Abstract
α-1,4-linked glucan chains branched through α-1,6 glucosidic lineages define the most frequently found storage polysaccharides in living cells. These glucans come in two very distinct forms known as glycogen and starch. The small water-soluble glycogen particles distribute widely in Archaea, Bacteria, and heterotrophic eukaryotes, while semicrystalline solid starch seems to be restricted to photosynthetic eukaryotes. This review focusses on the so-called glycosyl-nucleotide-dependent pathway of starch and glycogen synthesis. Through comparative biochemistry of storage polysaccharide metabolism in distinct clades, we will review the evidence sustaining that starch has evolved from preexisting glycogen metabolism several times during the evolution of photosynthetic eukaryotes and cyanobacteria. This review will also describe the possible function of storage polysaccharide metabolism in establishing metabolic symbiosis during plastid endosymbiosis. We will detail the evidence sustaining that storage polysaccharide metabolism was used by three distinct organisms to establish a tripartite symbiosis that facilitated metabolic integration of free-living cyanobacteria into evolving organelles.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Albrecht T, Haebel S, Koch A et al (2004) Yeast glycogenin (Glg2p) produced in Escherichia coli is simultaneously glucosylated at two vicinal tyrosine residues but results in a reduced bacterial glycogen accumulation. Eur J Biochem 271:3978–3989
Alonso-Casajus N, Dauvillee D, Viale AM et al (2006) Glycogen phosphorylase, the product of the glgP Gene, catalyzes glycogen breakdown by removing glucose units from the nonreducing ends in Escherichia coli. J Bacteriol 188:5266–5272
Archibald JM, Lane CE (2009) Going, going, not quite gone: nucleomorphs as a case study in nuclear genome reduction. J Hered 100:582–590
Arias MC, Danchin EG, Coutinho P et al (2012) Eukaryote to gut bacteria transfer of a glycoside hydrolase gene essential for starch breakdown in plants. Mob Genet Elem 2:81–87
Badger MR, Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622
Ball S (1998) Regulation of starch biosynthesis. Kluwer Academic Publishers, Dordrecht
Ball S (2002) The intricate pathway of starch biosynthesis and degradation in the monocellular alga Chlamydomonas reinhardtii. Aust J Chem 55:1–11
Ball S, Deschamps P (2008) Starch metabolism. In: Stem DB (ed) The chlamydomonas sourcebook: 2. Organellar and metabolic processes. Academic, London, pp 1–40
Ball S, Guan HP, James M et al (1996) From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell 86:349–352
Ball S, Colleoni C, Cenci U et al (2011) The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 62:1775–1801
Ball SG, Subtil A, Bhattacharya D et al (2013) Metabolic effectors secreted by bacterial pathogens: essential facilitators of plastid endosymbiosis? Plant Cell 25:7–21
Bandyopadhyay A, Elvitigala T, Liberton M et al (2013) Variations in the rhythms of respiration and nitrogen fixation in members of the unicellular diazotrophic cyanobacterial genus Cyanothece. Plant Physiol 161:1334–1346
Bäumer D, Preisfeld A, Ruppel HG (2001) Isolation and characterization of paramylon synthase from Euglena gracilis (Euglenophyceae). J Phycol 37:38–46
Baurain D, Brinkmann H, Petersen J et al (2010) Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol Biol Evol 27:1698–1709
Becker B, Hoef-Emden K, Melkonian M (2008) Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes. BMC Evol Biol 8:203
Beller M, Thiel K, Thul P et al (2010) Lipid droplets: a dynamic organelle moves into focus. FEBS Lett 584:2176–2182
Bergman B, Gallon JR, Rai AN et al (1997) N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19:139–185
Bhattacharya D, Archibald JM, Weber AP et al (2007) How do endosymbionts become organelles? Understanding early events in plastid evolution. Bioessays 29:1239–1246
Bhattacharya D, Price DC, Chan CX et al (2013) Genome of the red alga Porphyridium purpureum. Nat Commun 4:1941
