Suberin Biosynthesis, Assembly, and Regulation

Abstract

Suberin is a specialized cell wall modifying polymer comprising both phenolic-derived and fatty acid-derived monomers, which is deposited in below-ground dermal tissues (epidermis, endodermis, periderm) and above-ground periderm (i.e., bark). Suberized cells are largely impermeable to water and provide a critical protective layer preventing water loss and pathogen infection. The deposition of suberin is part of the skin maturation process of important tuber crops such as potato and can affect storage longevity. Historically, the term “suberin” has been used to describe a polyester of largely aliphatic monomers (fatty acids, ω-hydroxy fatty acids, α,ω-dioic acids, 1-alkanols), hydroxycinnamic acids, and glycerol. However, exhaustive alkaline hydrolysis, which removes esterified aliphatics and phenolics from suberized tissue, reveals a core poly(phenolic) macromolecule, the depolymerization of which yields phenolics not found in the aliphatic polyester. Time course analysis of suberin deposition, at both the transcriptional and metabolite levels, supports a temporal regulation of suberin deposition, with phenolics being polymerized into a poly(phenolic) domain in advance of the bulk of the poly(aliphatics) that characterize suberized cells. In the present review, we summarize the literature describing suberin monomer biosynthesis and speculate on aspects of suberin assembly. In addition, we highlight recent advances in our understanding of how suberization may be regulated, including at the phytohormone, transcription factor, and protein scaffold levels.

The making of suberin

“…Different tentative models for suberin macromolecular structure have been proposed in an effort to integrate the results obtained using NMR, suberin full and partial depolymerisation and TEM observations of suberin as alternating light/dark lamellae (Kolattukudy, 1980(Kolattukudy, , 2001Bernards, 2002;Grac ßa & Santos, 2007;Grac ßa, 2015). The most recent model is the one proposed by Grac ßa (2015), renamed as the 'integrated model' by Woolfson et al (2022). In this model, the aliphatic portion of the suberin polyester is mostly restricted to the light lamellae structured by glycerol-a,x-diacid-glycerol and also containing x-hydroxyacidglycerol units.…”

“…A different model has been proposed by Bernards (2002), named the ‘two‐domain model’ in Woolfson et al . (2022), especially with respect to the nature of the dark lamella. Whilst in Graça’s model the dark lamellae are made of lignin‐like polymers, in Bernards’ model they correspond to ferulic acid moieties forming part of the polyester.…”

Chemical and Molecular Characterization of Wound-Induced Suberization in Poplar (Populus alba × P. tremula) Stem Bark

“…Day 28 samples contained 1 mol% HCA, 9 mol% FA, 34 mol% α,ω-DCA, and 56 mol% ω-OHFA which are nearly identical to the 3:10:33:54 mol% breakdown observed for HCAs, FAs, α,ω-DCAs, and ω-OHFAs, respectively, in the native periderm controls (Figure 2c inset). Native periderm samples released a total monomer load of 20.00 ± 1.18 mg g DW −1 , whereas wound-healing suberin amounts were on average approximately 3%, 5%, and 10% of that for early (0-4), intermediate (5)(6)(7)(8)(9), and late (10-14) days, respectively. At 28 days post wounding, likely representing a fully healed periderm, the amount of suberin was only approximately 40% of the native periderm.…”

“…All trees were inflicted with 30 wounds, avoiding overlapping of wounds on the trunk of the tree (i.e., only one wound in any given vertical or horizontal line). The same 7 mm borer was used to remove the wound-healing tissue samples from each tree, sampled to a depth of the xylem at the initial wound site, at 0 (control), 1,2,3,4,5,6,7,8,9,10,11,12,13,14, and 28 days after wounding. Samples of three biological replicates for RNA extraction and chemical analyses were immediately placed in liquid nitrogen after harvesting and subsequently stored at −80 • C until use.…”

“…Suberin is a solvent-intractable heteropolymer found on the inner face of the primary cell wall. Current models describe it as an aliphatic polyester of glycerol and fatty acid derivatives that is crosslinked to polyphenolics and associated with solvent-extractable waxes [3][4][5][6]. It is proposed that the organized deposition of these domains produces the characteristic lamellar pattern observed under transmission electron microscopy (TEM [7]).…”