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Published on January 15, 2004; 10.1104/pp.103.032011

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Received August 20, 2003
Returned for revision September 14, 2003
Accepted October 30, 2003

Topology of the Maize Mixed Linkage (1->3),(1->4)-{beta}-D-Glucan Synthase at the Golgi Membrane

Breeanna R. Urbanowicz , Catherine Rayon , and Nicholas C. Carpita *

Department of Botany and Plant Pathology, 915 West State Street, Purdue University, West Lafayette, Indiana 47907-2054

* Corresponding author; email: carpita{at}purdue.edu.

Mixed-linkage (1->3),(1->4)-{beta}-D-glucan is a plant cell wall polysaccharide composed of cellotriosyl and cellotetraosyl units, with decreasingly smaller amounts of cellopentosyl, cellohexosyl, and higher cellodextrin units, each connected by single (1->3)-{beta}-linkages. (1->3),(1->4)-{beta}-Glucan is synthesized in vitro with isolated maize (Zea mays) Golgi membranes and UDP-[14C]D-glucose. The (1->3),(1->4)-{beta}-glucan synthase is sensitive to proteinase K digestion, indicating that part of the catalytic domain is exposed to the cytoplasmic face of the Golgi membrane. The detergent {3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonic acid} (CHAPS) also lowers (1->3),(1->4)-{beta}-glucan synthase activity. In each instance, the treatments selectively inhibit formation of the cellotriosyl units, whereas synthesis of the cellotetraosyl units is essentially unaffected. Synthesis of the cellotriosyl units is recovered when a CHAPS-soluble factor is permitted to associate with Golgi membranes at synthesis-enhancing CHAPS concentrations but lost if the CHAPS-soluble fraction is replaced by fresh CHAPS buffer. In contrast to other known Golgi-associated synthases, (1->3),(1->4)-{beta}-glucan synthase behaves as a topologic equivalent of cellulose synthase, where the substrate UDP-glucose is consumed at the cytosolic side of the Golgi membrane, and the glucan product is extruded through the membrane into the lumen. We propose that a cellulose synthase-like core catalytic domain of the (1->3),(1->4)-{beta}-glucan synthase synthesizes cellotetraosyl units and higher even-numbered oligomeric units and that a separate glycosyl transferase, sensitive to proteinase digestion and detergent extraction, associates with it to add the glucosyl residues that complete the cellotriosyl and higher odd-numbered units, and this association is necessary to drive polymer elongation.




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