Blank CE, Sanchez-Baracaldo P (2010) Timing of morphological and ecological innovations in the cyanobacteria – a key to understanding the rise in atmospheric oxygen. Geobiology 8:1–23
Borowitza MA (1978) Plastid development and floridean starch grain formation during carposporogenesis in the coralline red alga Lithothrix aspergillum gray. Protoplasma 95:217–228
Brautigan DL (2013) Protein Ser/Thr phosphatases – the ugly ducklings of cell signalling. FEBS J 280:324–345
Burris RH (1991) Nitrogenase. J Biol Chem 266:9339–9342
Busi MV, Barchiesi J, Martin M et al (2013) Starch metabolism in green algae. Starch/Stärke 66:28–40
Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366
Cavalier-Smith T, Chao EE, Snell EA et al (2014) Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa. Mol Phylogenet Evol 81C:71–85
Cenci U, Chabi M, Ducatez M et al (2013) Convergent evolution of polysaccharide debranching defines a common mechanism for starch accumulation in cyanobacteria and plants. Plant Cell 25:3961–3975
Cenci U, Nitschke F, Steup M et al (2014) Transition from glycogen to starch metabolism in Archaeplastida. Trends Plant Sci 19:18–28
Chandra G, Chater KF, Bornemann S (2011) Unexpected and widespread connections between bacterial glycogen and trehalose metabolism. Microbiology 157:1565–1572
Charng YY, Kakefuda G, Iglesias AA et al (1992) Molecular cloning and expression of the gene encoding ADP-glucose pyrophosphorylase from the cyanobacterium Anabaena sp. strain PCC 7120. Plant Mol Biol 20:37–47
Choi JH, Lee H, Kim YW et al (2009) Characterization of a novel debranching enzyme from Nostoc punctiforme possessing a high specificity for long branched chains. Biochem Biophys Res Commun 378:224–229
Collen J, Porcel B, Carre W et al (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A 110:5247–5252
Colleoni C, Suzuki E (2012) Chapter 5: Storage polysaccharide metabolism in Cyanobacteria. In: Tetlow IJ (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. Society for Experimental Biology, London
Colleoni C, Linka M, Deschamps P et al (2010) Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis. Mol Biol Evol 27:2691–2701
Collingro A, Tischler P, Weinmaier T et al (2011) Unity in variety – the pan-genome of the Chlamydiae. Mol Biol Evol 28:3253–3270
Compaore J, Stal LJ (2010) Oxygen and the light–dark cycle of nitrogenase activity in two unicellular cyanobacteria. Environ Microbiol 12:54–62
Coppin A, Varre JS, Lienard L et al (2004) Evolution of plant-like crystalline storage polysaccharide in the protozoan parasite Toxoplasma gondii argues for a red alga ancestry. J Mol Evol 60:257–267
Coutinho PM, Henrissat B (1999) Carbohydrate-active enzymes: an integrated database approach. Royal Society of Chemistry, Cambridge
Crowe SA, Dossing LN, Beukes NJ et al (2013) Atmospheric oxygenation three billion years ago. Nature 501:535–538
Curatti L, Giarrocco LE, Cumino AC et al (2008) Sucrose synthase is involved in the conversion of sucrose to polysaccharides in filamentous nitrogen-fixing cyanobacteria. Planta 228:617–625
Curtis BA, Tanifuji G, Burki F et al (2012) Cryptophyte and chlorarachniophyte nuclear genomes reveal evolutionary mosaicism and fate of nucleomorphs. Nature 492:59–65
Dauvillée D, Kinderf IS, Li Z et al (2005) Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187:1465–1473
Dauvillee D, Deschamps P, Ral JP et al (2009) Genetic dissection of floridean starch synthesis in the cytosol of the model dinoflagellate Crypthecodinium cohnii. Proc Natl Acad Sci U S A 106:21126–21130
Deane JA, Strachan IM, Saunders GW et al (2002) Cryptomonad evolution: nuclear 18S rDNA phylogeny versus cell morphology and pigmentation. J Phycol 38:1236–1244
Delrue B, Fontaine T, Routier F et al (1992) Waxy Chlamydomonas reinhardtii: monocellular algal mutants defective in amylose biosynthesis and granule-bound starch synthase activity accumulate a structurally modified amylopectin. J Bacteriol 174:3612–3620
Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Am Nat 154:S164–S177
