Carbohydrate-binding Modules Promote the Enzymatic Deconstruction of Intact Plant Cell Walls by Targeting and Proximity Effects

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2010 Aug 11

PMID 20696902

Citations 125

Authors

Cecile Herve

Artur Rogowski

Anthony W Blake

Susan E Marcus

Harry J Gilbert

J Paul Knox

Affiliations

Soon will be listed here.

Abstract

Cell wall degrading enzymes have a complex molecular architecture consisting of catalytic modules and noncatalytic carbohydrate-binding modules (CBMs). The function of CBMs in cell wall degrading processes is poorly understood. Here, we have evaluated the potential enzyme-targeting function of CBMs in the context of intact primary and secondary cell wall deconstruction. The capacity of a pectate lyase to degrade pectic homogalacturonan in primary cell walls was potentiated by cellulose-directed CBMs but not by xylan-directed CBMs. Conversely, the arabinofuranosidase-mediated removal of side chains from arabinoxylan in xylan-rich and cellulose-poor wheat grain endosperm cell walls was enhanced by a xylan-binding CBM but less so by a crystalline cellulose-specific module. The capacity of xylanases to degrade xylan in secondary cell walls was potentiated by both xylan- and cellulose-directed CBMs. These studies demonstrate that CBMs can potentiate the action of a cognate catalytic module toward polysaccharides in intact cell walls through the recognition of nonsubstrate polysaccharides. The targeting actions of CBMs therefore have strong proximity effects within cell wall structures, explaining why cellulose-directed CBMs are appended to many noncellulase cell wall hydrolases.

Citing Articles

Genome-Wide Identification and Analysis of Carbohydrate-Binding Modules in .

Wang Y, Huang Q, Chen X, Li H, Chang J, Zhang Y Int J Mol Sci. 2025; 26(3).

PMID: 39940689 PMC: 11817085. DOI: 10.3390/ijms26030919.

Isolation of a Novel Low-Temperature-Active and Organic-Solvent-Stable Mannanase from the Intestinal Metagenome of .

Kim D, Lee C, Lee Y, Yoon S, Kim S Int J Mol Sci. 2025; 26(1.

PMID: 39796082 PMC: 11720594. DOI: 10.3390/ijms26010216.

Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms.

Gasser M, Liu A, Altamia M, Brensinger B, Brewer S, Flatau R Microb Biotechnol. 2024; 17(12):e70064.

PMID: 39659293 PMC: 11632262. DOI: 10.1111/1751-7915.70064.

A modular enzyme with combined hemicellulose-removing and LPMO activity increases cellulose accessibility in softwood.

Forsberg Z, Tuveng T, Eijsink V FEBS J. 2024; 292(1):75-93.

PMID: 39190632 PMC: 11705215. DOI: 10.1111/febs.17250.

Acidothermus cellulolyticus E1 endoglucanase expressed in planta undergoes extensive hydroxyproline-O-glycosylation and exhibits enhanced impact on biomass digestibility.

Fang H, Dickey B, PerezLaguna D, Ulloa J, PerezSanchez P, Xu J Plant Cell Rep. 2024; 43(8):202.

PMID: 39073636 PMC: 11488174. DOI: 10.1007/s00299-024-03291-y.

References

Brown I, Mallen M, Charnock S, Davies G, Black G . Pectate lyase 10A from Pseudomonas cellulosa is a modular enzyme containing a family 2a carbohydrate-binding module. Biochem J. 2001; 355(Pt 1):155-65. PMC: 1221723. DOI: 10.1042/0264-6021:3550155. View

McCartney L, Blake A, Flint J, Bolam D, Boraston A, Gilbert H . Differential recognition of plant cell walls by microbial xylan-specific carbohydrate-binding modules. Proc Natl Acad Sci U S A. 2006; 103(12):4765-70. PMC: 1450244. DOI: 10.1073/pnas.0508887103. View

Din N, Damude H, Gilkes N, Miller Jr R, Warren R, Kilburn D . C1-Cx revisited: intramolecular synergism in a cellulase. Proc Natl Acad Sci U S A. 1994; 91(24):11383-7. PMC: 45235. DOI: 10.1073/pnas.91.24.11383. View

Guillen D, Sanchez S, Rodriguez-Sanoja R . Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol. 2009; 85(5):1241-9. DOI: 10.1007/s00253-009-2331-y. View

Herve C, Rogowski A, Gilbert H, Knox J . Enzymatic treatments reveal differential capacities for xylan recognition and degradation in primary and secondary plant cell walls. Plant J. 2009; 58(3):413-22. DOI: 10.1111/j.1365-313X.2009.03785.x. View

