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

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.

Genome wide association study of Arabidopsis seed mucilage layers at a regional scale

“…Fewer QTLs were found for the non-adherent mucilage than for the adherent mucilage, which is in agreement with the estimates of inter-population variance (13.8 % for non-adherent mucilage compared to 32.3 % for adherent mucilage). In A. thaliana, about one hundred genes have previously been characterized for their implication in seed mucilage biosynthesis and release (Viudes et al, 2021). Our GWA mapping approach allowed identifying 82 new candidate genes and only one belonging to the list of previously validated candidate genes.…”

“…In A. thaliana, around one hundred genes are participating to mucilage secretory cell formation and mucilage biosynthesis and release (Viudes et al, 2021). A large majority of these genes have been characterized through classical forward and reverse genetic studies.…”

Cell Wall Microdomains in the External Glands of Utricularia dichotoma Traps

“…Secondary cell walls are mostly formed in xylem cells (tracheary elements) or other cells for protection and structural support (fibers and other sclerenchymatous cells) [ 52 ]. However, a specific mucilaginous secondary cell wall is formed in the seed coat [ 53 , 54 , 55 , 56 ] of plant species, which use myxospermy [ 57 ]. Secondary cell walls differ from the primary cell wall not only in proportion of cellulose: hemicellulose: lignin but also (or primarily) in the chemical composition of hemicelluloses, and the presence of structural proteins.…”

Microtubule‐associated IQD9 orchestrates cellulose patterning in seed mucilage

“…The Arabidopsis research findings have been accompanied by advances in the mucilage structure of food crops such as Linum usitatissimum (flax; Viudes et al ., 2020) and Plantago ovata (psyllium; Cowley & Burton, 2021), which contain a higher proportion of nonpectic polymers. Despite the evolution of various mucilage traits within the family Brassicaceae (Viudes et al ., 2021), how MTs regulate the intricate organization of this specialized secondary cell wall has remained a relatively blank slate. The Arabidopsis genome encodes hundreds of putative MT‐associated proteins, but only MOR1 and TRM4 were previously shown to influence seed mucilage synthesis (McFarlane et al ., 2008; Hamada, 2014; Yang et al ., 2019).…”