Differential DNA Methylation Patterns Are Related to Phellogen Origin and Quality of Quercus suber Cork

Inácio, Vera; Barros, Pedro M.; Costa, Alexandre; Roussado, C.; Gonçalves, Elsa; Costa, Rita; Graça, José; Oliveira, M. Margarida; Morais-Cecílio, Leonor

doi:10.1371/journal.pone.0169018

Cited by 20 publications

(25 citation statements)

References 65 publications

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“…The studied traits were porosity coefficient, and pores area, length, and roundness ( Supplementary Table 3 ), described in detail elsewhere (Inácio et al, 2017). …”

Section: Methodsmentioning

confidence: 99%

“…The planks were harvested at breast height (at 1.30 m height from soil) from two adult trees located at Tapada da Ajuda field, Lisbon and seven adult trees located at a cork oak stand ( montado ) in Herdade dos Leitões, Montargil, Portugal. Trees were selected based on their cork quality parameters previously characterized ( Inácio et al, 2017 ). All tissues were harvested during the period of more intense phellogen activity between July and September 2016.…”

Section: Methodsmentioning

confidence: 99%

“…Few studies were conducted in cork oak such as in pollen nuclei ( Ribeiro et al, 2009 ), revealing an unexpected pattern of marks associated either with gene silencing or activation. Also, DNA methylation levels were correlated with tissue maturity during embryogenesis ( Rodríguez-Sanz et al, 2014 ; Pérez et al, 2015 ), and with differences in cork cellular characteristics (cork quality traits) which could be directly related to original ( Inácio et al, 2017 ) or traumatic phellogen activity ( Ramos et al, 2013 ; Inácio et al, 2017 ). Notwithstanding the crucial role played by the cork as a protective tissue and its highly valued product, studies on the role of these modifications in cork formation and differentiation are still scarce.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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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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“…The studied traits were porosity coefficient, and pores area, length, and roundness ( Supplementary Table 3 ), described in detail elsewhere (Inácio et al, 2017). …”

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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“…AtSUVH4 is the best known protein of the SUVH group and is involved mainly in the maintenance of cytosine methylation in a non-CG context [84,85]. DNA methylation variability may contribute to cork cell characteristics linked to quality [86]. Inácio et al (2018) emphasized the presence of both DNA and H3K9 methylation silencing pathways in cork.…”

Section: Discussionmentioning

confidence: 99%

Genome-Wide Identification of Epigenetic Regulators in Quercus suber

Silva

Sobral

Magalhães

et al. 2020

Preprint

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Modifications of DNA and histones, including methylation and acetylation, are critical for the epigenetic regulation of gene expression during plant development, particularly during environmental adaptation processes. However, information on the enzymes catalyzing all these modifications in perennial trees, such as Quercus suber, is still not available. In this study, several epigenetic modifier proteins, including eight DNA methyltransferases (DNA Mtases), three DNA demethylases (DDMEs) and ninety-one histone modifiers including thirty-five histone methyltransferases (HMTs), twenty-six histone demethylases (HDMTs), eight histone acetyltransferases (HATs) and twenty-two histone acetylases (HDACs) were identified in Q. suber. Phylogenetic analyses of the DNA and histone modifier proteins were performed using several plant species homologs, enabling the classification of the Q. suber proteins. Additional in silico analysis showed that some Q. suber DNA Mtases, DMEs and histone modifiers have the typical domains found in the plant model Arabidopsis, which might suggest a conserved functional role. A link between the expression levels of each gene in different Q. suber tissues (buds, flowers, acorns, embryos, cork and roots) with the functions already known for their closest homologs in other species was also established. Therefore, the data generated here are important for future studies exploring the role of epigenetic regulators in this economically important species.

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“…Consequently, its biomechanical properties will influence wall flexibility and strength. Recent reports point out to environmental influence on cork annual growth, porosity and thickness (Inácio et al, 2017; Lauw et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Phellem Cell-Wall Components Are Discriminants of Cork Quality in Quercus suber

et al. 2019

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Cork is a renewable, non-wood high valued forest product, with relevant ecological and economic impact in the Mediterranean-type ecosystems. Currently, cork is ranked according to its commercial quality. The most valuable planks are chosen for cork stoppers production. Cork planks with adequate thickness and porosity are classified as stoppable quality cork (SQC). The chemical composition of cork is known, but the regulation of metabolic pathways responsible of cork production and composition, hence of cork quality, is largely unknown. Here, we tested the hypothesis that post-genomic events may be responsible for the development of SQC and N-SQC (non-stoppable quality cork). Here, we show that combined proteomics and targeted metabolomics (namely soluble and cell wall bound phenolics) analyzed on recently formed phellem allows discriminate cork planks of different quality. Phellem cells of SQC and N-SQC displayed different reducing capacity, with consequential impact on both enzymatic pathways (e.g., glycolysis) and other cellular functions, including cell wall assembly and suberization. Glycolysis and respiration related proteins were abundant in both cork quality groups, whereas the level of several proteins associated to mitochondrial metabolism was higher in N-SQC. The soluble and cell wall-bound phenolics in recently formed phellem clearly discriminated SQC from N-SCQ. In our study, SQC was characterized by a high incorporation of aromatic components of the phenylpropanoid pathway in the cell wall, together with a lower content of hydrolysable tannins. Here, we propose that the level of hydrolysable tannins may represent a valuable diagnostic tool for screening recently formed phellem, and used as a proxy for the quality grade of cork plank produced by each tree.

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Differential DNA Methylation Patterns Are Related to Phellogen Origin and Quality of Quercus suber Cork

Cited by 20 publications

References 65 publications

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

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

Genome-Wide Identification of Epigenetic Regulators in Quercus suber

Phellem Cell-Wall Components Are Discriminants of Cork Quality in Quercus suber

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