Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes

J Biol Chem. 2006 Sep 29;281(39):29321-9. doi: 10.1074/jbc.M605903200. Epub 2006 Jul 14.

Abstract

Plant cell walls are degraded by glycoside hydrolases that often contain noncatalytic carbohydrate-binding modules (CBMs), which potentiate degradation. There are currently 11 sequence-based cellulose-directed CBM families; however, the biological significance of the structural diversity displayed by these protein modules is uncertain. Here we interrogate the capacity of eight cellulose-binding CBMs to bind to cell walls. These modules target crystalline cellulose (type A) and are located in families 1, 2a, 3a, and 10 (CBM1, CBM2a, CBM3a, and CBM10, respectively); internal regions of amorphous cellulose (type B; CBM4-1, CBM17, CBM28); and the ends of cellulose chains (type C; CBM9-2). Type A CBMs bound particularly effectively to secondary cell walls, although they also recognized primary cell walls. Type A CBM2a and CBM10, derived from the same enzyme, displayed differential binding to cell walls depending upon cell type, tissue, and taxon of origin. Type B CBMs and the type C CBM displayed much weaker binding to cell walls than type A CBMs. CBM17 bound more extensively to cell walls than CBM4-1, even though these type B modules display similar binding to amorphous cellulose in vitro. The thickened primary cell walls of celery collenchyma showed significant binding by some type B modules, indicating that in these walls the cellulose chains do not form highly ordered crystalline structures. Pectate lyase treatment of sections resulted in an increased binding of cellulose-directed CBMs, demonstrating that decloaking cellulose microfibrils of pectic polymers can increase CBM access. The differential recognition of cell walls of diverse origin provides a biological rationale for the diversity of cellulose-directed CBMs that occur in cell wall hydrolases and conversely reveals the variety of cellulose microstructures in primary and secondary cell walls.

MeSH terms

  • Arabidopsis / metabolism
  • Carbohydrate Metabolism
  • Carbohydrates / chemistry*
  • Cell Wall / metabolism*
  • Cellulose / chemistry*
  • Fluorescent Antibody Technique, Indirect
  • Models, Biological
  • Models, Molecular
  • Plant Proteins / chemistry
  • Polysaccharide-Lyases / chemistry
  • Protein Binding
  • Protein Conformation
  • Protein Folding

Substances

  • Carbohydrates
  • Plant Proteins
  • Cellulose
  • Polysaccharide-Lyases
  • pectate lyase