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Bark, the outermost tissue, plays an important role in protecting trees from damage induced by living organisms and the surrounding environment. Bark differs from the xylem primarily by the presence of suberin in cork cell walls. However, few studies have examined the role of suberin and its interactions with other chemical components in the cork. Consequently, this study aimed to understand the distribution of chemical components, including suberin and lignin, and their respective roles in cork cell walls, using Cerasus jamasakura (Siebold ex Koidz.) H. Ohba. Suberin and lignin were gradually and selectively removed from thin strip specimens. Fourier transform infrared (FTIR) spectroscopy suggested that desuberinization removed both suberin and part of the other matrix substances within a few minutes of treatment, whereas delignification exclusively removed lignin. Further microscopic observation revealed that suberin present was mainly in the secondary wall of cork cells, whereas lignin was present in both the tertiary wall and compound middle lamella. In addition, the cell wall collapse of the cork was only found in desuberinized specimens, whereas delignified specimens only showed monotonic contraction. Taken together, these results suggest that the presence of suberin in the cork contributes to the shape stability of cork cell walls.

Internal root aeration enables waterlogging‐tolerant species to grow in anoxic soil. Secondary aerenchyma, in the form of aerenchymatous phellem, is of importance to root aeration in some dicotyledonous species. Little is known about this type of aerenchyma in comparison with primary aerenchyma. Micro‐computed tomography was employed to visualize, in three dimensions, the microstructure of the aerenchymatous phellem in roots of Melilotus siculus . Tissue porosity and respiration were also measured for phellem and stelar tissues. A multiscale, three‐dimensional, diffusion–respiration model compared the predicted O 2 profiles in roots with those measured using O 2 microelectrodes. Micro‐computed tomography confirmed the measured high porosity of aerenchymatous phellem (44–54%) and the low porosity of stele (2–5%) A network of connected gas spaces existed in the phellem, but not within the stele. O 2 partial pressures were high in the phellem, but fell below the detection limit in the thicker upper part of the stele, consistent with the poorly connected low porosity and high respiratory demand. The presented model integrates and validates micro‐computed tomography with measured radial O 2 profiles for roots with aerenchymatous phellem, confirming the existence of near‐anoxic conditions at the centre of the stele in the basal parts of the root, coupled with only hypoxic conditions towards the apex.

During secondary growth in most eudicots and gymnosperms, the periderm replaces the epidermis as the frontier tissue protecting the vasculature from biotic and abiotic stresses. Despite its importance, the mechanisms underlying periderm establishment and formation are largely unknown. The herbaceous Arabidopsis thaliana undergoes secondary growth, including periderm formation in the root and hypocotyl. Thus, we focused on these two organs to establish a framework to study periderm development in a model organism. We identified a set of characteristic developmental stages describing periderm growth from the first cell division in the pericycle to the shedding of the cortex and epidermis. We highlight that two independent mechanisms are involved in the loosening of the outer tissues as the endodermis undergoes programmed cell death, whereas the epidermis and the cortex are abscised. Moreover, the phellem of Arabidopsis, as in trees, is suberized, lignified and peels off. In addition, putative regulators from oak and potato are also expressed in the Arabidopsis periderm. Collectively, the periderm of Arabidopsis shares many characteristics/features of woody and tuberous periderms, rendering Arabidopsis thaliana an attractive model for cork biology.

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.

Suberin and wax deposited in the cork (phellem) layer of the periderm form the lipophilic barrier that protects mature plant organs. Periderm lipids have been widely studied for their protective function with regards to dehydration and for how they respond to environmental stresses and wounding. However, despite advances in the biosynthetic pathways of suberin and associated wax, little is known about the regulation of their deposition. Here, we report on a potato NAC transcription factor gene, StNAC103, induced in the tuber phellem (skin). The StNAC103 promoter is active in cells undergoing suberization such as in the basal layer of the phellem, but also in the root apical meristem. Gene silencing in potato periderm correlates with an increase in the suberin and wax load, and specifically in alkanes, ω-hydroxyacids, diacids, ferulic acid, and primary alcohols. Concomitantly, silenced lines also showed up-regulation of key genes related to the biosynthesis and transport of suberin and wax in the tuber periderm. Taken together, our results suggest that StNAC103 has a role in the tight regulation of the formation of apoplastic barriers and is, to the best of our knowledge, the first candidate gene to be identified as being involved in the repression of suberin and wax deposition.

Several regulators of phellem/cork formation have been identified in recent years, using mainly transcriptomic approaches. However, this developmental process, showing parallels to the functioning of vascular cambium, remains poorly understood. The cork oak tree ( Quercus suber L.) exhibits a remarkable ability to form a traumatic phellogen after debarking, enabling sustainable cork production. We aimed at uncovering post-transcriptional mechanisms controlled by miRNAs, specifically involved in regulating phellogen functioning and phellem differentiation in cork oak. To achieve this, we conducted a comparative analysis of the small RNA transcriptome between differentiating phellem and xylem, both originating from secondary meristems (phellogen and vascular cambium). In addition to identifying miRNAs exclusive to phellogen/phellem tissues, we discovered 246 differentially expressed miRNAs between the two tissues, of which 74 are conserved. The most abundant miRNA families found in phellem tissues were MIR165/166, MIR167, MIR168 and MIR390. By analysing miRNA predicted targets and their expression in the same tissues, many of the differentially expressed miRNAs were found associated with sequence-specific DNA binding functions. Within these, transcription factor families HD-ZIP III, WRKY, NAC and MYB were highlighted as key in phellem differentiation. Furthermore, hormone-mediated signalling pathways, particularly involving auxin, appeared as an enriched biological process, as several ARF transcripts, among other auxin signalling genes like IAA11, ARF18 and ARF19, were identified as putative targets of conserved or novel miRNAs. Overall, our results provide a comprehensive overview of the miRNA landscape during cork formation, providing valuable knowledge for further functional studies and potential practical applications in forest management. Graphical Abstract

