title: Nitric Oxide Modulates Histone Acetylation at Stress Genes by Inhibition of Histone Deacetylases.
abstract: Histone acetylation, which is an important mechanism to regulate gene expression, is controlled by the opposing action of histone acetyltransferases and histone deacetylases (HDACs). In animals, several HDACs are subjected to regulation by nitric oxide (NO); in plants, however, it is unknown whether NO affects histone acetylation. We found that treatment with the physiological NO donor S-nitrosoglutathione (GSNO) increased the abundance of several histone acetylation marks in Arabidopsis (Arabidopsis thaliana), which was strongly diminished in the presence of the NO scavenger 2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide. This increase was likely triggered by NO-dependent inhibition of HDAC activity, since GSNO and S-nitroso-N-acetyl-dl-penicillamine significantly and reversibly reduced total HDAC activity in vitro (in nuclear extracts) and in vivo (in protoplasts). Next, genome-wide H3K9/14ac profiles in Arabidopsis seedlings were generated by chromatin immunoprecipitation sequencing, and changes induced by GSNO, GSNO/2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide or trichostatin A (an HDAC inhibitor) were quantified, thereby identifying genes that display putative NO-regulated histone acetylation. Functional classification of these genes revealed that many of them are involved in the plant defense response and the abiotic stress response. Furthermore, salicylic acid, which is the major plant defense hormone against biotrophic pathogens, inhibited HDAC activity and increased histone acetylation by inducing endogenous NO production. These data suggest that NO affects histone acetylation by targeting and inhibiting HDAC complexes, resulting in the hyperacetylation of specific genes. This mechanism might operate in the plant stress response by facilitating the stress-induced transcription of genes.
authors.affiliation: Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich/Neuherberg, Germany (A.M., A.A., E.G., J.D., C.L.).|Institute for Microbiology, Ernst-Moritz-Arndt-Universität Greifswald, 17489 Greifswald, Germany (J.B.).|Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan (K.W.); and.|Department of Biochemical Plant Pathology, Technische Universität München, 85354 Freising, Germany (J.D.).
authors.forename: Alexander
authors.initials: A
authors.lastname: Mengel
authors.affiliation: Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich/Neuherberg, Germany (A.M., A.A., E.G., J.D., C.L.).|Institute for Microbiology, Ernst-Moritz-Arndt-Universität Greifswald, 17489 Greifswald, Germany (J.B.).|Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan (K.W.); and.|Department of Biochemical Plant Pathology, Technische Universität München, 85354 Freising, Germany (J.D.).
authors.forename: Alexandra
authors.initials: A
authors.lastname: Ageeva
authors.affiliation: Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich/Neuherberg, Germany (A.M., A.A., E.G., J.D., C.L.).|Institute for Microbiology, Ernst-Moritz-Arndt-Universität Greifswald, 17489 Greifswald, Germany (J.B.).|Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan (K.W.); and.|Department of Biochemical Plant Pathology, Technische Universität München, 85354 Freising, Germany (J.D.).
authors.forename: Elisabeth
authors.identifier: 0000-0002-7511-5510
authors.initials: E
authors.lastname: Georgii
authors.affiliation: Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich/Neuherberg, Germany (A.M., A.A., E.G., J.D., C.L.).|Institute for Microbiology, Ernst-Moritz-Arndt-Universität Greifswald, 17489 Greifswald, Germany (J.B.).|Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan (K.W.); and.|Department of Biochemical Plant Pathology, Technische Universität München, 85354 Freising, Germany (J.D.).
authors.forename: Jörg
authors.identifier: 0000-0001-8410-5624
authors.initials: J
authors.lastname: Bernhardt
authors.affiliation: Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich/Neuherberg, Germany (A.M., A.A., E.G., J.D., C.L.).|Institute for Microbiology, Ernst-Moritz-Arndt-Universität Greifswald, 17489 Greifswald, Germany (J.B.).|Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan (K.W.); and.|Department of Biochemical Plant Pathology, Technische Universität München, 85354 Freising, Germany (J.D.).
authors.forename: Keqiang
authors.identifier: 0000-0002-5791-3594
authors.initials: K
authors.lastname: Wu
authors.affiliation: Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich/Neuherberg, Germany (A.M., A.A., E.G., J.D., C.L.).|Institute for Microbiology, Ernst-Moritz-Arndt-Universität Greifswald, 17489 Greifswald, Germany (J.B.).|Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan (K.W.); and.|Department of Biochemical Plant Pathology, Technische Universität München, 85354 Freising, Germany (J.D.).
authors.forename: Jörg
authors.initials: J
authors.lastname: Durner
authors.affiliation: Institute of Biochemical Plant Pathology, Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Munich/Neuherberg, Germany (A.M., A.A., E.G., J.D., C.L.); lindermayr@helmholtz-muenchen.de.|Institute for Microbiology, Ernst-Moritz-Arndt-Universität Greifswald, 17489 Greifswald, Germany (J.B.); lindermayr@helmholtz-muenchen.de.|Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan (K.W.); and lindermayr@helmholtz-muenchen.de.|Department of Biochemical Plant Pathology, Technische Universität München, 85354 Freising, Germany (J.D.) lindermayr@helmholtz-muenchen.de.
authors.forename: Christian
authors.identifier: 0000-0002-9343-4996
authors.initials: C
authors.lastname: Lindermayr
mesh_terms: D000107:Acetylation; D017360:Arabidopsis / Q000187:drug effects / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D005978:Glutathione / Q000494:pharmacology; D006655:Histone Deacetylases / Q000378:metabolism*; D006657:Histones / Q000378:metabolism*; D006877:Hydroxamic Acids / Q000494:pharmacology; D009569:Nitric Oxide / Q000378:metabolism*; D020030:Nitric Oxide Donors / Q000494:pharmacology; D026423:S-Nitroso-N-Acetylpenicillamine / Q000494:pharmacology; D026422:S-Nitrosoglutathione / Q000494:pharmacology; D026403:S-Nitrosothiols; D020156:Salicylic Acid / Q000378:metabolism / Q000494:pharmacology; D013312:Stress, Physiological / Q000235:genetics*
chemical_list: D029681:Arabidopsis Proteins; D006657:Histones; D006877:Hydroxamic Acids; D020030:Nitric Oxide Donors; D026403:S-Nitrosothiols; D009569:Nitric Oxide; C012589:trichostatin A; D026422:S-Nitrosoglutathione; D026423:S-Nitroso-N-Acetylpenicillamine; D006655:Histone Deacetylases; D005978:Glutathione; D020156:Salicylic Acid