The Making of Plant Armor: The Periderm

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 CO2. 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. Expected final online publication date for the Annual Review of Plant Biology, Volume 73 is May 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Spatial and temporal patterns of wound periderm development in Cryptomeria japonica bark

Limited investigations have been carried out on the physiological and growth responses of bark to wounding, even though wound periderms play crucial roles in tree defenses. To understand the mechanisms of wound periderm formation, we studied the growth responses and structural changes of wounded bark of three Cryptomeria japonica individuals. We observed the developmental time frame and morphology of wound periderms around mechanically induced wounds in summer. The wound responses included discoloration, lignification, and suberization in tissues present at the time of wounding, followed by wound periderm formation and secondary metabolite deposition. The trees had developed wound periderms approximately 4 weeks after wounding. The wound periderms were within 3 mm in the axial directions and within 1 mm in the lateral directions from the wound surfaces. The distinct patterns of wound periderm formation in the axial and lateral regions resulted from the arrangement and anatomical features of the cells adjacent to the wounds. The wound phellem cells were tangentially narrower and axially shorter in the side and upper/lower regions, respectively, of the wounds. Therefore, the cell division frequencies in the planes parallel to the wound surface may be greater than those in the other directions. Wound reactions in bark might initially be triggered by microenvironmental changes, such as the spread of desiccation, which depends directly on the morphology of phloem cell complexes.

Peridermal fruit skin formation in Actinidia sp. (kiwifruit) is associated with genetic loci controlling russeting and cuticle formation

Background The skin (exocarp) of fleshy fruit is hugely diverse across species. Most fruit types have a live epidermal skin covered by a layer of cuticle made up of cutin while a few create an outermost layer of dead cells (peridermal layer). Results In this study we undertook crosses between epidermal and peridermal skinned kiwifruit, and showed that epidermal skin is a semi-dominant trait. Furthermore, backcrossing these epidermal skinned hybrids to a peridermal skinned fruit created a diverse range of phenotypes ranging from epidermal skinned fruit, through fruit with varying degrees of patches of periderm (russeting), to fruit with a complete periderm. Quantitative trait locus (QTL) analysis of this population suggested that periderm formation was associated with four loci. These QTLs were aligned either to ones associated with russet formation on chromosome 19 and 24, or cuticle integrity and coverage located on chromosomes 3, 11 and 24. Conclusion From the segregation of skin type and QTL analysis, it appears that skin development in kiwifruit is controlled by two competing factors, cuticle strength and propensity to russet. A strong cuticle will inhibit russeting while a strong propensity to russet can create a continuous dead skinned periderm.

Epithelial dynamics shed light on the mechanisms underlying ear canal defects

ABSTRACTDefects in ear canal development can cause severe hearing loss as sound waves fail to reach the middle ear. Here, we reveal new mechanisms that control human canal development and highlight for the first time the complex system of canal closure and reopening. These processes can be perturbed in mutant mice and in explant culture, mimicking the defects associated with canal atresia. The more superficial part of the canal forms from an open primary canal that closes and then reopens. In contrast, the deeper part of the canal forms from an extending solid meatal plate that opens later. Closure and fusion of the primary canal was linked to loss of periderm, with failure in periderm formation in Grhl3 mutant mice associated with premature closure of the canal. Conversely, inhibition of cell death in the periderm resulted in an arrest of closure. Once closed, re-opening of the canal occurred in a wave, triggered by terminal differentiation of the epithelium. Understanding these complex processes involved in canal development sheds light on the underlying causes of canal atresia.

Russeting in Apple Is Initiated After Exposure to Moisture Ends—I. Histological Evidence

Russeting (periderm formation) is a critical fruit-surface disorder in apple (Malus × domestica Borkh.). The first symptom of insipient russeting is cuticular microcracking. Humid and rainy weather increases russeting. The aim was to determine the ontogeny of moisture-induced russeting in ‘Pinova’ apple. We recorded the effects of duration of exposure to water and the stage of fruit development at exposure on microcracking, periderm formation and cuticle deposition. Early on (21 or 31 days after full bloom; DAFB) short periods (2 to 12 d) of moisture exposure induced cuticular microcracking—but not later on (66 or 93 DAFB). A periderm was not formed during moisture exposure but 4 d after exposure ended. A periderm was formed in the hypodermis beneath a microcrack. Russeting frequency and severity were low for up to 4 d of moisture exposure but increased after 6 d. Cuticle thickness was not affected by moisture for up to 8 d but decreased for longer exposures. Cuticular ridge thickness decreased around a microcrack. In general, moisture did not affect cuticular strain release. We conclude that a hypodermal periderm forms after termination of moisture exposure and after microcrack formation. Reduced cuticle deposition may cause moisture-induced microcracking and, thus, russeting.

