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

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.

Seed germination and dormancy: The classic story, new puzzles, and evolution

“…Since the testa is impermeable to toluidine blue, ABA‐treated WT and bdg1 seeds, both of which exhibit testa rupture, were used for this experiment. While toluidine blue did not reach the embryo of WT seeds efficiently, enhanced staining of the bdg1 embryos was observed, suggesting increased permeability of the bdg1 endosperm (De Giorgi et al ). PAC application (in the absence of ABA), which reduces GA levels in seeds, completely prevents testa rupture in WT seeds.…”

“…PAC application (in the absence of ABA), which reduces GA levels in seeds, completely prevents testa rupture in WT seeds. In contrast, approximately 50% of the bdg1 seeds are able to rupture the testa even in the presence of PAC (De Giorgi et al ). The bdg1 seeds exhibit enhanced expansion of the ME cells under the “low GA condition”, compared to WT, which could explain promotion of testa rupture in this mutant (De Giorgi et al ).…”

“…In contrast, approximately 50% of the bdg1 seeds are able to rupture the testa even in the presence of PAC (De Giorgi et al ). The bdg1 seeds exhibit enhanced expansion of the ME cells under the “low GA condition”, compared to WT, which could explain promotion of testa rupture in this mutant (De Giorgi et al ). These results suggest that the cutin coat, which is located at the outermost layer of the endosperm cell walls (Figure B) and serves as an endosperm coating, negatively affects seed germination through the suppression of ME expansion.…”

“…In fact, the bdg1 seeds are less dormant compared to WT, although this conclusion was not obtained from natural primary dormancy phenotypes but was drawn from the experiments using far red light‐induced (secondary) dormancy and the release from that state (De Giorgi et al ). The viability of the bdg1 seeds, which was assessed by accelerated aging tests, was lower than that of WT seeds (De Giorgi et al ), suggesting that advanced deterioration occurs in the bdg1 seeds due to increased oxidation. All of these data support the idea that the cutin layer in the Arabidopsis endosperm is a regulator of gas entry.…”

Identification and characterization of mRNAs of receptor-like kinases MhyGSO1 and MhyGSO2 in flowering parasitic plant Monotropa hypopitys

“…На сегодняшний день известны некоторые регуляторы механизма формирования кутикулы (Abe et al, 2003;Aharoni et al, 2004;Hooker et al, 2007;Moussu et al, 2013;De Giorgi et al, 2015;Fiume et al, 2016). Киназы LRR-RLK, RECEPTOR-LIKE PROTEIN KINASE 1 (RPK1) и TOADSTOOL 2 (TOAD2) поддерживают идентичность центрального домена протодермальных клеток во время эмбриогенеза (Nodine, Tax, 2008).…”