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

ABSTRACT: 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.

SUBMITTER: Inacio V

PROVIDER: S-EPMC6120546 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundCork oak (Quercus suber L.) has a natural distribution across western Mediterranean regions and is a keystone forest tree species in these ecosystems. The fruiting phase is especially critical for its regeneration but the molecular mechanisms underlying the biochemical and physiological changes during cork oak acorn development are poorly understood. In this study, the transcriptome of the cork oak acorn, including the seed, was characterized in five stages of development, from early development to acorn maturation, to identify the dominant processes in each stage and reveal transcripts with important functions in gene expression regulation and response to water.ResultsA total of 80,357 expressed sequence tags (ESTs) were de novo assembled from RNA-Seq libraries representative of the several acorn developmental stages. Approximately 7.6 % of the total number of transcripts present in Q. suber transcriptome was identified as acorn specific. The analysis of expression profiles during development returned 2,285 differentially expressed (DE) transcripts, which were clustered into six groups. The stage of development corresponding to the mature acorn exhibited an expression profile markedly different from other stages. Approximately 22 % of the DE transcripts putatively code for transcription factors (TF) or transcriptional regulators, and were found almost equally distributed among the several expression profile clusters, highlighting their major roles in controlling the whole developmental process. On the other hand, carbohydrate metabolism, the biological pathway most represented during acorn development, was especially prevalent in mid to late stages as evidenced by enrichment analysis. We further show that genes related to response to water, water deprivation and transport were mostly represented during the early (S2) and the last stage (S8) of acorn development, when tolerance to water desiccation is possibly critical for acorn viability.ConclusionsTo our knowledge this work represents the first report of acorn development transcriptomics in oaks. The obtained results provide novel insights into the developmental biology of cork oak acorns, highlighting transcripts putatively involved in the regulation of the gene expression program and in specific processes likely essential for adaptation. It is expected that this knowledge can be transferred to other oak species of great ecological value.

Project description:BACKGROUND: Cork oak (Quercus suber) is one of the rare trees with the ability to produce cork, a material widely used to make wine bottle stoppers, flooring and insulation materials, among many other uses. The molecular mechanisms of cork formation are still poorly understood, in great part due to the difficulty in studying a species with a long life-cycle and for which there is scarce molecular/genomic information. Cork oak forests are of great ecological importance and represent a major economic and social resource in Southern Europe and Northern Africa. However, global warming is threatening the cork oak forests by imposing thermal, hydric and many types of novel biotic stresses. Despite the economic and social value of the Q. suber species, few genomic resources have been developed, useful for biotechnological applications and improved forest management. RESULTS: We generated in excess of 7 million sequence reads, by pyrosequencing 21 normalized cDNA libraries derived from multiple Q. suber tissues and organs, developmental stages and physiological conditions. We deployed a stringent sequence processing and assembly pipeline that resulted in the identification of ~159,000 unigenes. These were annotated according to their similarity to known plant genes, to known Interpro domains, GO classes and E.C. numbers. The phylogenetic extent of this ESTs set was investigated, and we found that cork oak revealed a significant new gene space that is not covered by other model species or EST sequencing projects. The raw data, as well as the full annotated assembly, are now available to the community in a dedicated web portal at http://www.corkoakdb.org. CONCLUSIONS: This genomic resource represents the first trancriptome study in a cork producing species. It can be explored to develop new tools and approaches to understand stress responses and developmental processes in forest trees, as well as the molecular cascades underlying cork differentiation and disease response.

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

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