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SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis

To combat DNA damage, organisms mount a DNA damage response (DDR) that results in cell cycle regulation, DNA repair and, in severe cases, cell death. Underscoring the importance of gene regulation in this response, studies in Arabidopsis have demonstrated that all of the aforementioned processes rel...

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Autores principales: Bourbousse, Clara, Vegesna, Neeraja, Law, Julie A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310815/
https://www.ncbi.nlm.nih.gov/pubmed/30541889
http://dx.doi.org/10.1073/pnas.1810582115
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author Bourbousse, Clara
Vegesna, Neeraja
Law, Julie A.
author_facet Bourbousse, Clara
Vegesna, Neeraja
Law, Julie A.
author_sort Bourbousse, Clara
collection PubMed
description To combat DNA damage, organisms mount a DNA damage response (DDR) that results in cell cycle regulation, DNA repair and, in severe cases, cell death. Underscoring the importance of gene regulation in this response, studies in Arabidopsis have demonstrated that all of the aforementioned processes rely on SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1), a NAC family transcription factor (TF) that has been functionally equated to the mammalian tumor suppressor, p53. However, the expression networks connecting SOG1 to these processes remain largely unknown and, although the DDR spans from minutes to hours, most transcriptomic data correspond to single time-point snapshots. Here, we generated transcriptional models of the DDR from GAMMA (γ)-irradiated wild-type and sog1 seedlings during a 24-hour time course using DREM, the Dynamic Regulatory Events Miner, revealing 11 coexpressed gene groups with distinct biological functions and cis-regulatory features. Within these networks, additional chromatin immunoprecipitation and transcriptomic experiments revealed that SOG1 is the major activator, directly targeting the most strongly up-regulated genes, including TFs, repair factors, and early cell cycle regulators, while three MYB3R TFs are the major repressors, specifically targeting the most strongly down-regulated genes, which mainly correspond to G2/M cell cycle-regulated genes. Together these models reveal the temporal dynamics of the transcriptional events triggered by γ-irradiation and connects these events to TFs and biological processes over a time scale commensurate with key processes coordinated in response to DNA damage, greatly expanding our understanding of the DDR.
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spelling pubmed-63108152019-01-04 SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis Bourbousse, Clara Vegesna, Neeraja Law, Julie A. Proc Natl Acad Sci U S A PNAS Plus To combat DNA damage, organisms mount a DNA damage response (DDR) that results in cell cycle regulation, DNA repair and, in severe cases, cell death. Underscoring the importance of gene regulation in this response, studies in Arabidopsis have demonstrated that all of the aforementioned processes rely on SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1), a NAC family transcription factor (TF) that has been functionally equated to the mammalian tumor suppressor, p53. However, the expression networks connecting SOG1 to these processes remain largely unknown and, although the DDR spans from minutes to hours, most transcriptomic data correspond to single time-point snapshots. Here, we generated transcriptional models of the DDR from GAMMA (γ)-irradiated wild-type and sog1 seedlings during a 24-hour time course using DREM, the Dynamic Regulatory Events Miner, revealing 11 coexpressed gene groups with distinct biological functions and cis-regulatory features. Within these networks, additional chromatin immunoprecipitation and transcriptomic experiments revealed that SOG1 is the major activator, directly targeting the most strongly up-regulated genes, including TFs, repair factors, and early cell cycle regulators, while three MYB3R TFs are the major repressors, specifically targeting the most strongly down-regulated genes, which mainly correspond to G2/M cell cycle-regulated genes. Together these models reveal the temporal dynamics of the transcriptional events triggered by γ-irradiation and connects these events to TFs and biological processes over a time scale commensurate with key processes coordinated in response to DNA damage, greatly expanding our understanding of the DDR. National Academy of Sciences 2018-12-26 2018-12-12 /pmc/articles/PMC6310815/ /pubmed/30541889 http://dx.doi.org/10.1073/pnas.1810582115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle PNAS Plus
Bourbousse, Clara
Vegesna, Neeraja
Law, Julie A.
SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis
title SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis
title_full SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis
title_fullStr SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis
title_full_unstemmed SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis
title_short SOG1 activator and MYB3R repressors regulate a complex DNA damage network in Arabidopsis
title_sort sog1 activator and myb3r repressors regulate a complex dna damage network in arabidopsis
topic PNAS Plus
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6310815/
https://www.ncbi.nlm.nih.gov/pubmed/30541889
http://dx.doi.org/10.1073/pnas.1810582115
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