Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms

Samuel C. Zeeman A B , Thierry Delatte A , Gaëlle Messerli A , Martin Umhang A , Michaela Stettler A , Tabea Mettler A , Sebastian Streb A , Heike Reinhold A and Oliver Kötting A
+ Author Affiliations
- Author Affiliations

A Institute of Plant Sciences, ETH Zurich, Universitätstrasse 2, CH-8092 Zurich, Switzerland.

B Corresponding author. Email: szeeman@ethz.ch

C This paper originates from a presentation at the 8th International Congress of Plant Molecular Biology, Adelaide, Australia, August 2006.

Functional Plant Biology 34(6) 465-473 https://doi.org/10.1071/FP06313
Submitted: 28 November 2006  Accepted: 7 February 2007   Published: 1 June 2007

Abstract

The aim of this article is to provide an overview of current models of starch breakdown in leaves. We summarise the results of our recent work focusing on Arabidopsis, relating them to other work in the field. Early biochemical studies of starch containing tissues identified numerous enzymes capable of participating in starch degradation. In the non-living endosperms of germinated cereal seeds, starch breakdown proceeds by the combined actions of α-amylase, limit dextrinase (debranching enzyme), β-amylase and α-glucosidase. The activities of these enzymes and the regulation of some of the respective genes on germination have been extensively studied. In living plant cells, additional enzymes are present, such as α-glucan phosphorylase and disproportionating enzyme, and the major pathway of starch breakdown appears to differ from that in the cereal endosperm in some important aspects. For example, reverse-genetic studies of Arabidopsis show that α-amylase and limit-dextrinase play minor roles and are dispensable for starch breakdown in leaves. Current data also casts doubt on the involvement of α-glucosidase. In contrast, several lines of evidence point towards a major role for β-amylase in leaves, which functions together with disproportionating enzyme and isoamylase (debranching enzyme) to produce maltose and glucose. Furthermore, the characterisation of Arabidopsis mutants with elevated leaf starch has contributed to the discovery of previously unknown proteins and metabolic steps in the pathway. In particular, it is now apparent that glucan phosphorylation is required for normal rates of starch mobilisation to occur, although a detailed understanding of this step is still lacking. We use this review to give a background to some of the classical genetic mutants that have contributed to our current knowledge.

Additional keywords: amylase, amylopectin, Arabidopsis thaliana L., carbohydrate metabolism, cereal endosperm, metabolic regulation.


Acknowledgements

We offer particular thanks to our close collaborators, Professor Alison M. Smith and Professor Steven M. Smith, and to our colleagues in the Arabidopsis Starch Metabolism Network (www.starchmetnet.org, accessed 17 March 2007). We also thank Martine Trevisan and Simona Eicke for excellent technical support, past and present, in our laboratory. Our research is funded by the Roche Research Foundation, the Swiss National Science Foundation (Nation Centre for Competence in Research – Plant Survival and Grant 3100–067312.01/1), and the EMBO Young Investigator Programme.


References


Asatsuma S, Sawada C, Itoh K, Okito M, Kitajima A, Mitsui T (2005) Involvement of α-amylase I-1 in starch degradation in rice chloroplasts. Plant & Cell Physiology 46, 858–869.
CrossRef | PubMed | open url image1

Baunsgaard L, Lütken H, Mikkelsen R, Glaring MA, Pham TT, Blennow A (2005) A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated α-glucans and is involved in starch degradation in Arabidopsis. The Plant Journal 41, 595–605.
CrossRef | PubMed | open url image1

Buléon A, Colonna P, Planchot V, Ball S (1998) Starch granules: structure and biosynthesis. International Journal of Biological Macromolecules 23, 85–112.
CrossRef | PubMed | open url image1

Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiology 79, 11–17.
PubMed |
open url image1

Caspar T, Lin T-P, Kakefuda G, Benbow L, Preiss J, Somerville C (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiology 95, 1181–1188.
PubMed |
open url image1

Chapman GW, Pallas JE, Mendicino J (1972) The hydrolysis of maltodextrins by a β-amylase isolated from leaves of Vicia faba. Biochimica et Biophysica Acta 276, 491–507.
CrossRef | PubMed | open url image1

Chatterton NJ, Silvius JE (1980) Photosynthate partitioning into leaf starch as affected by daily photosynthetic period duration in 6 species. Physiologia Plantarum 49, 141–144.
CrossRef | open url image1

Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. The Plant Journal 37, 853–863.
CrossRef | PubMed | open url image1

Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM (2001) A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. The Plant Journal 26, 89–100.
CrossRef | PubMed | open url image1

Delatte T, Umhang M, Trevisan M, Eicke S, Thorneycroft D, Smith SM, Zeeman SC (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. The Journal of Biological Chemistry 281, 12 050–12 059.
CrossRef | open url image1

