AR242-PP56-04 ARI 28 March 2005 15:47Starch DegradationAlison M. Smith,1Samuel C. Zeeman,2and Steven M. Smith3,41Department of Metabolic Biology, John Innes Centre, Norwich NR4 7UH,United Kingdom; email: [email protected] of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland;email: [email protected] of Cell and Molecular Biology, University of Edinburgh, Edinburgh EH9 3JH,United Kingdom; email: [email protected] of Biomedical, Biomolecular, and Chemical Sciences, University of WesternAustralia, Crawley, WA 6009 Australia; email: [email protected]. Rev. Plant Biol.2005. 56:73–98doi: 10.1146/annurev.arplant.56.032604.144257Copyrightc 2005 byAnnual Reviews. All rightsreservedFirst published online as aReview in Advance onJanuary 13, 20051543-5008/05/0602-0073$20.00Key Wordsamylase, Arabidopsis, cereal endosperm, chloroplast, maltoseAbstractRecent research reveals that starch degradation in Arabidopsis leaves atnight is significantly different from the “textbook” version of this pro-cess. Although parts of the pathway are now understood, other partsremain to be discovered. Glucans derived from starch granules are hy-drolyzed via β-amylase to maltose, which is exported from the chloro-plast. In the cytosol maltose is the substrate for a transglucosylationreaction, producing glucose and a glucosylated acceptor molecule. Theenzyme that attacks the starch granule to release glucans is not known,nor is the nature of the cytosolic acceptor molecule. An Arabidopsis-typepathway may operate in leaves of other species, and in nonphotosyn-thetic organs that accumulate starch transiently. However, in starch-storing organs such as cereal endosperms and legume seeds, the processdiffers from that in Arabidopsis and may more closely resemble the text-book pathway. We discuss the differences in relation to the biology ofeach system.73Annu. Rev. Plant. Biol. 2005.56:73-98. Downloaded from arjournals.annualreviews.orgby University of Georgia on 04/04/06. For personal use only.AR242-PP56-04 ARI 28 March 2005 15:47ContentsINTRODUCTION .................. 74THE PATHWAY OF STARCHDEGRADATION INARABIDOPSIS LEAVES ........... 74The Attack on the Granule Surface . 75The Importance of StarchPhosphorylating Enzymes ....... 77Debranching ...................... 77Metabolism of Soluble, LinearGlucans ........................ 78Fate of Maltose and Maltotriose . . . . 79The Metabolism of Maltose in theCytosol......................... 79Further Characterization of thePathway ........................ 80CONTROL OF FLUX THROUGHTHE PATHWAY INARABIDOPSIS LEAVES ........... 81Regulation at the Level of GeneExpression...................... 81Regulation of Enzyme Activity. . . . . . 82THE PATHWAY IN LEAVESOF OTHER SPECIES ............ 84The Production of Soluble, LinearGlucans ........................ 84Hydrolytic versus PhosphorolyticDegradation .................... 85Maltose Metabolism ............... 85THE PATHWAY IN OTHER PLANTORGANS ......................... 86The Attack on the Granulein Storage Organs............... 86Degradation of Soluble Glucansin Storage Organs............... 89The Pathway in Vegetative Tissues . 90CONCLUSION ..................... 90INTRODUCTIONOur aim in this article is to discuss new infor-mation about the pathway of starch degrada-tion in Arabidopsis leaves at night, and to use itto reassess our understanding of starch degra-dation in other plant organs. Although starchdegradation has been extensively studied in ger-minating cereal endosperm (8, 29, 76), the na-ture and regulation of the process in this andother plant organs is poorly understood. Thereis good a priori reason to think that the pro-cess in endosperms differs from that in otherorgans because the mature endosperm is not aliving tissue whereas starch degradation in allother plant organs occurs within living cells.Biochemical analyses show that many plant or-gans possess a wealth of isoforms of several dif-ferent types of enzymes capable of degradingstarch and related glucans. However, discover-ing the roles and importance of each of theseforms in catalyzing starch degradation in vivohas been hampered by a lack of tools for thispurpose. In the last five years, the genetic andgenomic resources available in Arabidopsis havefacilitated new approaches to the pathway inleaves. We present below the picture that hasemerged for Arabidopsis leaves, then discuss towhat extent this is applicable to leaves of otherspecies, and to other plant organs.THE PATHWAY OF STARCHDEGRADATION IN ARABIDOPSISLEAVESDuring the day, starch and sucrose are synthe-sized together as the products of photosyntheticcarbon assimilation in Arabidopsis leaves. Su-crose is exported to nonphotosynthetic parts ofthe plant, and starch accumulates in the chloro-plasts. The ratio of starch-to-sucrose synthe-sis varies with environmental conditions, but inour “standard” growth conditions (12 h light,20◦C, and about 180-µmol quanta of photosyn-thetically active radiation m−2s−1) about half ofthe newly assimilated carbon is partitioned intostarch, and the content at the end of the day is10–15-mg g−1fresh weight (14, 117). Duringthe subsequent night, the starch is degraded toprovide substrates for sucrose synthesis to allowcontinued export to nonphotosynthetic parts ofthe plant, and to provide carbon skeletons, en-ergy, and reductant within the leaf cell. Thesupply of carbohydrate provided by nighttimestarch degradation is essential for the normal74 Smith·Zeeman·SmithAnnu. Rev. Plant. Biol. 2005.56:73-98. Downloaded from arjournals.annualreviews.orgby University of Georgia on 04/04/06. For personal use only.AR242-PP56-04 ARI 28 March 2005 15:47Figure 1Proposed pathway of starch degradation in Arabidopsis leaves at night. Steps about which uncertainty remainsare represented as stippled or dashed arrows, and with question marks. GWD is glucan, water dikinase andPWD is phosphoglucan, water dikinase. Further details of the enzymes and reactions involved are in Table 1.growth of the plant. Mutants that synthesizeless starch during the day, or have a reducedcapacity to degrade it at night, have reducedgrowth rates under many environmental con-ditions (13, 85). In the following sections wediscuss the steps involved in converting granu-lar starch in the chloroplast into hexose phos-phate in the cytosol. The scheme we describeis presented in Figure 1, and further details onthe proteins involved are in