A tale of two morphs: developmental patterns and mechanisms of seed coat differentiation in the dimorphic diaspore model Aethionema arabicum (Brassicaceae)

Abstract

The developmental transition from a fertilized ovule to a dispersed diaspore (seed or fruit) involves complex differentiation processes of the ovule's integuments leading to the diversity in mature seed coat structures in angiosperms. In this study, comparative imaging and transcriptome analysis were combined to investigate the morph-specific developmental differences during outer seed coat differentiation and mucilage production in Aethionema arabicum, the Brassicaceae model for diaspore dimorphism. One of the intriguing adaptations of this species is the production and dispersal of morphologically distinct, mucilaginous and non-mucilaginous diaspores from the same plant (dimorphism). The dehiscent fruit morph programme producing multiple mucilaginous seed diaspores was used as the default trait combination, similar to Arabidopsis thaliana, and was compared with the indehiscent fruit morph programme leading to non-mucilaginous diaspores. Synchrotron-based radiation X-ray tomographic microscopy revealed a co-ordinated framework of morph-specific early changes in internal anatomy of developing A. arabicum gynoecia including seed abortion in the indehiscent programme and mucilage production by the mucilaginous seed coat. The associated comparative analysis of the gene expression patterns revealed that the unique seed coat dimorphism of Ae. arabicum provides an excellent model system for comparative study of the control of epidermal cell differentiation and mucilage biosynthesis by the mucilage transcription factor cascade and their downstream cell wall and mucilage remodelling genes. Elucidating the underlying molecular framework of the dimorphic diaspore syndrome is key to understanding differential regulation of bet-hedging survival strategies in challenging environments, timely in the face of global climatic change.

Myxospermy Evolution in Brassicaceae: A Highly Complex and Diverse Trait with Arabidopsis as an Uncommon Model

“…Moreover, A. arabicum (27) and Diptychocarpus strictus (not phenotyped here) were shown to have seeds with dimorphism on myxospermy ability [40,43]. This highlights that seed mucilage can be easily disabled or activated during seed formation without any genetic change and could be rather explained by complex dimorphism-related gene expression [38]. However, we did not observe any correlation between the global expression profile of A. thaliana MSC toolbox gene orthologs and dimorphism (Figure 7; Table S10) [38].…”

“…However, 1, 21 and 17 A. thaliana MSC toolbox genes were conversely upregulated in non-myxospermous seeds at 0, 1 and 30 DAP, respectively [38]. Moreover, none of these upregulated MSC toolbox gene orthologs were ranked among the most differentially expressed genes [38]. Therefore, it could be speculated that the A. thaliana MSC toolbox genes are rather specific to the specific myxospermous sub-traits observed in A. thaliana, and that use of this toolbox to decipher the molecular actors of myxospermy in other species could be tricky.…”

“…While considering the significant fold change ratio, 1, 22 and 14 of 105 A. thaliana MSC toolbox genes were upregulated in myxospermous vs. non-myxospermous seeds at 0, 1 and 30 DAP, respectively. However, 1, 21 and 17 A. thaliana MSC toolbox genes were conversely upregulated in non-myxospermous seeds at 0, 1 and 30 DAP, respectively [38]. Moreover, none of these upregulated MSC toolbox gene orthologs were ranked among the most differentially expressed genes [38].…”

“…Despite their relatively weak expression profile, a slightly but significantly higher expression profile occurred in the myxospermous C. sativa as compared to the non-myxospermous B. napus. However, using the recent elegant transcriptomic data from the dimorphic A. arabicum seeds [38] (Figure 8, Table S10), the opposite trends occurred. The expression value of each A. thaliana MSC toolbox gene ortholog was summed for the whole seed development kinetics samples and were displayed in % of the similarly processed 10 most expressed genes in the whole genome for each species.…”

“…In such cases, only genes of the sub clade containing the A. thaliana MSC toolbox gene and delimited by the closest A. arabicum sequence, as it is the early divergent species of the studied Brassicaceaes species, were considered as orthologs. The whole seed development kinetic expression values were retrieved: for A. thaliana, 6 seed developmental stages [34], for C. sativa, 6 cumulated seed developmental stages [35,36], for B. napus, 4 seed developmental stages [37] and for A. arabicum, 3 developmental stages of myxospermous vs. non-myxospermous dimorphic diaspores [38]. For each gene in each species, the expression values of whole seed development kinetics samples were summed and ranked using Microsoft Excel.…”