Fettke J, Eckermann N, Tiessen A, Geigenberger P, Steup M (2005a) Identification, subcellular localization and biochemical characterization of water-soluble heteroglycans (SHG) in leaves of Arabidopsis thaliana L.: distinct SHG reside in the cytosol and in the apoplast. The Plant Journal 43, 568–585.
CrossRef | PubMed | open url image1

Fettke J, Poeste S, Eckermann N, Tiessen A, Pauly M, Geigenberger P, Steup M (2005b) Analysis of cytosolic heteroglycans from leaves of transgenic potato (Solanum tuberosum L.) plants that under- or overexpress the Pho 2 phosphorylase isozyme. Plant & Cell Physiology 46, 1987–2004.
CrossRef | PubMed | open url image1

Fettke J, Chia T, Eckermann N, Smith A, Steup M (2006) A transglucosidase necessary for starch degradation and maltose metabolism in leaves at night acts on cytosolic heteroglycans (SHG). The Plant Journal 46, 668–684.
CrossRef | PubMed | open url image1

Fettke J, Eckermann N, Kötting O, Ritte G, Steup M (2007) Novel starch-related enzymes and carbohydrates. Cellular and Molecular Biology 52, OL883–OL904. open url image1

Fincher GB (1989) Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annual Review of Plant Physiology and Plant Molecular Biology 40, 305–346.
CrossRef | open url image1

Fordham-Skelton AP, Chilley P, Lumbreras V, Reignoux S, Fenton TR, Dahm CC, Pages M, Gatehouse JA (2002) A novel higher plant protein tyrosine phosphatase interacts with SNF1-related protein kinases via a KIS (kinase interaction sequence) domain. The Plant Journal 29, 705–715.
CrossRef | PubMed | open url image1

Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. The Plant Journal 39, 847–862.
CrossRef | PubMed | open url image1

Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a MYB gene in barley aleurone cells – evidence for MYB transactivation of a high-pI α-amylase gene promoter. The Plant Cell 7, 1879–1891.
CrossRef | PubMed | open url image1

Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen JV (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. The Plant Journal 17, 1–9.
CrossRef | PubMed | open url image1

Hussain H, Mant A, Seale R, Zeeman SC, Hinchliffe E , et al. (2003) Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. The Plant Cell 15, 133–149.
CrossRef | PubMed | open url image1

Jones G, Whelan WJ (1969) The action pattern of D-enzyme, a transmaltodextrinylase from potato. Carbohydrate Research 9, 483–490.
CrossRef | open url image1

Kaplan F, Guy CL (2005) RNA interference of Arabidopsis β-amylase 8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. The Plant Journal 44, 730–743.
CrossRef | PubMed | open url image1

Kerk D, Conley TR, Rodriguez FA, Tran HT, Nimick M, Muench DG, Moorhead GBG (2006) A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. The Plant Journal 46, 400–413.
CrossRef | PubMed | open url image1

Kötting O, Pusch K, Tiessen A, Geigenberger P, Steup M, Ritte G (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiology 137, 242–252.
CrossRef | PubMed | open url image1

Lin T-P, Preiss J (1988) Characterisation of D-enzyme (4-α-glucanotransferase) in Arabidopsis leaf. Plant Physiology 86, 260–265.
PubMed |
open url image1

Lloyd JR, Blennow A, Burhenne K, Kossmann J (2004) Repression of a novel isoform of disproportionating enzyme (stDPE2) in potato leads to inhibition of starch degradation in leaves but not tubers stored at low temperature. Plant Physiology 134, 1347–1354.
CrossRef | PubMed | open url image1

Lorberth R, Ritte G, Willmitzer L, Kossmann J (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nature Biotechnology 16, 473–477.
CrossRef | PubMed | open url image1

Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218, 466–473.
CrossRef | PubMed | open url image1

Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiology 138, 2280–2291.
CrossRef | PubMed | open url image1

Lu Y, Sharkey TD (2006) The importance of maltose in transitory starch breakdown. Plant, Cell & Environment 29, 353–366.
CrossRef | PubMed | open url image1

Lu Y, Steichen JM, Yao J, Sharkey TD (2006a) The role of cytosolic α-glucan phosphorylase in maltose metabolism and the comparison of amylomaltase in Arabidopsis and Escherichia coli. Plant Physiology 142, 878–889.
CrossRef | PubMed | open url image1

Lu Y, Steichen JM, Weise SE, Sharkey TD (2006b) Cellular and organ level localization of maltose in maltose-excess Arabidopsis mutants. Planta 224, 935–943.
CrossRef | PubMed | open url image1

Mikkelsen R, Mutenda KE, Mant A, Schürmann P, Blennow A (2005) α-Glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proceedings of the National Academy of Sciences USA 102, 1785–1790.
CrossRef | open url image1

