The Arabidopsis mature endosperm promotes seedling cuticle formation via release of sulfated peptides

Kay Gully,Mayumi Iwasaki,Anne Utz-Pugin,Sylvain Loubéry,Christiane Nawrath,Christelle Fuchs,Fiamma Paolo Longoni,Satoshi Fujita,Luis Lopez-Molina,Patrice Waridel,Urszula Piskurewicz,Laurent Mène-Saffrané,Julien De Giorgi,Woohyun Kim

doi:10.1016/j.devcel.2021.10.005

Kay Gully, Mayumi Iwasaki + Show 12 more

Open Access

https://doi.org/10.1016/j.devcel.2021.10.005

Copy DOI

Abstract

In Arabidopsis mature seeds, the onset of the embryo-to-seedling transition is nonautonomously controlled, being blocked by endospermic abscisic acid (ABA) release under unfavorable conditions. Whether the mature endosperm governs additional nonautonomous developmental processes during this transition is unknown. Mature embryos have a more permeable cuticle than seedlings, consistent with their endospermic ABA uptake capability. Seedlings acquire their well-sealing cuticles adapted to aerial lifestyle during germination. Endosperm removal prevents seedling cuticle formation, and seed reconstitution by endosperm grafting onto embryos shows that the endosperm promotes seedling cuticle development. Grafting different endosperm and embryo mutant combinations, together with biochemical, microscopy, and mass spectrometry approaches, reveal that the release of tyrosylprotein sulfotransferase (TPST)-sulfated CIF2 and PSY1 peptides from the endosperm promotes seedling cuticle development. Endosperm-deprived embryos produced nonviable seedlings bearing numerous developmental defects, not related to embryo malnutrition, all restored by exogenously provided endosperm. Hence, seedling establishment is nonautonomous, requiring the mature endosperm.

Highlights

Mature seeds are metabolically inert and highly resistant structures favoring plant dispersal (Baroux and Grossniklaus, 2019)
The mature seed of the Brassicaceae Arabidopsis thaliana consists of an outer dead seed coat arising from ovular integuments, underneath which a single layer of mature endosperm live cells surround the mature embryo
The seedling cuticle is formed during the embryo-toseedling transition We explored the formation of the seedling cuticle, including the mechanism leading to its strong sealing properties required for its aerial life upon emergence from the seed

Summary

Introduction

Mature seeds are metabolically inert and highly resistant structures favoring plant dispersal (Baroux and Grossniklaus, 2019). In non-persistent endosperm species, the endosperm may be absent from mature seeds, as in the orchid family, or be present as a minor component, as in the economically important Brassicaceae or Fabaceae families, which mainly store food in the embryo (Baroux and Grossniklaus, 2019). The latter case raises the question of the biological function of the endosperm in mature seeds of non-persistent endosperm species. The mature seed of the Brassicaceae Arabidopsis thaliana consists of an outer dead seed coat (testa) arising from ovular integuments, underneath which a single layer of mature endosperm live cells surround the mature embryo

Methods

Results

Discussion

Conclusion