GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive Genes

In the past, reactive nitrogen species (RNS) were supposed to be stress-induced by-products of disturbed metabolism that cause oxidative damage to biomolecules. However, emerging evidence demonstrates a substantial role of RNS as endogenous signals in eukaryotes. In plants, S-nitrosoglutathione (GSN...

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Main Authors: Eva Esther Rudolf, Patrick Hüther, Ignasi Forné, Elisabeth Georgii, Yongtao Han, Rüdiger Hell, Markus Wirtz, Axel Imhof, Claude Becker, Jörg Durner, Christian Lindermayr
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/10/7/1128
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author Eva Esther Rudolf
Patrick Hüther
Ignasi Forné
Elisabeth Georgii
Yongtao Han
Rüdiger Hell
Markus Wirtz
Axel Imhof
Claude Becker
Jörg Durner
Christian Lindermayr
author_facet Eva Esther Rudolf
Patrick Hüther
Ignasi Forné
Elisabeth Georgii
Yongtao Han
Rüdiger Hell
Markus Wirtz
Axel Imhof
Claude Becker
Jörg Durner
Christian Lindermayr
author_sort Eva Esther Rudolf
collection DOAJ
description In the past, reactive nitrogen species (RNS) were supposed to be stress-induced by-products of disturbed metabolism that cause oxidative damage to biomolecules. However, emerging evidence demonstrates a substantial role of RNS as endogenous signals in eukaryotes. In plants, S-nitrosoglutathione (GSNO) is the dominant RNS and serves as the <sup>•</sup>NO donor for S-nitrosation of diverse effector proteins. Remarkably, the endogenous GSNO level is tightly controlled by S-nitrosoglutathione reductase (GSNOR) that irreversibly inactivates the glutathione-bound NO to ammonium. Exogenous feeding of diverse RNS, including GSNO, affected chromatin accessibility and transcription of stress-related genes, but the triggering function of RNS on these regulatory processes remained elusive. Here, we show that GSNO reductase-deficient plants (<i>gsnor1-3</i>) accumulate S-adenosylmethionine (SAM), the principal methyl donor for methylation of DNA and histones. This SAM accumulation triggered a substantial increase in the methylation index (MI = [SAM]/[S-adenosylhomocysteine]), indicating the transmethylation activity and histone methylation status in higher eukaryotes. Indeed, a mass spectrometry-based global histone profiling approach demonstrated a significant global increase in H3K9me2, which was independently verified by immunological detection using a selective antibody. Since H3K9me2-modified regions tightly correlate with methylated DNA regions, we also determined the DNA methylation status of <i>gsnor1-3</i> plants by whole-genome bisulfite sequencing. DNA methylation in the CG, CHG, and CHH contexts in <i>gsnor1-3</i> was significantly enhanced compared to the wild type. We propose that GSNOR1 activity affects chromatin accessibility by controlling the transmethylation activity (MI) required for maintaining DNA methylation and the level of the repressive chromatin mark H3K9me2.
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spelling doaj.art-571bafa37a524333bdc79e66ef9de76e2023-11-22T03:05:57ZengMDPI AGAntioxidants2076-39212021-07-01107112810.3390/antiox10071128GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive GenesEva Esther Rudolf0Patrick Hüther1Ignasi Forné2Elisabeth Georgii3Yongtao Han4Rüdiger Hell5Markus Wirtz6Axel Imhof7Claude Becker8Jörg Durner9Christian Lindermayr10Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Oberschleißheim, GermanyGregor Mendel Institute of Molecular Plant Biology, Austrian Academy Sciences, Vienna BioCenter (VBC), 1030 Wien, AustriaProtein Analysis Unit, Ludwig-Maximilians-Universität München, 82152 Martinsried, GermanyInstitute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Oberschleißheim, GermanyInstitute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Oberschleißheim, GermanyCentre for Organismal Studies, Ruprecht-Karls-Universität Heidelberg, 69120 Heidelberg, GermanyCentre for Organismal Studies, Ruprecht-Karls-Universität Heidelberg, 69120 Heidelberg, GermanyProtein Analysis Unit, Ludwig-Maximilians-Universität München, 82152 Martinsried, GermanyGregor Mendel Institute of Molecular Plant Biology, Austrian Academy Sciences, Vienna BioCenter (VBC), 1030 Wien, AustriaInstitute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Oberschleißheim, GermanyInstitute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Oberschleißheim, GermanyIn the past, reactive nitrogen species (RNS) were supposed to be stress-induced by-products of disturbed metabolism that cause oxidative damage to biomolecules. However, emerging evidence demonstrates a substantial role of RNS as endogenous signals in eukaryotes. In plants, S-nitrosoglutathione (GSNO) is the dominant RNS and serves as the <sup>•</sup>NO donor for S-nitrosation of diverse effector proteins. Remarkably, the endogenous GSNO level is tightly controlled by S-nitrosoglutathione reductase (GSNOR) that irreversibly inactivates the glutathione-bound NO to ammonium. Exogenous feeding of diverse RNS, including GSNO, affected chromatin accessibility and transcription of stress-related genes, but the triggering function of RNS on these regulatory processes remained elusive. Here, we show that GSNO reductase-deficient plants (<i>gsnor1-3</i>) accumulate S-adenosylmethionine (SAM), the principal methyl donor for methylation of DNA and histones. This SAM accumulation triggered a substantial increase in the methylation index (MI = [SAM]/[S-adenosylhomocysteine]), indicating the transmethylation activity and histone methylation status in higher eukaryotes. Indeed, a mass spectrometry-based global histone profiling approach demonstrated a significant global increase in H3K9me2, which was independently verified by immunological detection using a selective antibody. Since H3K9me2-modified regions tightly correlate with methylated DNA regions, we also determined the DNA methylation status of <i>gsnor1-3</i> plants by whole-genome bisulfite sequencing. DNA methylation in the CG, CHG, and CHH contexts in <i>gsnor1-3</i> was significantly enhanced compared to the wild type. We propose that GSNOR1 activity affects chromatin accessibility by controlling the transmethylation activity (MI) required for maintaining DNA methylation and the level of the repressive chromatin mark H3K9me2.https://www.mdpi.com/2076-3921/10/7/1128nitric oxideS-nitrosoglutathioneS-nitrosoglutathione reductasemetaboloepigeneticS-adenosylhomocysteineDNA methylation
spellingShingle Eva Esther Rudolf
Patrick Hüther
Ignasi Forné
Elisabeth Georgii
Yongtao Han
Rüdiger Hell
Markus Wirtz
Axel Imhof
Claude Becker
Jörg Durner
Christian Lindermayr
GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive Genes
Antioxidants
nitric oxide
S-nitrosoglutathione
S-nitrosoglutathione reductase
metaboloepigenetic
S-adenosylhomocysteine
DNA methylation
title GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive Genes
title_full GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive Genes
title_fullStr GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive Genes
title_full_unstemmed GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive Genes
title_short GSNOR Contributes to Demethylation and Expression of Transposable Elements and Stress-Responsive Genes
title_sort gsnor contributes to demethylation and expression of transposable elements and stress responsive genes
topic nitric oxide
S-nitrosoglutathione
S-nitrosoglutathione reductase
metaboloepigenetic
S-adenosylhomocysteine
DNA methylation
url https://www.mdpi.com/2076-3921/10/7/1128
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