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
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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.
The Making of Plant Armor: The Periderm Serra, Olga; Mähönen, Ari Pekka; Hetherington, Alexander J ...
Annual review of plant biology,
2022-May-20, Letnik:
73, Številka:
1
Journal Article
Recenzirano
Odprti dostop
The periderm acts as armor protecting the plant's inner tissues from biotic and abiotic stress. It forms during the radial thickening of plant organs such as stems and roots and replaces the function ...of primary protective tissues such as the epidermis and the endodermis. A wound periderm also forms to heal and protect injured tissues. The periderm comprises a meristematic tissue called the phellogen, or cork cambium, and its derivatives: the lignosuberized phellem and the phelloderm. Research on the periderm has mainly focused on the chemical composition of the phellem due to its relevance as a raw material for industrial processes. Today, there is increasing interest in the regulatory network underlying periderm development as a novel breeding trait to improve plant resilience and to sequester CO
2
. Here, we discuss our current understanding of periderm formation, focusing on aspects of periderm evolution, mechanisms of periderm ontogenesis, regulatory networks underlying phellogen initiation and cork differentiation, and future challenges of periderm research.
Quercus suber (cork oak) is a sustainably exploited forest resource, producing a unique renewable raw material known as cork. With drought events imposing a negative impact on tree vitality, further ...research is needed to enhance our understanding of the genetic and environmental factors regulating cork development, to foster the resilience of cork oak ecosystems. We focused on characterizing long-term drought-induced molecular adaptations occurring in stems, and identifying key genetic pathways regulating phellem development. One-year-old cork oak plants were grown for 6 months under well-watered, or water-deficit (WD) conditions and main stems were targeted for histological characterization and transcriptomic analysis. WD treatment reduced meristem activity at both vascular cambium and phellogen, impairing secondary growth. Transcriptional analysis revealed a global downregulation of genes related to cell division, differentiation, and cell wall biogenesis in phellem, inner bark, and xylem under WD conditions. Phellem and inner bark showed upregulation of photosynthesis-related genes, highlighting a determinant role of stem photosynthesis in the adaptation to long-term drought. We show that developing phellem cells contain chloroplasts and their abundance increases under WD. Lastly, we propose new candidate regulatory genes involved in regulating phellogen activity and demonstrate the role of phellem in drought-induced bark photosynthesis in young plants.
•Drought negatively affects secondary growth, particularly at the vascular cambium.•New candidate genes regulating phellogen activity in crosstalk with drought are proposed.•Phellem is an active player in drought-induced bark photosynthesis in young plants.
Vascular plants with secondary growth develop a periderm mostly composed of dead suberized cork cells to face environmental hostile conditions. Cork oak has a highly active and long-living phellogen ...forming a remarkably thick periderm that is periodically debarked for industrial purposes. This wounding originates the quick formation of a new traumatic periderm, making cork oak an exceptional model to study the first periderm differentiation during normal development in young sprigs and traumatic (wound) periderm formation after debarking. Here we studied the poorly known first periderm differentiation steps that involve cell wall suberization, polyphenolic accumulation, and programmed cell death (PCD) by combining TEM, histochemical, and molecular methods in periderms from young sprigs. These processes were further compared with traumatic periderms formed after wounding using molecular and histochemical techniques, such as the polyphenolic accumulation. In the first periderms from young sprigs, four distinct differentiation stages were defined according to the presence of PCD morphological features. First young and traumatic periderms showed an upregulation of genes related to suberin biosynthesis, proanthocyanidins biosynthesis and transport, autophagy, and PCD. Traumatic periderms revealed an overall upregulation of these genes, likely resulting from ontogeny differences and distinct phellogen origin associated with a faster metabolism, highlighting the impact of wounding on phellogen activity after debarking. First periderms from young sprigs showed gradual accumulation of proanthocyanidins in the vacuoles throughout PCD stages until total filled lumens, whereas in traumatic periderms these compounds were found cell wall linked in already empty cells. This work enabled a comprehensive overview of the cork cells differentiation processes contributing to deepening the knowledge of the fundamental ontogenic program of this protective tissue, which is also a unique forest product, constituting the basis of a sustainable and profitable industry.
