MUCILAGE-RELATED10 Produces Galactoglucomannan That Maintains Pectin and Cellulose Architecture in Arabidopsis Seed Mucilage

Abstract

Plants invest a lot of their resources into the production of an extracellular matrix built of polysaccharides. While the composition of the cell wall is relatively well characterized, the functions of the individual polymers and the enzymes that catalyze their biosynthesis remain poorly understood. We exploited the Arabidopsis (Arabidopsis thaliana) seed coat epidermis (SCE) to study cell wall synthesis. SCE cells produce mucilage, a specialized secondary wall that is rich in pectin, at a precise stage of development. A coexpression search for MUCILAGE-RELATED (MUCI) genes identified MUCI10 as a key determinant of mucilage properties. MUCI10 is closely related to a fenugreek (Trigonella foenumgraecum) enzyme that has in vitro galactomannan a-1,6-galactosyltransferase activity. Our detailed analysis of the muci10 mutants demonstrates that mucilage contains highly branched galactoglucomannan (GGM) rather than unbranched glucomannan. MUCI10 likely decorates glucomannan, synthesized by CELLULOSE SYNTHASE-LIKE A2, with galactose residues in vivo. The degree of galactosylation is essential for the synthesis of the GGM backbone, the structure of cellulose, mucilage density, as well as the adherence of pectin. We propose that GGM scaffolds control mucilage architecture along with cellulosic rays and show that Arabidopsis SCE cells represent an excellent model in which to study the synthesis and function of GGM. Arabidopsis natural varieties with defects similar to muci10 mutants may reveal additional genes involved in GGM synthesis. Since GGM is the most abundant hemicellulose in the secondary walls of gymnosperms, understanding its biosynthesis may facilitate improvements in the production of valuable commodities from softwoods.

Xylans Provide the Structural Driving Force for Mucilage Adhesion to the Arabidopsis Seed Coat

“…Despite their low abundance, these components could play essential roles in controlling mucilage properties (Voiniciuc et al, 2015c). For example, glucomannans and galactoglucomannans synthesized by CSLA2 and MUCI10 seem to be involved in structuring the adherent layer of mucilage (Yu et al, 2014;Voiniciuc et al, 2015b). Determining how these different polymers are involved in RG-I attachment to cellulose is challenging, and it is unclear which are part of the mucilage itself or originate from fragments of primary cell wall released when the epidermal cells rupture on imbibition.…”

“…Therefore, in addition to Xyl branching of RG-I, other pectin modifications also would appear to influence adherence, and these remain to be characterized. Glucomannans and galactoglucomannans can interact with cellulose and appear to participate in the organization and crystallization of mucilage cellulose (Yu et al, 2014;Voiniciuc et al, 2015b). csla2 and muci10 mutants affected in glucomannan and galactoglucomannan synthesis have more densely packed adherent layer polymers, with a small repartitioning of RG-I to the outer mucilage layer.…”

“…csla2 and muci10 mutants affected in glucomannan and galactoglucomannan synthesis have more densely packed adherent layer polymers, with a small repartitioning of RG-I to the outer mucilage layer. Voiniciuc et al (2015b) proposed that galactoglucomannan serves as a scaffold around the cellulosic rays that control mucilage density. This would involve interactions between galactoglucomannan and cellulose and, probably, other mucilage polymers.…”

Monitoring Polysaccharide Dynamics in the Plant Cell Wall

“…The dynamics of mannan have yet to be explored in great detail, although new insights into their structural roles were gained in recent years (Yu et al, 2014;Voiniciuc et al, 2015a). Some mAb probes are available (e.g.…”

Highly Branched Xylan Made by IRX14 and MUCI21 Links Mucilage to Arabidopsis Seeds

“…Recently, heteromannan produced by CELLULOSE SYNTHASE-LIKE A2 (Yu et al, 2014) and MUCILAGE-RELATED10 (MUCI10; Voiniciuc et al, 2015a) was shown to control the density of polysaccharides in the mucilage capsule. Using a coexpression and sequencebased strategy, we predicted that MUCI10 (GT34 member) is a mucilage biosynthetic gene.…”