Deschamps P, Haferkamp I, Dauvillée D et al (2006) Nature of the periplastidial pathway of starch synthesis in the cryptophyte Guillardia theta. Eukaryot Cell 5:954–963
Deschamps P, Colleoni C, Nakamura Y et al (2008a) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25:536–548
Deschamps P, Guillebeault D, Devassine J et al (2008b) The heterotrophic dinoflagellate Crypthecodinium cohnii defines a model genetic system to investigate cytoplasmic starch synthesis. Eukaryot Cell 7:872–880
Deschamps P, Haferkamp I, d’Hulst C et al (2008c) The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci 13:574–582
Deschamps P, Moreau H, Worden AZ et al (2008d) Early gene duplication within chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics 178:2373–2387
Devillers CH, Piper ME, Ballicora MA et al (2003) Characterization of the branching patterns of glycogen branching enzyme truncated on the N-terminus. Arch Biochem Biophys 418:34–38
Douglas SE, Penny SL (1999) The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 48:236–244
Douglas S, Zauner S, Fraunholz M et al (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410:1091–1096
Ekman P, Yu S, Pedersén M (1991) Effects of altered salinity, darkness and algal nutrient status on floridoside and starch content, alpha-galactosidase activity and agar yield of cultivated Gracilaria sordida. Br Phycol J 26:123–131
Facchinelli F, Pribil M, Oster U et al (2013) Proteomic analysis of the Cyanophora paradoxa muroplast provides clues on early events in plastid endosymbiosis. Planta 237:637–651
Falcon LI, Cipriano F, Chistoserdov AY et al (2002) Diversity of diazotrophic unicellular cyanobacteria in the tropical North Atlantic Ocean. Appl Environ Microbiol 68:5760–5764
Falkowski P, Raven JA (2007) Aquatic photosynthesis. Princeton University Press, Princeton
Fathinejad S, Steiner JM, Reipert S et al (2008) A carboxysomal carbon-concentrating mechanism in the cyanelles of the ‘coelacanth’ of the algal world, Cyanophora paradoxa? Physiol Plant 133:27–32
Fettke J, Hejazi M, Smirnova J et al (2009) Eukaryotic starch degradation: integration of plastidial and cytosolic pathways. J Exp Bot 60:2907–2922
Forsyth G, Hirst EL, Oxford AE (1953) Protozoal polysaccharides. Structure of a polysaccharide produced by Cycloposthium. J Chem Soc 2030–2033
Fredrick JF (1968) Biochemical evolution of glucosyl transferase isozymes in algae. Ann N Y Acad Sci 151:413–423
Frueauf JB, Ballicora MA, Preiss J (2002) Alteration of inhibitor selectivity by site-directed mutagenesis of Arg(294) in the ADP-glucose pyrophosphorylase from Anabaena PCC 7120. Arch Biochem Biophys 400:208–214
Fu J, Xu X (2006) The functional divergence of two glgP homologues in Synechocystis sp. PCC 6803. FEMS Microbiol Lett 260:201–209
Glöckner G, Noegel A (2013) Comparative genomics in the Amoebozoa clade. Biol Rev 88:215–225
Goldemberg SH, Marechal LR (1963) Biosynthesis of paramylon in Euglena gracilis. Biochim Biophys Acta 71:743–744
Grosche C, Hempel F, Bolte K et al (2014) The periplastidal compartment: a naturally minimized eukaryotic cytoplasm. Curr Opin Microbiol 22C:88–93
Grundel M, Scheunemann R, Lockau W et al (2012) Impaired glycogen synthesis causes metabolic overflow reactions and affects stress responses in the Cyanobacterium Synechocystis sp. PCC 6803. Microbiology 158:3032–3043
Guerra LT, Xu Y, Bennette N et al (2013) Natural osmolytes are much less effective substrates than glycogen for catabolic energy production in the marine cyanobacterium Synechococcus sp. strain PCC 7002. J Biotechnol 166:65–75
Haferkamp I, Deschamps P, Ast M et al (2006) Molecular and biochemical analysis of periplastidial starch metabolism in the cryptophyte Guillardia theta. Eukaryot Cell 5:964–971
Henrissat B, Deleury E, Coutinho PM (2002) Glycogen metabolism loss: a common marker of parasitic behaviour in bacteria? Trends Genet 18:437–440
Higo A, Katoh H, Ohmori K et al (2006) The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 152:979–987
