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

Sébastien Viudes,Vincent Burlat,Christophe Dunand

doi:10.3390/cells10092470

Abstract

The ability to extrude mucilage upon seed imbibition (myxospermy) occurs in several Angiosperm taxonomic groups, but its ancestral nature or evolutionary convergence origin remains misunderstood. We investigated seed mucilage evolution in the Brassicaceae family with comparison to the knowledge accumulated in Arabidopsis thaliana. The myxospermy occurrence was evaluated in 27 Brassicaceae species. Phenotyping included mucilage secretory cell morphology and topochemistry to highlight subtle myxospermy traits. In parallel, computational biology was driven on the one hundred genes constituting the so-called A. thaliana mucilage secretory cell toolbox to confront their sequence conservation to the observed phenotypes. Mucilage secretory cells show high morphology diversity; the three studied Arabidopsis species had a specific extrusion modality compared to the other studied Brassicaceae species. Orthologous genes from the A. thaliana mucilage secretory cell toolbox were mostly found in all studied species without correlation with the occurrence of myxospermy or even more sub-cellular traits. Seed mucilage may be an ancestral feature of the Brassicaceae family. It consists of highly diverse subtle traits, probably underlined by several genes not yet characterized in A. thaliana or by species-specific genes. Therefore, A. thaliana is probably not a sufficient reference for future myxospermy evo–devo studies.

Highlights

During land plant evolution, secondary growth and seeds were major innovations leading to the impressive species radiation currently observed in spermatophytes [1]
Myxospermy was found in all studied lineages, and importantly, in the two Aethionema species belonging to the early divergent group
The thickest mucilage secretory cells (MSCs) belong to the two myxospermous mustards, and the non-myxospermous species show variable epidermal cell thickness, up to the thinnest and widest cells observed in R. sativum (18)

Summary

Introduction

Secondary growth and seeds were major innovations leading to the impressive species radiation currently observed in spermatophytes (seed plants) [1]. In Arabidopsis thaliana, five outer cell layers undergo specialization during seed development, to be dehydrated and form a compacted seed coat in the mature dry seed. In this dead tissue, the two main layers are the inner integument enriched in pigments and the outer integument accumulating polysaccharides [4]. A. thaliana SM represents 3% of seed dry mass and is mainly composed of sparsely branched rhamnogalacturonan I (RG-I) pectins [6,12] This composition allows the use of ruthenium red to assess SM occurrence, and immunocytolabeling with cell-wall-specific probes for more accurate SM phenotyping [13,14]. One third of them are involved in the transcriptional regulatory pathway, half are direct actors of mucilage synthesis, secretion, modification and structure, and the remaining part regroups genes implicated in cell wall dynamics and hormone synthesis and perception (Table S1) [7]

Objectives

Methods

Results

Conclusion