genes coding key enzymes in both pathways, in some cases in both non-stressed and stressed plants. Our results show that beyond the control of the expression of Hsfs and HSPs, HsfB1 has a wider activity range by regulating important metabolic pathways providing an important link between stress response and physiological tomato development. Frontiers Media S.A. 2020-12-23 /pmc/articles/PMC7785825/ /pubmed/33424907 http://dx.doi.org/10.3389/fpls.2020.610599 Text en Copyright © 2020 Paupière, Tikunov, Schleiff, Bovy and Fragkostefanakis. 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(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
Paupière, Marine Josephine
Tikunov, Yury
Schleiff, Enrico
Bovy, Arnaud
Fragkostefanakis, Sotirios
Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1
title Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1
title_full Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1
title_fullStr Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1
title_full_unstemmed Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1
title_short Reprogramming of Tomato Leaf Metabolome by the Activity of Heat Stress Transcription Factor HsfB1
title_sort reprogramming of tomato leaf metabolome by the activity of heat stress transcription factor hsfb1
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7785825/
https://www.ncbi.nlm.nih.gov/pubmed/33424907
http://dx.doi.org/10.3389/fpls.2020.610599
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