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

Author:

Reynoud Nicolas1ORCID,Geneix Nathalie1ORCID,Petit Johann2ORCID,D’Orlando Angelina13ORCID,Fanuel Mathieu13ORCID,Marion Didier1ORCID,Rothan Christophe2ORCID,Lahaye Marc1ORCID,Bakan Bénédicte1ORCID

Affiliation:

1. INRAE, Unité Biopolymères, Interactions, Assemblages, BP71627 44316, Nantes Cedex3 , France

2. INRAE, Univ. Bordeaux, UMR BFP , F-33140, Villenave d’Ornon, France

3. INRAE PROBE research infrastructure, BIBS Facility , F- 44300, Nantes, France

Abstract

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 pretreatment, 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 spatiotemporal 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.

Funder

Region Pays de la Loire and INRAE – TRANSFORM Department

ANR (Agence Nationale de la Recherche) grant COPLAnAR

Publisher

Oxford University Press (OUP)

Subject

Plant Science,Genetics,Physiology

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