Cork cells in cork oak periderms undergo programmed cell death and proanthocyanidin deposition.

Vera Inácio,Leonor Morais-Cecílio,Carolina Lobato,José Graça,Christophe Plomion

doi:10.1093/treephys/tpab031

Vera Inácio, Leonor Morais-Cecílio + Show 3 more

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https://doi.org/10.1093/treephys/tpab031

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Abstract

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 transmission electron microscopy, 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.

Highlights

To capture sunlight, vascular plants like trees have adapted by developing lignified stems that rise above other plants
We studied the formation of cork oak periderms from the first phellogen derivative cell layer to the well-developed isolating tissue by analyzing the various differentiation processes involved: cell wall suberization, phenolic tannin inclusions, and the programmed cell death (PCD) leading to the ultimate differentiation stage
Hereafter, we will refer to the samples collected from young sprigs as young differentiating cork (YDC) and samples collected from amadia cork planks as traumatic differentiating cork (TDC)

Summary

Introduction

Vascular plants like trees have adapted by developing lignified stems that rise above other plants These secondary growth stems are built from two meristems: the vascular cambium and the cork cambium or phellogen (Evert 2006). First and young periderms, which can be seen in very young sprigs, are the product of the original phellogen, which will grow to virgin cork, while the ensuing, the amadia corks, are traumatic, known as wound periderm, the product of the traumatic phellogens To fulfill their protective role, cork cells have ‘suberized’ cell walls rich in suberin, a biopolymer typical of this tissue (reviewed in Graça 2015). Several enzymes involved in suberin monomer biosynthesis, assembly and regulation have been described (reviewed in Vishwanath et al 2015)

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