Tree bark is a highly specialized array of tissues that plays important roles in plant protection and development. Bark tissues develop from two lateral meristems; the phellogen (cork cambium) ...produces the outermost stem–environment barrier called the periderm, while the vascular cambium contributes with phloem tissues. Although bark is diverse in terms of tissues, functions and species, it remains understudied at higher resolution.
We dissected the stem of silver birch (Betula pendula) into eight major tissue types, and characterized these by a combined transcriptomics and metabolomics approach. We further analyzed the varying bark types within the Betulaceae family.
The two meristems had a distinct contribution to the stem transcriptomic landscape. Furthermore, inter- and intraspecies analyses illustrated the unique molecular profile of the phellem. We identified multiple tissue-specific metabolic pathways, such as the mevalonate/betulin biosynthesis pathway, that displayed differential evolution within the Betulaceae. A detailed analysis of suberin and betulin biosynthesis pathways identified a set of underlying regulators and highlighted the important role of local, small-scale gene duplication events in the evolution of metabolic pathways.
This work reveals the transcriptome and metabolic diversity among bark tissues and provides insights to its development and evolution, as well as its biotechnological applications.
•The globoid stem galls under senescence can still react to biotic stimuli.•Ant movement in and out of the galls stimulate plant cell reactions.•The post-gall senescence reveals a reassumption of ...plant cell cycles.•The gall-ant-fungi interaction promotes a particular case of post-gall senescence.•Empty galls enter senescence for they close after the escape of the galling insect.
Eremanthus erythropappus (DC.) McLeisch (Asteraceae), popularly known as “candeia”, is a common species in Minas Gerais state – Brazil and hosts six gall morphotypes. Our focus relies on the diagnosis of how one of these morphotypes, i.e., globoid stem galls induced by Neolasioptera sp. (Diptera: Cecidomyiidae) in the senescent stage can still react to the biotic stimuli of ants and fungi. These senescent globoid galls can be found in two forms: (1) empty galls characterized by the exit channel scar closed by plant tissue development, and (2) ant-occupied galls characterized by open exit channels, and the gall chamber occupied by ants and fungi. We hypothesize that the anatomical profile of senescent galls on E. erythropappus may favour the formation of peculiar ant-nest galls. The anatomical analyses revealed that phellogen activity along the exit channel completely closes the empty-galls after the escape of the galling Neolasioptera sp. The ant-occupied galls host seven different genera of ants, whose movement in and out of the gall may prevent the closing of the exit channel and allow the invasion of opportunistic fungal hyphae. The gall-ant-fungi interaction relies on the ants mechanically maintaining the opening of the exit channel previously dug by the galling Neolasioptera, while the fungi stimulate the metabolism of the cells in gall tissues. This interaction between E. erythropappus, fungi and ants, is responsible for the tissue responses and the maintenance of the peculiar ant-nest galls.
•Inner bark thickness at the community level vary across a continental-size biome range.•There was little variation in outer bark for branches and main stem.•Higher water deficit was associated with ...higher inner bark thickness•Bark trait composition of species in core region were nested within peripheral regions
Savanna tree communities occurring in confluence zones with other biomes likely experience different environmental pressures, resulting in shifts in the selection of individual traits, the combinations of such traits, and species composition. In seasonally dry fire-prone environments, plant survival is presumably associated with adaptive changes in bark properties related to fire protection and water storage. Here, we integrated the multiple functions of the bark to investigate whether different selective pressures could influence patterns of variation in bark structure and allocation across species in a broad geographical range. We measured thickness, density, and water content of the inner and outer bark in branches and the main stem of the 51 most abundant species in three savanna communities differing in climatic aridity, one located at the core region of Cerrado in Central Brazil and the other two at its periphery, in the transition zones with Amazonia and Atlantic forest biomes. We found no difference in outer bark thickness but markedly difference in inner bark thickness between the three plant communities. In the central region, where dry season is long and fire is frequent, branches and main stem showed thicker inner bark. Contrastingly, in the south periphery region, where dry season is short, species showed thinner inner bark in both branches and main stem. Species from the north periphery region, where mean annual precipitation is higher, but fire is frequent and the dry season is also long, showed similar main stem inner bark thickness, but thinner branch inner bark compared to core region species. Our findings support the idea that investing in inner bark thickness and bark moisture may be the most advantageous strategy in plant communities that suffer from high evaporative demand during a long period and are at a high risk of fire.