Nielsen TH, Wischmann B, Enevoldsen K, Møller BL (1994) Starch phosphorylation in potato tubers proceeds concurrently with de novo biosynthesis of starch. Plant Physiology 105, 111–117.
PubMed |
open url image1

Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303, 87–89.
CrossRef | PubMed | open url image1

Niittylä T, Comparot-Moss S, Lue W-L, Messerli G, Trevisan M , et al. (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. Journal of Biological Chemistry 281, 11 815–11 818.
CrossRef | open url image1

Ritte G, Lorberth R, Steup M (2000) Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. The Plant Journal 21, 387–391.
CrossRef | PubMed | open url image1

Ritte G, Scharf A, Eckermann N, Haebel S, Steup M (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiology 135, 2068–2077.
CrossRef | PubMed | open url image1

Ritte G, Heydenreich M, Mahlow S, Haebel S, Kötting O, Steup M (2006) Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Letters 580, 4872–4876.
CrossRef | PubMed | open url image1

Schäfer G, Heber U, Heldt HW (1977) Glucose transport into spinach chloroplasts. Plant Physiology 60, 286–289.
PubMed |
open url image1

Scheidig A, Fröhlich A, Schulze S, Lloyd JR, Kossmann J (2002) Down regulation of a chloroplast-targeted β-amylase leads to a starch-excess phenotype in leaves. The Plant Journal 30, 581–591.
CrossRef | PubMed | open url image1

Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annual Review of Plant Biology 56, 73–98.
CrossRef | PubMed | open url image1

Sokolov LN, Dominguez-Solis JR, Allary A-L, Buchanan BB, Luan S (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proceedings of the National Academy of Sciences USA 103, 9732–9737.
CrossRef | open url image1

Sonnewald U, Basner A, Greve B, Steup M (1995) A second L-type isozyme of potato glucan phosphorylase: cloning, antisense inhibition and expression analysis. Plant Molecular Biology 27, 567–576.
CrossRef | PubMed | open url image1

Stanley D, Fitzgerald AM, Farnden KJF, McRae EA (2002) Characterization of putative amylases from apple (Malus domestica) and Arabidopsis thaliana. Biologia Supp 57, 137–148. open url image1

Trethewey RN, ap Rees T (1994a) A mutant of Arabidopsis thaliana lacking the ability to transport glucose across the chloroplast envelope. The Biochemical Journal 301, 449–454.
PubMed |
open url image1

Trethewey RN, ap Rees T (1994b) The role of the hexose transporter in the chloroplasts of Arabidopsis thaliana L. Planta 195, 168–174.
CrossRef | open url image1

Wattebled F, Dong Y, Dumez S, Delvallé D, Planchot R , et al. (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiology 138, 184–195.
CrossRef | PubMed | open url image1

Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, Hebbeker U, Flügge U-I (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. The Plant Cell 12, 787–801.
CrossRef | PubMed | open url image1

Weise SE, Weber APM, Sharkey TD (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218, 474–482.
CrossRef | PubMed | open url image1

Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD (2006) Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiology 141, 879–886.
CrossRef | PubMed | open url image1

Worby CA, Gentry MS, Dixon JE (2006) Laforin: a dual specificity phosphatase that dephosphorylates complex carbohydrates. Journal of Biological Chemistry 281, 30 412–30 418.
CrossRef | open url image1

Yu T-S, Kofler H, Häusler RE, Hille D, Flügge U-I , et al. (2001) SEX1 is a general regulator of starch degradation in plants and not the chloroplast hexose transporter. The Plant Cell 13, 1907–1918.
CrossRef | PubMed | open url image1

Yu T-S, Zeeman SC, Thorneycroft D, Fulton DC, Dunstan H , et al. (2005) α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. Journal of Biological Chemistry 280, 9773–9779.
CrossRef | PubMed | open url image1

Zeeman SC, Northrop F, Smith AM, ap Rees T (1998) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolyzing enzyme. The Plant Journal 15, 357–365.
CrossRef | PubMed | open url image1

Zeeman SC, ap Rees T (1999) Changes in carbohydrate metabolism and assimilate partitioning in starch-excess mutants of Arabidopsis. Plant, Cell & Environment 22, 1445–1453.
CrossRef | open url image1

Zeeman SC, Pilling E, Tiessen A, Kato L, Donald AM, Smith AM (2002) Starch synthesis in Arabidopsis; granule synthesis, composition and structure. Plant Physiology 129, 516–529.
CrossRef | PubMed | open url image1

Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004) The role of plastidial α-glucan phosphorylase in starch degradation and tolerance of abiotic stress in Arabidopsis leaves. Plant Physiology 135, 849–858.
CrossRef | PubMed | open url image1

Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. The Biochemical Journal 401, 13–28.
CrossRef | PubMed | open url image1








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