Hirabaru C, Izumo A, Fujiwara S et al (2010) The primitive rhodophyte Cyanidioschyzon merolae contains a semiamylopectin-type, but not an amylose-type, alpha-glucan. Plant Cell Physiol 51:682–693
Huang J, Gogarten JP (2007) Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol 8:R99
Husnik F, Nikoh N, Koga R et al (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153:1567–1578
Izumo A, Fujiwara S, Sakurai T et al (2011) Effects of granule-bound starch synthase I-defective mutation on the morphology and structure of pyrenoidal starch in Chlamydomonas. Plant Sci 180:238–245
James MG, Robertson DS, Myers AM (1995) Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7:417–429
Kiel JA, Boels JM, Beldman G et al (1990) Nucleotide sequence of the Synechococcus sp. PCC7942 branching enzyme gene (glgB): expression in Bacillus subtilis. Gene 89:77–84
Kiss JK, Roberts EM, Brown RM et al (1988) X-ray and dissolution studies of paramylon storage granules from Euglena. Protoplasma 146:150–156
Kopp RE, Kirschvink JL, Hilburn IA et al (2005) The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc Natl Acad Sci U S A 102:11131–11136
Kotting O, Pusch K, Tiessen A et al (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol 137:242–252
Kotting O, Santelia D, Edner C et al (2009) STARCH-EXCESS4 is a laforin-like Phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21:334–346
Kubo A, Fujita N, Harada K et al (1999) The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol 121:399–410
Ladeira RB, Freitas MA, Silva EF et al (2005) Glycogen as a carbohydrate energy reserve in trophozoites of Giardia lamblia. Parasitol Res 96:418–421
Lafora GR, Glueck B (1911) Beitrag zur histopathologie der myoklonischen epilepsie. Z Gesamte Neurol Psychiatr 6:1–14
Larsson J, Nylander JA, Bergman B (2011) Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol 11:187
Latysheva N, Junker VL, Palmer WJ et al (2012) The evolution of nitrogen fixation in cyanobacteria. Bioinformatics 28:603–606
Le Gall L, Saunders GW (2007) A nuclear phylogeny of the Florideophyceae (Rhodophyta) inferred from combined EF2, small subunit and large subunit ribosomal DNA: establishing the new red algal subclass Corallinophycidae. Mol Phylogenet Evol 43:1118–1130
Linka M, Jamai A, Weber AP (2008) Functional characterization of the plastidic phosphate translocator gene family from the thermo-acidophilic red alga Galdieria sulphuraria reveals specific adaptations of primary carbon partitioning in green plants and red algae. Plant Physiol 148:1487–1496
Lister DL, Bateman JM, Purton S et al (2003) DNA transfer from chloroplast to nucleus is much rarer in Chlamydomonas than in tobacco. Gene 316:33–38
Lluisma AO, Ragan MA (1998) Characterization of a galactose-1-phosphate uridylyltransferase gene from the marine red alga Gracilaria gracilis. Curr Genet 34:112–119
Loddenkotter B, Kammerer B, Fischer K et al (1993) Expression of the functional mature chloroplast triose phosphate translocator in yeast internal membranes and purification of the histidine-tagged protein by a single metal-affinity chromatography step. Proc Natl Acad Sci U S A 90:2155–2159
Lorenzo-Morales J, Kliescikova J, Martinez-Carretero E et al (2008) Glycogen phosphorylase in Acanthamoeba spp.: determining the role of the enzyme during the encystment process using RNA interference. Eukaryot Cell 7:509–517
Lou J, Dawson KA, Strobel HJ (1997) Glycogen biosynthesis via UDP-glucose in the ruminal bacterium Prevotella bryantii B1(4). Appl Environ Microbiol 63:4355–4359
Lu Y, Sharkey TD (2006) The importance of maltose in transitory starch breakdown. Plant Cell Environ 29:353–366
Lu C, Lei L, Peng B et al (2013) Chlamydia trachomatis GlgA is secreted into host cell cytoplasm. PLoS One 8:e68764
Maddelein ML, Libessart N, Bellanger F et al (1994) Toward an understanding of the biogenesis of the starch granule. Determination of granule-bound and soluble starch synthase functions in amylopectin synthesis. J Biol Chem 269:25150–25157
Manners DJ, Ryley JF (1952) Studies on the metabolism of the Protozoa. II. The glycogen of the ciliate Tetrahymena pyriformis (Glaucoma piriformis). Biochem J 52:480–482
