Biomechanical properties of the tomato (Solanum lycopersicum) fruit cuticle during development are modulated by changes in the relative amounts of its components

Abstract

Summary In this study, growth‐dependent changes in the mechanical properties of the tomato (Solanum lycopersicum) cuticle during fruit development were investigated in two cultivars with different patterns of cuticle growth and accumulation. The mechanical properties were determined in uniaxial tensile tests using strips of isolated cuticles. Changes in the functional groups of the cuticle chemical components were analysed by attenuated total reflectance–Fourier transform infrared (ATR‐FTIR). The early stages of fruit growth are characterized by an elastic cuticle, and viscoelastic behaviour only appeared at the beginning of cell enlargement. Changes in the cutin:polysaccharide ratio during development affected the strength required to achieve viscoelastic deformation. The increase in stiffness and decrease in extensibility during ripening, related to flavonoid accumulation, were accompanied by an increase in cutin depolymerization as a result of a reduction in the overall number of ester bonds. Quantitative changes in cuticle components influence the elastic/viscoelastic behaviour of the cuticle. The cutin:polysaccharide ratio modulates the stress required to permanently deform the cuticle and allow cell enlargement. Flavonoids stiffen the elastic phase and reduce permanent viscoelastic deformation. Ripening is accompanied by a chemical cleavage of cutin ester bonds. An infrared (IR) band related to phenolic accumulation can be used to monitor changes in the cutin esterification index.

CHSsilencing suggests a negative cross-talk between wax and flavonoid pathways in tomato fruit cuticle

“…Ripening has been shown to cause a reduction in the number of ester bonds in the cutin matrix. 2 This reduction was shown to be associated with flavonoid incorporation to the cuticle and not ripening since the pink sectors ripened but had a higher number of ester bonds than the red sectors. Clearly, flavonoids seem to affect the expression of several genes involved in the last stages of cuticle deposition and/or remodeling.…”

“…In tomato, phenolics accumulated in the fruit cuticle vary with the developmental stage, being the main compounds coumaric and benzoic acid during fruit growth and flavonoids such as naringenin chalcone and naringenin flavanone during ripening. 2 Incorporation of flavonoids was postulated to modify the cuticle's mechanical properties by increasing its resistance to deformation. 3 Thus, during the period of organ expansion, the cuticle can be deformed with little stress applied.…”

“…Cuticles of the pink regions were significantly different from those of the red sectors but also from the mature green stage already reported in the literature. 2,4 In tomato, flavonoids are synthetized during fruit development 7,8 and most of them are assumed to accumulate in the vacuole.…”

“…3 Thus, during the period of organ expansion, the cuticle can be deformed with little stress applied. 2 CHALCONE SYNTHASE (CHS) is the enzyme responsible for the synthesis of chalconaringenin, the flavonoid mainly accumulated in tomato fruit cuticle and responsible for its orange-yellow color. Flavonoids are being shown to interact with several metabolic pathways sometimes by altering hormone levels.…”

“…As such, they have been shown to modify the physical properties of the cuticle, especially the biomechanics. 2,13 Waxes are complex mixtures of very long chain aliphatic molecules (aldehydes, alcohols, fatty acids, alkanes) and cyclic compounds (sterols, triterpenoids) 14 which are the product of different metabolic pathways. 15 Our results indicate a negative interaction between the flavonoid and wax pathways; however, it remains to be determined which type or types of waxes are modified.…”