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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...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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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. |
format | Online Article Text |
id | pubmed-8855596 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
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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