Manners DJ, Ryley JF (1955) Studies on the metabolism of the protozoa. 6. The glycogens of the parasitic flagellates Trichomonas foetus and Trichomonas gallinae. Biochem J 59:369–372
Marin B, Nowack EC, Melkonian M (2005) A plastid in the making: evidence for a second primary endosymbiosis. Protist 156:425–432
Martijn J, Ettema TJ (2013) From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem Soc Trans 41:451–457
Matsuzaki M, Misumi O, Shin IT et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657
McCracken DA, Cain JR (1981) Amylose in Floridean starch. New Phytol 88
Meeuse BJ, Kreger DR (1954) On the nature of floridean starch and Ulva starch. Biochim Biophys Acta 13:593–595
Meeuse BJ, Andries M, Wood JA (1960) Floridean starch. J Exp Bot 11:129–140
Miao X, Wu Q, Wu G et al (2003) Sucrose accumulation in salt-stressed cells of agp gene deletion-mutant in cyanobacterium Synechocystis sp PCC 6803. FEMS Microbiol Lett 218:71–77
Moran-Zorzano MT, Alonso-Casajus N, Munoz FJ et al (2007) Occurrence of more than one important source of ADPglucose linked to glycogen biosynthesis in Escherichia coli and Salmonella. FEBS Lett 581:4423–4429
Moriyama T, Sakurai K, Sekine K et al (2014) Subcellular distribution of central carbohydrate metabolism pathways in the red alga Cyanidioschyzon merolae. Planta 240:585–598
Mouille G, Maddelein ML, Libessart N et al (1996) Preamylopectin processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8:1353–1366
Moustafa A, Reyes-Prieto A, Bhattacharya D (2008) Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PLoS One 3:e2205
Murakami T, Kanai T, Takata H et al (2006) A novel branching enzyme of the GH-57 family in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Bacteriol 188:5915–5924
Nagashima H, Nakamura S, Nisizawa K et al (1971) Enzymatic synthesis of floridean starch in red alga Serraticardia maxima. Plant Cell Physiol 12:243–253
Nakamura Y, Takahashi J, Sakurai A et al (2005) Some Cyanobacteria synthesize semi-amylopectin type alpha-polyglucans instead of glycogen. Plant Cell Physiol 46:539–545
Nakayama A, Yamamoto K, Tabata S (2001) Identification of the catalytic residues of bifunctional glycogen debranching enzyme. J Biol Chem 276:28824–28828
Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9:297–300
Nowack EC, Melkonian M, Glockner G (2008) Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr Biol 18:410–418
Nyvall P, Pelloux J, Davies HV et al (1999) Purification and characterisation of a novel starch synthase selective for uridine 5′-diphosphate glucose from the red alga Gracilaria tenuistipitata. Planta 209:143–152
Nyvall P, Pedersen M, Kenne L et al (2000) Enzyme kinetics and chemical modification of alpha-1,4-glucan lyase from Gracilariopsis sp. Phytochemistry 54:139–145
Ojcius DM, Degani H, Mispelter J et al (1998) Enhancement of ATP levels and glucose metabolism during an infection by Chlamydia. NMR studies of living cells. J Biol Chem 273:7052–7058
Pade N, Linka N, Ruth W et al (2014) Floridoside and isofloridoside are synthesized by trehalose 6-phosphate synthase-like enzymes in the red alga Galdieria sulphuraria. New Phytol. doi:10.1111/nph.13108
Page-Sharp M, Behm CA, Smith GD (1999) Involvement of the compatible solutes trehalose and sucrose in the response to salt stress of a cyanobacterial Scytonema species isolated from desert soils. Biochim Biophys Acta 1472:519–528
Palmer TN, Ryman BE, Whelan WJ (1976) The action pattern of amylomaltase from Escherichia coli. Eur J Biochem 69:105–115
Park JT, Shim JH, Tran PL et al (2011) Role of maltose enzymes in glycogen synthesis by Escherichia coli. J Bacteriol 193:2517–2526
Petersen J, Ludewig AK, Michael V et al (2014) Chromera velia, endosymbioses and the rhodoplex hypothesis – plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol Evol 6:666–684
Pittenauer E, Schmid ER, Allmaier G et al (1993) Structural characterization of the cyanelle peptidoglycan of Cyanophora paradoxa by 252Cf plasma desorption mass spectrometry and fast atom bombardment/tandem mass spectrometry. Biol Mass Spectrom 22:524–536
