Abstract

Cuticles are specialized cell wall structures that form at the surface of terrestrial plant organs. They are largely comprised lipidic compounds and are deposited in the apoplast, external to the polysaccharide-rich primary wall, creating a barrier to diffusion of water and solutes, as well as to environmental factors. The predominant cuticle component is cutin, a polyester that is assembled as a complex matrix, within and on the surface of which aliphatic and aromatic wax molecules accumulate, further modifying its properties. To reach the point of cuticle assembly the different acyl lipid-containing components are first exported from the cell across the plasma membrane and then traffic across the polysaccharide wall. The export of cutin precursors and waxes from the cell is known to involve plasma membrane-localized ATP-binding cassette (ABC) transporters; however, other secretion mechanisms may also contribute. Indeed, extracellular vesiculo-tubular structures have recently been reported in Arabidopsis thaliana (Arabidopsis) to be associated with the deposition of suberin, a polyester that is structurally closely related to cutin. Intriguingly, similar membranous structures have been observed in leaves and petals of Arabidopsis, although in lower numbers, but no close association with cutin formation has been identified. The possibility of multiple export mechanisms for cuticular components acting in parallel will be discussed, together with proposals for how cuticle precursors may traverse the polysaccharide cell wall before their assimilation into the cuticle macromolecular architecture.

Highlights

  • A lipidic, hydrophobic cuticle is deposited on the nascent epidermal surface of the entire embryo (Ingram and Nawrath, 2017; Berhin et al, 2019), where it forms an intimate association with the underlying hydrated polysaccharide cell wall

  • In addition to wild-type (WT) Arabidopsis, we examined several mutants that have a reduction in cutin abundance due to distinct changes in cutin precursor formation or a deficiency in ABCG32 expression (Bessire et al, 2011; Mazurek et al, 2017)

  • Given the large amounts of material needed to assemble the thick cuticles of some organs, such as tomato and pepper fruit cuticles (>1 mg/cm−2 cutin monomers; Figure 1A; Graça et al, 2002), we suggest that the movement of cuticular lipids across the apoplast is more likely to be a passive process that avoids investment in metabolically expensive transport proteins (Fich et al, 2016; Philippe et al, 2020b)

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Summary

INTRODUCTION

A lipidic, hydrophobic cuticle is deposited on the nascent epidermal surface of the entire embryo (Ingram and Nawrath, 2017; Berhin et al, 2019), where it forms an intimate association with the underlying hydrated polysaccharide cell wall. Investment in metabolically expensive transport proteins (Fich et al, 2016; Philippe et al, 2020b) Such a mechanism would involve the diffusion of amphiphilic cutin precursors and hydrophobic waxes in the hydrophilic environment of the cell wall as a physicochemical phase-separation process. An important factor in this regard may be that suberin has a relatively high phenolic content, which could affect the mobility of its precursors and promote physical associations with lignin, a phenolic polymer that is deposited in cell secondary walls close to the PM (Philippe et al, 2020b) Another feature that may influence the sites of cutinization or suberization is the potential involvement of multiple classes of proteins associated with their coordinated secretion at the PM. Fundamental questions remain regarding the relationship between composition, architecture and assembly, and the molecular and physicochemical basis for the organization of the cuticle and the cell wall-cuticle continuum is still essentially a blank canvas

MATERIALS AND METHODS
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