Abstract
Terrestrialization of vascular plants, i.e., Angiosperm, is associated with the development of cuticular barriers that prevent biotic and abiotic stresses and support plant growth and development. To fulfill these multiple functions, cuticles have developed a unique supramolecular and dynamic assembly of molecules and macromolecules. Plant cuticles are not only an assembly of lipid compounds, i.e., waxes and cutin polyester, as generally presented in the literature, but also of polysaccharides and phenolic compounds, each fulfilling a role dependent on the presence of the others. This mini-review is focused on recent developments and hypotheses on cuticle architecture–function relationships through the prism of non-lipid components, i.e., cuticle-embedded polysaccharides and polyester-bound phenolics.
Highlights
Terrestrial colonization of plants came along with the development of four sophisticated hydrophobic macromolecular assemblies, i.e., cuticle, suberin, lignin and sporopollenin (Yeats and Rose, 2013; Graça, 2015; Li et al, 2019; Ralph et al, 2019), which enabled plants to resist to the harsh conditions of the environment, to stiffen their architecture, to ensure nutrient and water adsorption, their reproduction and land dispersion
Plant cuticles are composed of three main types of chemical components, i.e., lipids, carbohydrates, and phenolics
It is interesting to note that major cuticle-associated transcription factors, e.g., SHINE or MIXTA regulate coordinately the synthesis of polysaccharides, cutin monomer, wax and phenolics, and epidermal patterning (Shi et al, 2011; Lashbrooke et al, 2016). This fine regulation comes along with a dynamic of the cuticle architecture needed for and occurring during organ growth. This is well illustrated with the recent observation of a cutin: cutin transacylase activity capable of rearranging the architecture of the cutin polyester by a cut and paste mechanism during the growth of plant epidermis (Xin and Fry, 2021), similar to the xyloglucan endotransglucosylase/hydrolase (XTH) for polysaccharides remodeling during organ growth (Rose et al, 2002) or to the suberin polymerization-degradation process catalyzed by clusters of enzymes from the GDSL-family of esterase/lipase during lateral root formation (Ursache et al, 2021)
Summary
Terrestrial colonization of plants came along with the development of four sophisticated hydrophobic macromolecular assemblies, i.e., cuticle, suberin, lignin and sporopollenin (Yeats and Rose, 2013; Graça, 2015; Li et al, 2019; Ralph et al, 2019), which enabled plants to resist to the harsh conditions of the environment, to stiffen their architecture, to ensure nutrient and water adsorption, their reproduction and land dispersion. E.g., in the control of water and gas exchanges, in the defense signaling against biotic and abiotic stresses, in plant development with many interactions with hormone signaling and cell wall biosynthesis, in the protection against UV radiation, in the retention of environmental pollutants, in the induction of responses to mechanical stimuli, and constitute an habitat for the plant microbiome (Schönherr and Riederer, 1989; Martin and Rose, 2014; Meder et al, 2018; Cordovez et al, 2019) These multiple functions impact crop yields and quality, including post-harvest quality and processing which has boosted research on the structure, assembly, and biosynthesis of their macromolecular and molecular constituents. Plant Cuticle Architecture–Function Relationships ensuing hypotheses on its architecture, its evolution during organ development and its relationship with their functional properties
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