Plancke C, Colleoni C, Deschamps P et al (2008) Pathway of cytosolic starch synthesis in the model glaucophyte Cyanophora paradoxa. Eukaryot Cell 7:247–257
Porchia AC, Curatti L, Salerno GL (1999) Sucrose metabolism in cyanobacteria: sucrose synthase from Anabaena sp. strain PCC 7119 is remarkably different from the plant enzymes with respect to substrate affinity and amino-terminal sequence. Planta 210:34–40
Preiss J (1984) Bacterial glycogen synthesis and its regulation. Annu Rev Microbiol 38:419–458
Price DC, Chan CX, Yoon HS et al (2012) Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335:843–847
Ragan MA, Bird CJ, Rice EL et al (1994) A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene. Proc Natl Acad Sci U S A 91:7276–7280
Reyes-Prieto A, Moustafa A, Bhattacharya D (2008) Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr Biol 18:956–962
Rodriguez-Ezpeleta N, Brinkmann H, Burey SC et al (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15:1325–1330
Rogers PV, Luo S, Sucic JF et al (1992) Characterization and cloning of glycogen phosphorylase 1 from Dictyostelium discoideum. Biochim Biophys Acta 1129:262–272
Rogers PV, Sucic JF, Yin Y et al (1994) Disruption of glycogen phosphorylase gene expression in Dictyostelium: evidence for altered glycogen metabolism and developmental coregulation of the gene products. Differentiation 56:1–12
Rutherford CL, Peery RB, Sucic JF et al (1992) Cloning, structural analysis, and expression of the glycogen phosphorylase-2 gene in Dictyostelium. J Biol Chem 267:2294–2302
Sanchez-Baracaldo P, Ridgwell A, Raven JA (2014) A neoproterozoic transition in the marine nitrogen cycle. Curr Biol 24:652–657
Sanchez-Puerta MV, Lippmeier JC, Apt KE et al (2007) Plastid genes in a non-photosynthetic dinoflagellate. Protist 158:105–117
Santos CR, Tonoli CC, Trindade DM et al (2011) Structural basis for branching-enzyme activity of glycoside hydrolase family 57: structure and stability studies of a novel branching enzyme from the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. Proteins 79:547–557
Sawada T, Nakamura Y, Ohdan T et al (2014) Diversity of reaction characteristics of glucan branching enzymes and the fine structure of alpha-glucan from various sources. Arch Biochem Biophys 562C:9–21
Schlichting R, Bothe H (1993) The cyanelle (Organelles of a low evolutionary scale) possess a phosphate-translocator and a glucose-carrier in Cyanophora paradoxa. Botanica Acta 106:428–434
Schneegurt MA, Sherman DM, Nayar S et al (1994) Oscillating behavior of carbohydrate granule formation and dinitrogen fixation in the cyanobacterium Cyanothece sp. strain ATCC 51142. J Bacteriol 176:1586–1597
Schonknecht G, Chen WH, Ternes CM et al (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210
Schwoppe C, Winkler HH, Neuhaus HE (2002) Properties of the glucose-6-phosphate transporter from Chlamydia pneumoniae (HPTcp) and the glucose-6-phosphate sensor from Escherichia coli (UhpC). J Bacteriol 184:2108–2115
Schwoppe C, Winkler HH, Neuhaus HE (2003) Connection of transport and sensing by UhpC, the sensor for external glucose-6-phosphate in Escherichia coli. Eur J Biochem 270:1450–1457
Serodio J, Cruz S, Cartaxana P et al (2014) Photophysiology of kleptoplasts: photosynthetic use of light by chloroplasts living in animal cells. Philos Trans R Soc Lond B Biol Sci 369:20130242
Sesma JI, Iglesias AA (1998) Synthesis of floridean starch in the red alga Gracilaria gracilis occurs via ADP-glucose. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic Publishers, Dordrecht, pp 3537–3540
Sheath RG, Hellebust JA, Sawa T (1979) Floridean starch metabolism of Porphyridium purpureum Rhophyta I. Changes during ageing of batch culture. Phycologia 18:292–293
Sheng J, Preiss J (1997) Arginine294 is essential for the inhibition of Anabaena PCC 7120 ADP-glucose pyrophosphorylase by phosphate. Biochemistry 36:13077–13084
