Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis

Somatic embryogenesis (SE), which is a process that involves the in vitro-induced embryogenic reprogramming of plant somatic cells, requires dynamic changes in the cell transcriptome. These changes are fine-tuned by many genetic and epigenetic factors, including posttranslational histone modificatio...

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Main Authors: Joanna Morończyk, Agnieszka Brąszewska, Barbara Wójcikowska, Karolina Chwiałkowska, Katarzyna Nowak, Anna M. Wójcik, Mirosław Kwaśniewski, Małgorzata D. Gaj
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Language:English
Published: MDPI AG 2022-03-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/11/5/863
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author Joanna Morończyk
Agnieszka Brąszewska
Barbara Wójcikowska
Karolina Chwiałkowska
Katarzyna Nowak
Anna M. Wójcik
Mirosław Kwaśniewski
Małgorzata D. Gaj
author_facet Joanna Morończyk
Agnieszka Brąszewska
Barbara Wójcikowska
Karolina Chwiałkowska
Katarzyna Nowak
Anna M. Wójcik
Mirosław Kwaśniewski
Małgorzata D. Gaj
author_sort Joanna Morończyk
collection DOAJ
description Somatic embryogenesis (SE), which is a process that involves the in vitro-induced embryogenic reprogramming of plant somatic cells, requires dynamic changes in the cell transcriptome. These changes are fine-tuned by many genetic and epigenetic factors, including posttranslational histone modifications such as histone acetylation. Antagonistically acting enzymes, histone acetyltransferases (HATs) and deacetylases (HDACs), which control histone acetylation in many developmental processes, are believed to control SE. However, the function of specific HAT/HDACs and the genes that are subjected to histone acetylation-mediated regulation during SE have yet to be revealed. Here, we present the global and gene-specific changes in histone acetylation in Arabidopsis explants that are undergoing SE. In the TSA (trichostatin A)-induced SE, we demonstrate that H3 and H4 acetylation might control the expression of the critical transcription factor (<i>TF</i>) genes of a vital role in SE, including <i>LEC1</i>, <i>LEC2</i> (<i>LEAFY COTYLEDON 1; 2</i>), <i>FUS3</i> (<i>FUSCA 3</i>) and <i>MYB118</i> (<i>MYB DOMAIN PROTEIN 118</i>). Within the HATs and HDACs, which mainly positively regulate SE, we identified HDA19 as negatively affecting SE by regulating <i>LEC1</i>, <i>LEC2</i> and <i>BBM</i>. Finally, we provide some evidence on the role of HDA19 in the histone acetylation-mediated regulation of <i>LEC2</i> during SE. Our results reveal an essential function of histone acetylation in the epigenetic mechanisms that control the <i>TF</i> genes that play critical roles in the embryogenic reprogramming of plant somatic cells. The results implicate the complexity of Hac-related gene regulation in embryogenic induction and point to differences in the regulatory mechanisms that are involved in auxin- and TSA-induced SE.
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spelling doaj.art-4f07fff9a13b48dca2a9e0f7f2503a732023-11-23T22:51:25ZengMDPI AGCells2073-44092022-03-0111586310.3390/cells11050863Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of ArabidopsisJoanna Morończyk0Agnieszka Brąszewska1Barbara Wójcikowska2Karolina Chwiałkowska3Katarzyna Nowak4Anna M. Wójcik5Mirosław Kwaśniewski6Małgorzata D. Gaj7Institute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, 40-007 Katowice, PolandInstitute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, 40-007 Katowice, PolandInstitute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, 40-007 Katowice, PolandCentre for Bioinformatics and Data Analysis, Medical University of Bialystok, 15-269 Bialystok, PolandInstitute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, 40-007 Katowice, PolandInstitute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, 40-007 Katowice, PolandCentre for Bioinformatics and Data Analysis, Medical University of Bialystok, 15-269 Bialystok, PolandInstitute of Biology, Biotechnology and Environmental Protection, Faculty of Natural Sciences, University of Silesia in Katowice, 40-007 Katowice, PolandSomatic embryogenesis (SE), which is a process that involves the in vitro-induced embryogenic reprogramming of plant somatic cells, requires dynamic changes in the cell transcriptome. These changes are fine-tuned by many genetic and epigenetic factors, including posttranslational histone modifications such as histone acetylation. Antagonistically acting enzymes, histone acetyltransferases (HATs) and deacetylases (HDACs), which control histone acetylation in many developmental processes, are believed to control SE. However, the function of specific HAT/HDACs and the genes that are subjected to histone acetylation-mediated regulation during SE have yet to be revealed. Here, we present the global and gene-specific changes in histone acetylation in Arabidopsis explants that are undergoing SE. In the TSA (trichostatin A)-induced SE, we demonstrate that H3 and H4 acetylation might control the expression of the critical transcription factor (<i>TF</i>) genes of a vital role in SE, including <i>LEC1</i>, <i>LEC2</i> (<i>LEAFY COTYLEDON 1; 2</i>), <i>FUS3</i> (<i>FUSCA 3</i>) and <i>MYB118</i> (<i>MYB DOMAIN PROTEIN 118</i>). Within the HATs and HDACs, which mainly positively regulate SE, we identified HDA19 as negatively affecting SE by regulating <i>LEC1</i>, <i>LEC2</i> and <i>BBM</i>. Finally, we provide some evidence on the role of HDA19 in the histone acetylation-mediated regulation of <i>LEC2</i> during SE. Our results reveal an essential function of histone acetylation in the epigenetic mechanisms that control the <i>TF</i> genes that play critical roles in the embryogenic reprogramming of plant somatic cells. The results implicate the complexity of Hac-related gene regulation in embryogenic induction and point to differences in the regulatory mechanisms that are involved in auxin- and TSA-induced SE.https://www.mdpi.com/2073-4409/11/5/863Arabidopsisauxinhistone acetylationsomatic embryogenesistranscription factorstrichostatin A
spellingShingle Joanna Morończyk
Agnieszka Brąszewska
Barbara Wójcikowska
Karolina Chwiałkowska
Katarzyna Nowak
Anna M. Wójcik
Mirosław Kwaśniewski
Małgorzata D. Gaj
Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis
Cells
Arabidopsis
auxin
histone acetylation
somatic embryogenesis
transcription factors
trichostatin A
title Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis
title_full Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis
title_fullStr Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis
title_full_unstemmed Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis
title_short Insights into the Histone Acetylation-Mediated Regulation of the Transcription Factor Genes That Control the Embryogenic Transition in the Somatic Cells of Arabidopsis
title_sort insights into the histone acetylation mediated regulation of the transcription factor genes that control the embryogenic transition in the somatic cells of arabidopsis
topic Arabidopsis
auxin
histone acetylation
somatic embryogenesis
transcription factors
trichostatin A
url https://www.mdpi.com/2073-4409/11/5/863
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