An Endosperm-Associated Cuticle Is Required for Arabidopsis Seed Viability, Dormancy and Early Control of Germination.

Julien De Giorgi,Luis Lopez-Molina,Urszula Piskurewicz,Christophe Bailly,Laurent Mène-Saffrané,Anne Utz-Pugin,Sylvain Loubery,Kirsten Bomblies

doi:10.1371/journal.pgen.1005708

Julien De Giorgi, Luis Lopez-Molina + Show 6 more

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https://doi.org/10.1371/journal.pgen.1005708

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Abstract

Cuticular layers and seeds are prominent plant adaptations to terrestrial life that appeared early and late during plant evolution, respectively. The cuticle is a waterproof film covering plant aerial organs preventing excessive water loss and protecting against biotic and abiotic stresses. Cutin, consisting of crosslinked fatty acid monomers, is the most abundant and studied cuticular component. Seeds are dry, metabolically inert structures promoting plant dispersal by keeping the plant embryo in an arrested protected state. In Arabidopsis thaliana seeds, the embryo is surrounded by a single cell endosperm layer itself surrounded by a seed coat layer, the testa. Whole genome analyses lead us to identify cutin biosynthesis genes as regulatory targets of the phytohormones gibberellins (GA) and abscisic acid (ABA) signaling pathways that control seed germination. Cutin-containing layers are present in seed coats of numerous species, including Arabidopsis, where they regulate permeability to outer compounds. However, the role of cutin in mature seed physiology and germination remains poorly understood. Here we identify in mature seeds a thick cuticular film covering the entire outer surface of the endosperm. This seed cuticle is defective in cutin-deficient bodyguard1 seeds, which is associated with alterations in endospermic permeability. Furthermore, mutants affected in cutin biosynthesis display low seed dormancy and viability levels, which correlates with higher levels of seed lipid oxidative stress. Upon seed imbibition cutin biosynthesis genes are essential to prevent endosperm cellular expansion and testa rupture in response to low GA synthesis. Taken together, our findings suggest that in the course of land plant evolution cuticular structures were co-opted to achieve key physiological seed properties.

Highlights

Plant ancestors were aquatic organisms and their colonization of terrestrial habitats is a major chapter in the history of plant evolution
As well, the “near-dead” embryo is able to germinate and turn into a fragile young seedling. The fragility of this transition is betrayed by the existence of control mechanisms that block germination in response to harmful environmental conditions
We show that mature seeds of the model plant Arabidopsis contain an earlier land plant evolutionary innovation: the cuticle, a waxy film covering the aerial parts of the plant preventing excessive transpiration

Summary

Introduction

Plant ancestors were aquatic organisms and their colonization of terrestrial habitats is a major chapter in the history of plant evolution. The cuticle is a hydrophobic film covering aerial plant structures that appeared prior to seeds during land plant evolution. It limits transpiration and gas exchanges with the environment, while protecting the plant against pathogens and insects [1,2,3]. Cutin is a major cuticle component consisting of C16 and C18 oxygenated fatty acid monomers crosslinked with one another forming a polymeric hydrophobic network [4]. The first steps of cutin biosynthesis involve transfer of acyl-CoA by long-chain acyl-CoA synthetase (LACS) to fatty acid monomers [5, 6]. The function of BDG1 remains unclear it may be involved in the polymerization of cutin monomers

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