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

Plant Physiol. 2016 May;171(1):165-78. doi: 10.1104/pp.16.00211. Epub 2016 Mar 15.

Abstract

Arabidopsis (Arabidopsis thaliana) seed coat epidermal cells produce large amounts of mucilage that is released upon imbibition. This mucilage is structured into two domains: an outer diffuse layer that can be easily removed by agitation and an inner layer that remains attached to the outer seed coat. Both layers are composed primarily of pectic rhamnogalacturonan I (RG-I), the inner layer also containing rays of cellulose that extend from the top of each columella. Perturbation in cellulosic ray formation has systematically been associated with a redistribution of pectic mucilage from the inner to the outer layer, in agreement with cellulose-pectin interactions, the nature of which remained unknown. Here, by analyzing the outer layer composition of a series of mutant alleles, a tight proportionality of xylose, galacturonic acid, and rhamnose was evidenced, except for mucilage modified5-1 (mum5-1; a mutant showing a redistribution of mucilage pectin from the inner adherent layer to the outer soluble one), for which the rhamnose-xylose ratio was increased drastically. Biochemical and in vitro binding assay data demonstrated that xylan chains are attached to RG-I chains and mediate the adsorption of mucilage to cellulose microfibrils. mum5-1 mucilage exhibited very weak adsorption to cellulose. MUM5 was identified as a putative xylosyl transferase recently characterized as MUCI21. Together, these findings suggest that the binding affinity of xylose ramifications on RG-I to a cellulose scaffold is one of the factors involved in the formation of the adherent mucilage layer.

MeSH terms

  • Arabidopsis / enzymology
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Wall / chemistry
  • Cell Wall / metabolism*
  • Cellulose / metabolism
  • Cluster Analysis
  • Gene Expression Regulation, Plant*
  • Genes, Plant
  • Genetic Linkage
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Hexuronic Acids / metabolism
  • Mutation
  • Pectins / chemistry
  • Pectins / metabolism
  • Plant Extracts / chemistry
  • Plant Mucilage / chemistry
  • Plant Mucilage / genetics*
  • Plant Mucilage / metabolism*
  • Rhamnose / metabolism
  • Seeds / enzymology
  • Seeds / metabolism*
  • Sequence Analysis, DNA
  • Staining and Labeling
  • Xylans / chemistry
  • Xylans / metabolism*
  • Xylose / metabolism

Substances

  • Arabidopsis Proteins
  • Hexuronic Acids
  • Plant Extracts
  • Plant Mucilage
  • Xylans
  • rhamnogalacturonan I
  • galacturonic acid
  • Pectins
  • Cellulose
  • Xylose
  • CESA5 protein, Arabidopsis
  • Glucosyltransferases
  • Rhamnose