Kellett L, Poole D, Ferreira L, Durrant A, Hazlewood G, Gilbert H . Xylanase B and an arabinofuranosidase from Pseudomonas fluorescens subsp. cellulosa contain identical cellulose-binding domains and are encoded by adjacent genes. Biochem J. 1990; 272(2):369-76. PMC: 1149709. DOI: 10.1042/bj2720369. View

Hashimoto H . Recent structural studies of carbohydrate-binding modules. Cell Mol Life Sci. 2006; 63(24):2954-67. PMC: 11136102. DOI: 10.1007/s00018-006-6195-3. View

Knox J . Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol. 2008; 11(3):308-13. DOI: 10.1016/j.pbi.2008.03.001. View

Black G, Rixon J, Clarke J, Hazlewood G, Theodorou M, Morris P . Evidence that linker sequences and cellulose-binding domains enhance the activity of hemicellulases against complex substrates. Biochem J. 1996; 319 ( Pt 2):515-20. PMC: 1217798. DOI: 10.1042/bj3190515. View

10.

Marcus S, Verhertbruggen Y, Herve C, Ordaz-Ortiz J, Farkas V, Pedersen H . Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol. 2008; 8:60. PMC: 2409341. DOI: 10.1186/1471-2229-8-60. View

11.

Gilbert H, Hazlewood G, Laurie J, Orpin C, Xue G . Homologous catalytic domains in a rumen fungal xylanase: evidence for gene duplication and prokaryotic origin. Mol Microbiol. 1992; 6(15):2065-72. DOI: 10.1111/j.1365-2958.1992.tb01379.x. View

12.

Montanier C, Lammerts van Bueren A, Dumon C, Flint J, Correia M, Prates J . Evidence that family 35 carbohydrate binding modules display conserved specificity but divergent function. Proc Natl Acad Sci U S A. 2009; 106(9):3065-70. PMC: 2651348. DOI: 10.1073/pnas.0808972106. View

13.

Urbanowicz B, Catala C, Irwin D, Wilson D, Ripoll D, Rose J . A tomato endo-beta-1,4-glucanase, SlCel9C1, represents a distinct subclass with a new family of carbohydrate binding modules (CBM49). J Biol Chem. 2007; 282(16):12066-74. DOI: 10.1074/jbc.M607925200. View

14.

Ordaz-Ortiz J, Marcus S, Knox J . Cell wall microstructure analysis implicates hemicellulose polysaccharides in cell adhesion in tomato fruit pericarp parenchyma. Mol Plant. 2009; 2(5):910-21. DOI: 10.1093/mp/ssp049. View

15.

Pell G, Taylor E, Gloster T, Turkenburg J, Fontes C, Ferreira L . The mechanisms by which family 10 glycoside hydrolases bind decorated substrates. J Biol Chem. 2003; 279(10):9597-605. DOI: 10.1074/jbc.M312278200. View

16.

Pell G, Szabo L, Charnock S, Xie H, Gloster T, Davies G . Structural and biochemical analysis of Cellvibrio japonicus xylanase 10C: how variation in substrate-binding cleft influences the catalytic profile of family GH-10 xylanases. J Biol Chem. 2003; 279(12):11777-88. DOI: 10.1074/jbc.M311947200. View

17.

Bolam D, Ciruela A, Simpson P, Williamson M, Rixon J, Boraston A . Pseudomonas cellulose-binding domains mediate their effects by increasing enzyme substrate proximity. Biochem J. 1998; 331 ( Pt 3):775-81. PMC: 1219417. DOI: 10.1042/bj3310775. View

18.

Poole D, Morag E, Lamed R, Bayer E, Hazlewood G, Gilbert H . Identification of the cellulose-binding domain of the cellulosome subunit S1 from Clostridium thermocellum YS. FEMS Microbiol Lett. 1992; 78(2-3):181-6. DOI: 10.1016/0378-1097(92)90022-g. View

19.

Cantarel B, Coutinho P, Rancurel C, Bernard T, Lombard V, Henrissat B . The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2008; 37(Database issue):D233-8. PMC: 2686590. DOI: 10.1093/nar/gkn663. View

20.

Beylot M, McKie V, Voragen A, Gilbert H . The Pseudomonas cellulosa glycoside hydrolase family 51 arabinofuranosidase exhibits wide substrate specificity. Biochem J. 2001; 358(Pt 3):607-14. PMC: 1222095. DOI: 10.1042/0264-6021:3580607. View