The cutin polymer matrix undergoes a fine architectural tuning from early tomato fruit development to ripening

Abstract

The cuticle is a complex polymer matrix that protects all aerial organs of plants, fulfills multiple roles in plant-environment interactions, and is critical for plant development. These functions are associated with the structural features of cuticles, and the architectural modeling of cuticles during plant development is crucial for understanding their physical properties and biological functions. In this work, the in-depth architecture of the cutin polymer matrix during fruit development was investigated. Using cherry tomato fruit (Solanum lycopersicum) as a model from the beginning of the cell expansion phase to the red ripe stage, we designed an experimental scheme combining sample pre-treatment, Raman mapping, multivariate data analyses and biochemical analyses. These approaches revealed clear chemical areas with different contributions of cutin, polysaccharides and phenolics within the cutin polymer matrix. Besides, we demonstrated that these areas are finely tuned during fruit development, including compositional and macromolecular rearrangements. The specific spatio-temporal accumulation of phenolic compounds (p-coumaric acid and flavonoids) suggests that they fulfill distinct functions during fruit development. In addition, we highlighted an unexpected dynamic remodeling of the cutin-embedded polysaccharides pectin, cellulose and hemicellulose. Such structural tuning enables consistent adaption of the cutin-polysaccharide continuum and the functional performance of the fruit cuticle at the different developmental stages. This study provides insights into the plant cuticle architecture and in particular into the organization of the epidermal cell wall-cuticle.

Cuticle development and underlying transcriptome-metabolome associations during early seedling establishment

“…These analyses revealed cuticle compositional differences, and these are primarily determined by organ differentiation. Indeed, high resolution spectroscopic imaging of the cuticle has revealed architectural changes during cuticle development, associated with both the cuticular waxes and the cutin components (Jun et al, 2010; Reynoud et al, 2021; Reynoud et al, 2022). One of the limitations associated with understanding the functional consequences of these alterations of the plant cuticle is the lack of detailed structural information concerning this hydrophobic matrix.…”

Cuticle architecture and mechanical properties: a functional relationship delineated through correlated multimodal imaging

“…Flowers were tagged at anthesis and fruits at 10, 15, 20, 25, 30, 35 and 40 Days Post Anthesis (DPA) were harvested. Exocarp was collected at the equatorial part of the fruits, chemically fixed and impregnated in paraffin as previously described (Reynoud et al, 2022). Paraffin blocks were cut with an ultramicrotome (Leica EM UC7, Leica Microsystems SAS, Nanterre, France) equipped with diamond knifes (Histo and Ultra, Diatome, Nidau, Switzerland) to obtain 1µm-thick cross-sections.…”

“…Indeed, the plant cuticle is a biocomposite made of a complex supramolecular assembly of monomeric and polymeric lipids, polysaccharides and phenolics (Fernández et al ., 2016; Philippe et al ., 2020; Reynoud et al ., 2022). Cutin, the hydrophobic scaffold of cuticles is an insoluble polyester of oxygenated fatty acids (Hunneman & Eglinton, 1972; Bhanot et al ., 2021) whose polymerization index can vary during the plant development (Philippe et al ., 2016).…”

“…(Philippe et al ., 2020). Finally, phenolic compounds including esterified hydroxycinnamic acids (Riley & Kolattukudy, 1975; Graça & Lamosa, 2010) and free and bound flavonoids are also found in the cutin polyester (Hunt & Baker, 1980; Reynoud et al ., 2022). The composition and proportion of plant cuticle components vary during fruit growth and ripening (Domínguez et al ., 2008; España et al ., 2014b).…”

“…The composition and proportion of plant cuticle components vary during fruit growth and ripening (Domínguez et al ., 2008; España et al ., 2014b). Recently, fine chemical Raman mapping of the tomato fruit cuticle revealed the in-depth spatial heterogeneity of its components (lipids, polysaccharides, phenolics) (González Moreno et al ., 2022) including the cutin polymer matrix (Reynoud et al ., 2022). The additional observation of the fine architectural tuning of the corresponding chemical clusters along fruit development raise the question of their impact on the mechanical properties of the cuticle.…”