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Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold

BACKGROUND: DNA methylation is thought to influence the expression of genes, especially in response to changing environmental conditions and developmental changes. Sugar beet (Beta vulgaris ssp. vulgaris), and other biennial or perennial plants are inevitably exposed to fluctuating temperatures thro...

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Autores principales: Gutschker, Sindy, Corral, José María, Schmiedl, Alfred, Ludewig, Frank, Koch, Wolfgang, Fiedler-Wiechers, Karin, Czarnecki, Olaf, Harms, Karsten, Keller, Isabel, Martins Rodrigues, Cristina, Pommerrenig, Benjamin, Neuhaus, H. Ekkehard, Zierer, Wolfgang, Sonnewald, Uwe, Müdsam, Christina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8855596/
https://www.ncbi.nlm.nih.gov/pubmed/35176993
http://dx.doi.org/10.1186/s12864-022-08312-2
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author Gutschker, Sindy
Corral, José María
Schmiedl, Alfred
Ludewig, Frank
Koch, Wolfgang
Fiedler-Wiechers, Karin
Czarnecki, Olaf
Harms, Karsten
Keller, Isabel
Martins Rodrigues, Cristina
Pommerrenig, Benjamin
Neuhaus, H. Ekkehard
Zierer, Wolfgang
Sonnewald, Uwe
Müdsam, Christina
author_facet Gutschker, Sindy
Corral, José María
Schmiedl, Alfred
Ludewig, Frank
Koch, Wolfgang
Fiedler-Wiechers, Karin
Czarnecki, Olaf
Harms, Karsten
Keller, Isabel
Martins Rodrigues, Cristina
Pommerrenig, Benjamin
Neuhaus, H. Ekkehard
Zierer, Wolfgang
Sonnewald, Uwe
Müdsam, Christina
author_sort Gutschker, Sindy
collection PubMed
description BACKGROUND: DNA methylation is thought to influence the expression of genes, especially in response to changing environmental conditions and developmental changes. Sugar beet (Beta vulgaris ssp. vulgaris), and other biennial or perennial plants are inevitably exposed to fluctuating temperatures throughout their lifecycle and might even require such stimulus to acquire floral competence. Therefore, plants such as beets, need to fine-tune their epigenetic makeup to ensure phenotypic plasticity towards changing environmental conditions while at the same time steering essential developmental processes. Different crop species may show opposing reactions towards the same abiotic stress, or, vice versa, identical species may respond differently depending on the specific kind of stress. RESULTS: In this study, we investigated common effects of cold treatment on genome-wide DNA methylation and gene expression of two Beta vulgaris accessions via multi-omics data analysis. Cold exposure resulted in a pronounced reduction of DNA methylation levels, which particularly affected methylation in CHH context (and to a lesser extent CHG) and was accompanied by transcriptional downregulation of the chromomethyltransferase CMT2 and strong upregulation of several genes mediating active DNA demethylation. CONCLUSION: Integration of methylomic and transcriptomic data revealed that, rather than methylation having directly influenced expression, epigenetic modifications correlated with changes in expression of known players involved in DNA (de)methylation. In particular, cold triggered upregulation of genes putatively contributing to DNA demethylation via the ROS1 pathway. Our observations suggest that these transcriptional responses precede the cold-induced global DNA-hypomethylation in non-CpG, preparing beets for additional transcriptional alterations necessary for adapting to upcoming environmental changes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08312-2.
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spelling pubmed-88555962022-02-23 Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold Gutschker, Sindy Corral, José María Schmiedl, Alfred Ludewig, Frank Koch, Wolfgang Fiedler-Wiechers, Karin Czarnecki, Olaf Harms, Karsten Keller, Isabel Martins Rodrigues, Cristina Pommerrenig, Benjamin Neuhaus, H. Ekkehard Zierer, Wolfgang Sonnewald, Uwe Müdsam, Christina BMC Genomics Research BACKGROUND: DNA methylation is thought to influence the expression of genes, especially in response to changing environmental conditions and developmental changes. Sugar beet (Beta vulgaris ssp. vulgaris), and other biennial or perennial plants are inevitably exposed to fluctuating temperatures throughout their lifecycle and might even require such stimulus to acquire floral competence. Therefore, plants such as beets, need to fine-tune their epigenetic makeup to ensure phenotypic plasticity towards changing environmental conditions while at the same time steering essential developmental processes. Different crop species may show opposing reactions towards the same abiotic stress, or, vice versa, identical species may respond differently depending on the specific kind of stress. RESULTS: In this study, we investigated common effects of cold treatment on genome-wide DNA methylation and gene expression of two Beta vulgaris accessions via multi-omics data analysis. Cold exposure resulted in a pronounced reduction of DNA methylation levels, which particularly affected methylation in CHH context (and to a lesser extent CHG) and was accompanied by transcriptional downregulation of the chromomethyltransferase CMT2 and strong upregulation of several genes mediating active DNA demethylation. CONCLUSION: Integration of methylomic and transcriptomic data revealed that, rather than methylation having directly influenced expression, epigenetic modifications correlated with changes in expression of known players involved in DNA (de)methylation. In particular, cold triggered upregulation of genes putatively contributing to DNA demethylation via the ROS1 pathway. Our observations suggest that these transcriptional responses precede the cold-induced global DNA-hypomethylation in non-CpG, preparing beets for additional transcriptional alterations necessary for adapting to upcoming environmental changes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08312-2. BioMed Central 2022-02-17 /pmc/articles/PMC8855596/ /pubmed/35176993 http://dx.doi.org/10.1186/s12864-022-08312-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Gutschker, Sindy
Corral, José María
Schmiedl, Alfred
Ludewig, Frank
Koch, Wolfgang
Fiedler-Wiechers, Karin
Czarnecki, Olaf
Harms, Karsten
Keller, Isabel
Martins Rodrigues, Cristina
Pommerrenig, Benjamin
Neuhaus, H. Ekkehard
Zierer, Wolfgang
Sonnewald, Uwe
Müdsam, Christina
Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold
title Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold
title_full Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold
title_fullStr Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold
title_full_unstemmed Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold
title_short Multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (Beta vulgaris subsp. vulgaris) in response to cold
title_sort multi-omics data integration reveals link between epigenetic modifications and gene expression in sugar beet (beta vulgaris subsp. vulgaris) in response to cold
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8855596/
https://www.ncbi.nlm.nih.gov/pubmed/35176993
http://dx.doi.org/10.1186/s12864-022-08312-2
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