Bark, the outermost tissue, plays an important role in protecting trees from damage induced by living organisms and the surrounding environment. Bark differs from the xylem primarily by the presence of suberin in cork cell walls. However, few studies have examined the role of suberin and its interactions with other chemical components in the cork. Consequently, this study aimed to understand the distribution of chemical components, including suberin and lignin, and their respective roles in cork cell walls, using Cerasus jamasakura (Siebold ex Koidz.) H. Ohba. Suberin and lignin were gradually and selectively removed from thin strip specimens. Fourier transform infrared (FTIR) spectroscopy suggested that desuberinization removed both suberin and part of the other matrix substances within a few minutes of treatment, whereas delignification exclusively removed lignin. Further microscopic observation revealed that suberin present was mainly in the secondary wall of cork cells, whereas lignin was present in both the tertiary wall and compound middle lamella. In addition, the cell wall collapse of the cork was only found in desuberinized specimens, whereas delignified specimens only showed monotonic contraction. Taken together, these results suggest that the presence of suberin in the cork contributes to the shape stability of cork cell walls.

• Light-induced tuber greening is one of the most important quality defects of potato. Although varietal and maturity factors are known to affect greening resistance, physiological mechanisms of resistance are poorly understood. We proposed that physiological and biochemical factors within the tuber periderm provide resistance and hypothesised that resistance is primarily related to suberin content. • We investigated differences in the tuber periderm between genotypes and tuber maturities that varied in greening propensity. We examined suberin and light-induced pigment accumulation, and phellem cell development and studied greening propensity in mutant and chemically treated tubers with enhanced suberisation. • Resistance to greening was strongly linked to increased suberin in the periderm, which varied with variety and tuber maturity. Furthermore, greening was reduced in mutant and chemically treated tubers with enhanced suberisation. Increases in phellem cell layers and light-induced carotenoids and anthocyanins were identified as secondary resistance factors. • Our work represents the first physiological mechanism of varietal and tuber maturity resistance to greening, expanding the known functionality of suberin and providing for the first time a biomarker that will aid producers and breeders in selection and improvement of potato varieties for greening resistance.

Abstract Background and Aims Submergence is a severe stress for most plants. Melilotus siculus is a waterlogging- (i.e. root zone hypoxia) tolerant annual forage legume, but data were lacking for the effects of partial and full submergence of the shoots. The aim was to compare the tolerance to partial and full submergence of 15 M. siculus accessions and to assess variation in traits possibly contributing to tolerance. Recovery ability post-submergence was also evaluated. Methods A factorial experiment imposed treatments of water level [aerated root zone with shoots in air as controls, stagnant root zone with shoots in air, stagnant root zone with partial (75 %) or full shoot submergence] on 15 accessions, for 7 d on 4-week-old plants in a 20/15 °C day/night phytotron. Measurements included: shoot and root growth, hyponastic petiole responses, petiole gas-filled spaces, leaflet sugars, leaflet surface hydrophobicity, leaflet gas film thickness and phellem area near the base of the main root. Recovery following full submergence was also assessed. Key Results Accessions differed in shoot and root growth during partial and full shoot submergence. Traits differing among accessions and associated with tolerance were leaflet gas film thickness upon submergence, gas-filled spaces in petioles and phellem tissue area near the base of the main root. All accessions were able to re-orientate petioles towards the vertical under both partial and full submergence. Petiole extension rates were maintained during partial submergence, but decreased during full submergence. Leaflet sugars accumulated during partial submergence, but were depleted during full submergence. Growth resumption after full submergence differed among accessions and was positively correlated with the number of green leaves retained at desubmergence. Conclusions Melilotus siculus is able to tolerate partial and full submergence of at least 7 d. Leaflet surface hydrophobicity and associated gas film retention, petiole gas-filled porosity and root phellem abundance are important traits contributing to tolerance. Post-submergence recovery growth differs among accessions. The ability to retain green leaves is essential to succeed during recovery.

Background The periderm is basic for land plants due to its protective role during radial growth, which is achieved by the polymers deposited in the cell walls. In most trees, like holm oak, the first periderm is frequently replaced by subsequent internal periderms yielding a heterogeneous outer bark made of a mixture of periderms and phloem tissues, known as rhytidome. Exceptionally, cork oak forms a persistent or long-lived periderm which results in a homogeneous outer bark of thick phellem cell layers known as cork. Cork oak and holm oak distribution ranges overlap to a great extent, and they often share stands, where they can hybridize and produce offspring showing a rhytidome-type bark. Results Here we use the outer bark of cork oak, holm oak, and their natural hybrids to analyse the chemical composition, the anatomy and the transcriptome, and further understand the mechanisms underlying periderm development. We also include a unique natural hybrid individual corresponding to a backcross with cork oak that, interestingly, shows a cork-type bark. The inclusion of hybrid samples showing rhytidome-type and cork-type barks is valuable to approach cork and rhytidome development, allowing an accurate identification of candidate genes and processes. The present study underscores that abiotic stress and cell death are enhanced in rhytidome-type barks whereas lipid metabolism and cell cycle are enriched in cork-type barks. Development-related DEGs showing the highest expression, highlight cell division, cell expansion, and cell differentiation as key processes leading to cork or rhytidome-type barks. Conclusion Transcriptome results, in agreement with anatomical and chemical analyses, show that rhytidome and cork-type barks are active in periderm development, and suberin and lignin deposition. Development and cell wall-related DEGs suggest that cell division and expansion are upregulated in cork-type barks whereas cell differentiation is enhanced in rhytidome-type barks.