The metabolic environment of the developing embryo: A multidisciplinary approach on oilseed rapeseed

Hardy Rolletschek,Simon Mayer,Berin Boughton,Steffen Wagner,Stefan Ortleb,Christina Kiel,Ute Roessner,Ljudmilla Borisjuk

doi:10.1016/j.jplph.2021.153505

Abstract

Brassicaceae seeds consist of three genetically distinct structures: the embryo, endosperm and seed coat, all of which are involved in assimilate allocation during seed development. The complexity of their metabolic interrelations remains unresolved to date. In the present study, we apply state-of-the-art imaging and analytical approaches to assess the metabolic environment of the Brassica napus embryo. Nuclear magnetic resonance imaging (MRI) provided volumetric data on the living embryo and endosperm, revealing how the endosperm envelops the embryo, determining endosperm's priority in assimilate uptake from the seed coat during early development. MRI analysis showed higher levels of sugars in the peripheral endosperm facing the seed coat, but a lower sugar content within the central vacuole and the region surrounding the embryo. Feeding intact siliques with 13C-labeled sucrose allowed tracing of the post-phloem route of sucrose transfer within the seed at the heart stage of embryogenesis, by means of mass spectrometry imaging. Quantification of over 70 organic and inorganic compounds in the endosperm revealed shifts in their abundance over different stages of development, while sugars and potassium were the main determinants of osmolality throughout these stages. Our multidisciplinary approach allows access to the hidden aspects of endosperm metabolism, a task which remains unattainable for the small-seeded model plant Arabidopsis thaliana.

Highlights

Crops belonging to the Brassicaceae family, such as oilseed rape (Brassica napus), exhibit high phylogenetic similarity to the model plant Arabidopsis thaliana, on which extensive investigations have provided valuable information and molecular tools (Provart et al, 2016)
Our study provides in vivo evidences for the metabolic dominance of endosperm over the embryo during pre-storage phase of development in oilseed rapeseed
This phenomenon is likely predetermined by the origin of endosperm: “with an excess of maternal chromosomes over paternal ones, the mother can exert greater control over nutrient allocation to the progeny in relation to her own fitness” (Baroux et al, 2002)

Summary

Introduction

Crops belonging to the Brassicaceae family, such as oilseed rape (Brassica napus), exhibit high phylogenetic similarity to the model plant Arabidopsis thaliana, on which extensive investigations have provided valuable information and molecular tools (Provart et al, 2016). The developing seeds of both plants represent complex metabolic systems, involving at least a tripartite interaction among the testa (integuments or seed coat), endosperm and embryo. These three components form a system of autonomous, yet interacting organs, each regulated by their own genetic program (Lau et al, 2012). In A. thaliana and B. napus, rapid growth of the testa and endosperm at early development is critical in seed size determination (Garcia et al, 2005; Li and Berger, 2012; Lafon-Placette and Kohler, 2014; Ingram, 2020).

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