Sox2 Controls Periderm and Rugae Development to Inhibit Oral Adhesions

In humans, ankyloglossia and cleft palate are common congenital craniofacial anomalies, and these are regulated by a complex gene regulatory network. Understanding the genetic underpinnings of ankyloglossia and cleft palate will be an important step toward rational treatment of these complex anomalies. We inactivated the Sry (sex-determining region Y)–box 2 ( Sox2) gene in the developing oral epithelium, including the periderm, a transient structure that prevents abnormal oral adhesions during development. This resulted in ankyloglossia and cleft palate with 100% penetrance in embryos examined after embryonic day 14.5. In Sox2 conditional knockout embryos, the oral epithelium failed to differentiate, as demonstrated by the lack of keratin 6, a marker of the periderm. Further examination revealed that the adhesion of the tongue and mandible expressed the epithelial markers E-Cad and P63. The expanded epithelia are Sox9-, Pitx2-, and Tbx1-positive cells, which are markers of the dental epithelium; thus, the dental epithelium contributes to the development of oral adhesions. Furthermore, we found that Sox2 is required for palatal shelf extension, as well as for the formation of palatal rugae, which are signaling centers that regulate palatogenesis. In conclusion, the deletion of Sox2 in oral epithelium disrupts palatal shelf extension, palatal rugae formation, tooth development, and periderm formation. The periderm is required to inhibit oral adhesions and ankyloglossia, which is regulated by Sox2. In addition, oral adhesions occur through an expanded dental epithelial layer that inhibits epithelial invagination and incisor development. This process may contribute to dental anomalies due to ankyloglossia.

Russeting in ‘Apple’ Mango: Triggers and Mechanisms

Russeting is an important surface disorder of many fruitcrop species. The mango cultivar ‘Apple’ is especially susceptible to russeting. Russeting compromises both fruit appearance and postharvest performance. The objective was to identify factors, mechanisms, and consequences of russeting in ‘Apple’ mango. Russeting was quantified on excised peels using image analysis and a categorical rating scheme. Water vapour loss was determined gravimetrically. The percentage of the skin area exhibiting russet increased during development. Russet began at lenticels then spread across the surface, ultimately forming a network of rough, brown patches over the skin. Cross-sections revealed stacks of phellem cells, typical of a periderm. Russet was more severe on the dorsal surface of the fruit than on the ventral and more for fruit in the upper part of the canopy than in the lower. Russet differed markedly across orchards sites of different climates. Russet was positively correlated with altitude, the number of rainy days, and the number of cold nights but negatively correlated with minimum, maximum, and mean daily temperatures, dew point temperature, and heat sum. Russeted fruit had higher transpiration rates than non-russeted fruits and higher skin permeance to water vapour. Russet in ‘Apple’ mango is due to periderm formation that is initiated at lenticels. Growing conditions conducive for surface wetness exacerbate russeting.

Anatomical Characteristics of Sunlight-induced Bark (Periderm) Coverages on Columnar Cacti of Central Mexico

More than twenty-three species of tall, long-lived columnar cacti from a large variety of locations within the Americas show sunlight-induced periderm development on their stems. Periderm coverages lead to cactus morbidity and mortality. Our objective was to determine if periderm coverage patterns and anatomical characteristics of periderm formation differ among five cactus species located at a single site. Periderm coverages, patterns of periderm coverages and histological changes during the periderm formation process were determined for five native species of tall, long-lived columnar cacti in the Tehuacán Valley of Puebla, Mexico during May to June 2019. Periderm coverages and patterns of periderm on cactus surface varied among the species. On surfaces, some species had periderm form at crests initially, while one species had initial periderm form where troughs join. All species had the same internal tissues but the characteristics of these tissues varied among species. In response to periderm formation, one species retained its cuticle while one species retained its hypodermis intact and another produced cork cells inside the hypodermis. Overall, the histological changes that result from periderm formation were specific for each species and no pair of species showed the same responses to periderm formation. In conjunction with data from species from South America, eight distinct scenarios of histological manifestations were documented. Although, each of the five cactus species were in the same location and received the same amount of sunlight exposures, each species showed unique periderm coverages on surfaces, unique anatomical characteristics and unique anatomical responses. Thus, location was not the primary determinant of responses.

Stepwise polarisation of developing bilayered epidermis is mediated by aPKC and E-cadherin in zebrafish

The epidermis, a multilayered epithelium, surrounds and protects the vertebrate body. It develops from a bilayered epithelium formed of the outer periderm and underlying basal epidermis. How apicobasal polarity is established in the developing epidermis has remained poorly understood. We show that both the periderm and the basal epidermis exhibit polarised distribution of adherens junctions in zebrafish. aPKC, an apical polarity regulator, maintains the robustness of polarisation of E-cadherin- an adherens junction component- in the periderm. E-cadherin in one layer controls the localisation of E-cadherin in the second layer in a layer non-autonomous manner. Importantly, E-cadherin controls the localisation and levels of Lgl, a basolateral polarity regulator, in a layer autonomous as well non-autonomous manner. Since periderm formation from the enveloping layer precedes the formation of the basal epidermis, our analyses suggest that peridermal polarity, initiated by aPKC, is transduced in a stepwise manner by E-cadherin to the basal layer.