Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes Expression

Plants are subjected to adverse conditions being outer protective tissues fundamental to their survival. Tree stems are enveloped by a periderm made of cork cells, resulting from the activity of the meristem phellogen. DNA methylation and histone modifications have important roles in the regulation...

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Main Authors: Vera Inácio, Madalena T. Martins, José Graça, Leonor Morais-Cecílio
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2018.01194/full
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author Vera Inácio
Madalena T. Martins
José Graça
Leonor Morais-Cecílio
author_facet Vera Inácio
Madalena T. Martins
José Graça
Leonor Morais-Cecílio
author_sort Vera Inácio
collection DOAJ
description Plants are subjected to adverse conditions being outer protective tissues fundamental to their survival. Tree stems are enveloped by a periderm made of cork cells, resulting from the activity of the meristem phellogen. DNA methylation and histone modifications have important roles in the regulation of plant cell differentiation. However, studies on its involvement in cork differentiation are scarce despite periderm importance. Cork oak periderm development was used as a model to study the formation and differentiation of secondary protective tissues, and their behavior after traumatic wounding (traumatic periderm). Nuclei structural changes, dynamics of DNA methylation, and posttranslational histone modifications were assessed in young and traumatic periderms, after cork harvesting. Lenticular phellogen producing atypical non-suberized cells that disaggregate and form pores was also studied, due to high impact for cork industrial uses. Immunolocalization of active and repressive marks, transcription analysis of the corresponding genes, and correlations between gene expression and cork porosity were investigated. During young periderm development, a reduction in nuclei area along with high levels of DNA methylation occurred throughout epidermis disruption. As cork cells became more differentiated, whole nuclei progressive chromatin condensation with accumulation in the nuclear periphery and increasing DNA methylation was observed. Lenticular cells nuclei were highly fragmented with faint 5-mC labeling. Phellogen nuclei were less methylated than in cork cells, and in lenticular phellogen were even lower. No significant differences were detected in H3K4me3 and H3K18ac signals between cork cells layers, although an increase in H3K4me3 signals was found from the phellogen to cork cells. Distinct gene expression patterns in young and traumatic periderms suggest that cork differentiation might be under specific silencing regulatory pathways. Significant correlations were found between QsMET1, QsMET2, and QsSUVH4 gene expression and cork porosity. This work evidences that DNA methylation and histone modifications play a role in cork differentiation and epidermis induced tension-stress. It also provides the first insights into chromatin dynamics during cork and lenticular cells differentiation pointing to a distinct type of remodeling associated with cell death.
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spelling doaj.art-ff66e2b4a59149eea170e6087f37ca3c2022-12-22T02:51:37ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-08-01910.3389/fpls.2018.01194390675Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes ExpressionVera Inácio0Madalena T. Martins1José Graça2Leonor Morais-Cecílio3Linking Landscape, Environment, Agriculture and Food (LEAF), Institute of Agronomy, University of Lisbon, Lisbon, PortugalLinking Landscape, Environment, Agriculture and Food (LEAF), Institute of Agronomy, University of Lisbon, Lisbon, PortugalForest Research Center (CEF), Institute of Agronomy, University of Lisbon, Lisbon, PortugalLinking Landscape, Environment, Agriculture and Food (LEAF), Institute of Agronomy, University of Lisbon, Lisbon, PortugalPlants are subjected to adverse conditions being outer protective tissues fundamental to their survival. Tree stems are enveloped by a periderm made of cork cells, resulting from the activity of the meristem phellogen. DNA methylation and histone modifications have important roles in the regulation of plant cell differentiation. However, studies on its involvement in cork differentiation are scarce despite periderm importance. Cork oak periderm development was used as a model to study the formation and differentiation of secondary protective tissues, and their behavior after traumatic wounding (traumatic periderm). Nuclei structural changes, dynamics of DNA methylation, and posttranslational histone modifications were assessed in young and traumatic periderms, after cork harvesting. Lenticular phellogen producing atypical non-suberized cells that disaggregate and form pores was also studied, due to high impact for cork industrial uses. Immunolocalization of active and repressive marks, transcription analysis of the corresponding genes, and correlations between gene expression and cork porosity were investigated. During young periderm development, a reduction in nuclei area along with high levels of DNA methylation occurred throughout epidermis disruption. As cork cells became more differentiated, whole nuclei progressive chromatin condensation with accumulation in the nuclear periphery and increasing DNA methylation was observed. Lenticular cells nuclei were highly fragmented with faint 5-mC labeling. Phellogen nuclei were less methylated than in cork cells, and in lenticular phellogen were even lower. No significant differences were detected in H3K4me3 and H3K18ac signals between cork cells layers, although an increase in H3K4me3 signals was found from the phellogen to cork cells. Distinct gene expression patterns in young and traumatic periderms suggest that cork differentiation might be under specific silencing regulatory pathways. Significant correlations were found between QsMET1, QsMET2, and QsSUVH4 gene expression and cork porosity. This work evidences that DNA methylation and histone modifications play a role in cork differentiation and epidermis induced tension-stress. It also provides the first insights into chromatin dynamics during cork and lenticular cells differentiation pointing to a distinct type of remodeling associated with cell death.https://www.frontiersin.org/article/10.3389/fpls.2018.01194/fullCORKphellogenlenticelslenticular phellogen5-mCH3K4Me3
spellingShingle Vera Inácio
Madalena T. Martins
José Graça
Leonor Morais-Cecílio
Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes Expression
Frontiers in Plant Science
CORK
phellogen
lenticels
lenticular phellogen
5-mC
H3K4Me3
title Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes Expression
title_full Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes Expression
title_fullStr Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes Expression
title_full_unstemmed Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes Expression
title_short Cork Oak Young and Traumatic Periderms Show PCD Typical Chromatin Patterns but Different Chromatin-Modifying Genes Expression
title_sort cork oak young and traumatic periderms show pcd typical chromatin patterns but different chromatin modifying genes expression
topic CORK
phellogen
lenticels
lenticular phellogen
5-mC
H3K4Me3
url https://www.frontiersin.org/article/10.3389/fpls.2018.01194/full
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AT josegraca corkoakyoungandtraumaticperidermsshowpcdtypicalchromatinpatternsbutdifferentchromatinmodifyinggenesexpression
AT leonormoraiscecilio corkoakyoungandtraumaticperidermsshowpcdtypicalchromatinpatternsbutdifferentchromatinmodifyinggenesexpression