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Hetero-trans-β-Glucanase Produces Cellulose-Xyloglucan Covalent Bonds in the Cell Walls of Structural Plant Tissues and Is Stimulated by Expansin

Authors :
Martina Pičmanová
Lenka Franková
Andrew Hudson
Stephen C. Fry
Jia Wooi Loh
Klaus Herburger
Christopher E. French
Marcos Valenzuela-Ortega
Frank Meulewaeter
Source :
Molecular Plant
Publication Year :
2020

Abstract

Current cell-wall models assume no covalent bonding between cellulose and hemicelluloses such as xyloglucan or mixed-linkage β-d-glucan (MLG). However, Equisetum hetero-trans-β-glucanase (HTG) grafts cellulose onto xyloglucan oligosaccharides (XGOs) – and, we now show, xyloglucan polysaccharide – in vitro, thus exhibiting CXE (cellulose:xyloglucan endotransglucosylase) activity. In addition, HTG also catalyzes MLG-to-XGO bonding (MXE activity). In this study, we explored the CXE action of HTG in native plant cell walls and tested whether expansin exposes cellulose to HTG by disrupting hydrogen bonds. To quantify and visualize CXE and MXE action, we assayed the sequential release of HTG products from cell walls pre-labeled with substrate mimics. We demonstrated covalent cellulose–xyloglucan bonding in plant cell walls and showed that CXE and MXE action was up to 15% and 60% of total transglucanase action, respectively, and peaked in aging, strengthening tissues: CXE in xylem and cells bordering intercellular canals and MXE in sclerenchyma. Recombinant bacterial expansin (EXLX1) strongly augmented CXE activity in vitro. CXE and MXE action in living Equisetum structural tissues potentially strengthens stems, while expansin might augment the HTG-catalyzed CXE reaction, thereby allowing efficient CXE action in muro. Our methods will enable surveys for comparable reactions throughout the plant kingdom. Furthermore, engineering similar hetero-polymer formation into angiosperm crop plants may improve certain agronomic traits such as lodging tolerance.<br />Studying a hetero-transglucanase showed that cellulose and mixed-linkage glucan can be covalently linked to the hemicellulose xyloglucan in native plant cell walls. These reactions increase with tissue age and predominate in structural tissues and in cells surrounding cavities, suggesting a role in tissue strengthening. Expansin strongly augments cellulose hetero-transglucosylation but has no effect on mixed-linkage glucan.

Details

ISSN :
17529867
Volume :
13
Issue :
7
Database :
OpenAIRE
Journal :
Molecular plant
Accession number :
edsair.doi.dedup.....95c717638017bf85d6cb9b1cf87bdcd0