The development of plant tissues and organs during post-embryonic growth occurs through the activity of both primary and secondary meristems. While primary meristems (root and shoot apical meristems) ...promote axial plant growth, secondary meristems (vascular and cork cambium or phellogen) promote radial thickening and plant axes strengthening. The vascular cambium forms the secondary xylem and phloem, whereas the cork cambium gives rise to the periderm that envelops stems and roots. Periderm takes on an increasingly important role in plant survival under climate change scenarios, but it is also a forest product with unique features, constituting the basis of a sustainable and profitable cork industry. There is established evidence that epigenetic mechanisms involving histone post-translational modifications, DNA methylation, and small RNAs play important roles in the activity of primary meristem cells, their maintenance, and differentiation of progeny cells. Here, we review the current knowledge on the epigenetic regulation of secondary meristems, particularly focusing on the phellogen activity. We also discuss the possible involvement of DNA methylation in the regulation of periderm contrasting phenotypes, given the potential impact of translating this knowledge into innovative breeding programs.
ABSTRACT The curing before storing the tubers is necessary for the formation of damage periderm, promoting greater post-harvest conservation. In which, the rate curing and the maintenance of the ...quality of the tubers depends on the temperature. This way, the search aimed to determine the effect of the curing temperature on the regeneration of the damage periderm and on the carbohydrate metabolism of cultivar Markies and Challenger potatoes tubers destined for industry. For this, the curing was carried out for 14 days on tubers with excoriation injury and tubers without excoriation (control) at temperatures of 8, 14 and 20 °C (RH ± 90%). The fresh mass loss rate (FMLR) daily was higher in the excoriation tubers. The excoriation injury and the temperature of 8 °C increased the total soluble sugar (TSS), reducing sugars (RS) and non-reducing sugars (NRS) of the tubers of ‘Markies’ and TSS of ‘Challenger’. The excoriation injury tuber the process of cell division was induced in the periclinal plane, forming phellogen, with few layers of collapsed cortical cells. In both cultivars, at 14 °C the new phellogen became more evident and at 20 °C some layers of a new cork were formed. In ‘Markies’ the development of new periderm was earlier than in ‘Challenger’, even at 8 °C. It is concluded that the temperature of 14 ºC provided better curing and regeneration of the excoriation periderm tubers maintain post-fry quality of potatoes destination by industry processing.
Key message
This compilation is focused on the role of cork oak periderm, a protective layer with unique physical and chemical traits for the cork industry, highlighting the recent periderm-specific ...genomic resources available.
Cork oak is a unique species with the ability to produce a continuous and renewable cork throughout its lifespan. Periderm is a protective tissue composed of the phellem, phellogen, and phelloderm that replaces the epidermis. Phellem or “cork”, the outermost layer, is produced by the original phellogen, a secondary meristem originated from the dedifferentiation of mature parenchyma cells. The formation and differentiation of periderm have been widely studied demonstrating the importance of fatty acid biosynthesis, phenylpropanoid, and metabolism of suberin, a complex glycerol-based polymer and the principal component of phellem. The contributions of several areas reveal new clues concerning the molecular mechanisms behind periderm differentiation. However, the whole process is still poorly understood. In this review, we compile information regarding the cellular structure and molecular basis, including the regulatory network of periderm formation and differentiation, focusing on the cork oak. The cork quality and its genetic and epigenetic mechanisms are also explored, highlighting the importance of molecular regulation in such economically important species. An increased understanding of the all periderm differentiation process may serve as a basis for future studies on functional genomics with an impact on fundamental science and on the forest industry for the production of high-quality cork.
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