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Complex carbohydrate found to regulate plant growth

Twenty-five years ago, Alan Darvill and colleagues described one of the most complex carbohydrates found in nature. Called rhamnogalacturan II or RG-II, it is found in plant cell walls.

The carbohydrate is found in all higher plants and it requires a host of different proteins to manufacture. Yet for more than two decades, scientists haven't had a clue about its function.

"In a sense, we've been on a quest to understand what it's doing in plants ever since we discovered it," said Darvill, professor of biochemistry and co-director of UGA's Complex Carbohydrate Research Center.

With a lot of hard work, the efforts of dozens of scientists around the world, and a bit of luck, that quest has come to an end.

In an article published in today's issue of Science, CCRC scientists present evidence that normal plant growth depends on how RG-II is organized in cell walls.

"RG-II has been known as an obscure, structurally weird polysaccharide that plants make," said Malcolm O'Neill, senior research associate at UGA's CCRC. "But we had no idea why plants went to all the effort to make it. There are 50 to 60 enzymes involved, 12 different sugars and 22 different linkages. There's even one sugar that's actually not been found anywhere else."

The work of O'Neill, Darvill, Stefan Eberhard and Peter Albersheim shows that normal plant growth depends on the ability of RG-II strands to cross-link with boron and form a network in the cell wall matrix. Boron cross-links RG-II strands together in a fishnet-like structure that holds other components in the cell wall in place.

"You can think of the cell wall as a bit like reinforced concrete," O'Neill said. "Tiny cellulose fibers are the steel rods and the matrix is the concrete. Only in the cell wall, the concrete has the consistency of jello."

One clue to RG-II's role emerged when O'Neill found that a dwarf mutant of Arabidopsis - a relative of cabbage and mustard - had normal amounts of RG-II in its cell walls but only half of the RG-II was cross-linked by boron.

"Without that cross-linking, the cell walls apparently don't have the strength to expand normally and the plant is dwarfed," he said.

Since the Arabidopsis mutant was known to lack the enzyme that makes the sugar L-fucose, O'Neill said he suspected that RG-II in the mutant would be deficient in fucose. RG-II is made of about 30 sugars arranged in a chain with four sidechains and L-fucose is found on two of the sidechains. O'Neill found that the mutant's RG-II not only lacked fucose, but also substituted a different sugar in its place.

He also discovered that when mutants received fertilizer containing L-fucose, plant growth was normal. That's because the plants contained normal amounts of fucose and RG-II molecules occurred as the boron cross-linked form.

"The sugar substitution changes the shape of the molecule," Darvill said. "As in all molecules - and in all biology - it's the shapes of molecules that control their function."

In a normal plant, boron binds to RG-II and forms a bridge that holds everything together. In the mutant, a little bit of the structure of the RGII has been changed and because of the change in shape, it can't hold the boron quite as well, Darvill said. Fertilizing mutants with high levels of boron also reversed dwarfing because the high amount of available boron effectively forced RG-II to cross-link.

"It almost makes this carbohydrate analogous to proteins, where activity depends on their shapes," Darvill said. "Here's a carbohydrate that has a shape that has an activity." This work shows answers to both the role of boron and RG-II in plants, Darvill said.

"The boron is stuck between two molecules and holds them together," he said. "If you don't allow that to happen, then you don't get normal plant growth."

University of Georgia. August 2001.

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