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J. Biol. Chem., Vol. 281, Issue 17, 12050-12059, April 28, 2006

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Evidence for Distinct Mechanisms of Starch Granule Breakdown in Plants^*

Thierry Delatte, Martin Umhang, Martine Trevisan, Simona Eicke, David Thorneycroft^¶, Steven M. Smith^¶1, and Samuel C. Zeeman²

From the Institute of Plant Sciences, ETH Zurich, CH-8092 Zurich, Switzerland, the Institute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland, and the ^¶Institute of Cell and Molecular Biology, University of Edinburgh, Edinburgh EH9 3JH, Scotland, United Kingdom

The aim of this work was to understand the initial steps of starch breakdown inside chloroplasts. In the non-living endosperm of germinating cereal grains, starch breakdown is initiated by -amylase secreted from surrounding cells. However, loss of -amylase from Arabidopsis does not prevent chloroplastic starch breakdown (Yu, T.-S., Zeeman, S. C., Thorneycroft, D., Fulton, D. C., Dunstan, H., Lue, W.-L., Hegemann, B., Tung, S.-Y., Umemoto, T., Chapple, A., Tsai, D.-L., Wang, S.-M, Smith, A. M., Chen, J., and Smith, S. M. (2005) J. Biol. Chem. 280, 9773-9779), implying that other enzymes must attack the starch granule. Here, we present evidence that the debranching enzyme isoamylase 3 (ISA3) acts at the surface of the starch granule. Atisa3 mutants have more leaf starch and a slower rate of starch breakdown than wild-type plants. The amylopectin of Atisa3 contains many very short branches and ISA3-GFP localizes to granule-like structures inside chloroplasts. We suggest that ISA3 removes short branches from the granule surface. To understand how some starch is still degraded in Atisa3 mutants we eliminated a second debranching enzyme, limit dextrinase (pullulanase-type). Atlda mutants are indistinguishable from the wild type. However, the Atisa3/Atlda double mutant has a more severe starch-excess phenotype and a slower rate of starch breakdown than Atisa3 single mutants. The double mutant accumulates soluble branched oligosaccharides (limit dextrins) that are undetectable in the wild-type and the single mutants. Together these results suggest that glucan debranching occurs primarily at the granule surface via ISA3, but in its absence soluble branched glucans are debranched in the stroma via limit dextrinase. Consistent with this model, chloroplastic -amylase AtAMY3, which could release soluble branched glucans, is induced in Atisa3 and in the Atisa3/Atlda double mutant.

Received for publication, December 22, 2005 , and in revised form, February 14, 2006.

^* The work was supported by Swiss National Science Foundation Grant 3100-067312.01/1. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ Present address: ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Western Australia 6009, Australia.

² To whom correspondence should be addressed. Tel.: 41-44-632-8275; Fax: 41-44-632-1044; E-mail: szeeman{at}ethz.ch.

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