Shih PM, Matzke NJ (2013) Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc Natl Acad Sci U S A 110:12355–12360
Shimonaga T, Fujiwara S, Kaneko M et al (2007) Variation in storage alpha-polyglucans of red algae: amylose and semi-amylopectin types in Porphyridium and glycogen type in Cyanidium. Mar Biotechnol (NY) 9:192–202
Shimonaga T, Konishi M, Oyama Y et al (2008) Variation in storage alpha-glucans of the Porphyridiales (Rhodophyta). Plant Cell Physiol 49:103–116
Shoguchi E, Shinzato C, Kawashima T et al (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399–1408
Singh PK (1973) Nitrogen fixation by the unicellular blue-green alga Aphanothece. Arch Mikrobiol 92:59–62
Stadnichuk IN, Semenova LR, Smirnova GP et al (2007) A highly branched storage polyglucan in the thermoacidophilic red microalga Galdieria maxima cells. Prikl Biokhim Mikrobiol 43:88–93
Stegemann S, Hartmann S, Ruf S et al (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci U S A 100:8828–8833
Steiner JM, Yusa F, Pompe JA et al (2005) Homologous protein import machineries in chloroplasts and cyanelles. Plant J 44:646–652
Streb S, Delatte T, Umhang M et al (2008) Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell 20:3448–3466
Summons RE, Jahnke LL, Hope JM et al (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:554–557
Suzuki E, Umeda K, Nihei S, Moriya K, Ohkawa H, Fujiwara S, Tsuzuki M, Nakamura Y (2007) Role of the GlgX protein in glycogen metabolism of the cyanobacterium, Synechococcus elongatus PCC 7942. Biochim Biophys Acta 1770:763–773
Suzuki E, Ohkawa H, Moriya K et al (2010) Carbohydrate metabolism in mutants of the cyanobacterium Synechococcus elongatus PCC 7942 defective in glycogen synthesis. Appl Environ Microbiol 76:3153–3159
Suzuki E, Onoda M, Colleoni C et al (2013) Physicochemical variation of cyanobacterial starch, the insoluble alpha-Glucans in cyanobacteria. Plant Cell Physiol 54:465–473
Szydlowski N, Ragel P, Raynaud S et al (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21:2443–2457
Tagliabracci VS, Turnbull J, Wang W et al (2007) Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo. Proc Natl Acad Sci U S A 104:19262–19266
Tomos AD, Northcote DH (1978) A protein-glucan intermediate during paramylon synthesis. Biochem J 174:283–290
Torija MJ, Novo M, Lemassu A et al (2005) Glycogen synthesis in the absence of glycogenin in the yeast Saccharomyces cerevisiae. FEBS Lett 579:3999–4004
Tresse E, Kosta A, Giusti C et al (2008) A UDP-glucose derivative is required for vacuolar autophagic cell death. Autophagy 4:680–691
Tuttle RC, Loeblich AR 3rd (1974) Genetic recombination in the dinoflagellate Crypthecodinium cohnii. Science 185:1061–1062
Tuttle RC, Loeblich AR 3rd (1977) N-methyl-N′-nitro-N-nitrosoguanidine and UV induced mutants of the dinoflagellate Crypthecodinium cohnii. J Protozool 24:313–316
Ugalde JE, Parodi AJ, Ugalde RA (2003) De novo synthesis of bacterial glycogen: Agrobacterium tumefaciens glycogen synthase is involved in glucan initiation and elongation. Proc Natl Acad Sci U S A 100:10659–10663
Villarejo A, Martinez F, del Pino Plumed M et al (1996) The induction of the CO2 concentrating mechanism in a starch-less mutant of Chlamydomonas reinhardtii. Physiol Plant 98:798–802
Viola R, Nyvall P, Pedersen M (2001) The unique features of starch metabolism in red algae. Proc Biol Sci 268:1417–1422
Vogel K, Barber AA (1968) Degradation of paramylon by Euglena gracilis. J Protozool 15:657–662
Wattebled F, Buleon A, Bouchet B et al (2002) Granule-bound starch synthase I. A major enzyme involved in the biogenesis of B-crystallites in starch granules. Eur J Biochem 269:3810–3820
Wattebled F, Dong Y, Dumez S et al (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiol 138:184–195
Weber AP, Linka M, Bhattacharya D (2006) Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryot Cell 5:609–612
Williams TA, Foster PG, Nye TM et al (2012) A congruent phylogenomic signal places eukaryotes within the Archaea. Proc Biol Sci 279:4870–4879
Williamson BD, Favis R, Brickey DA et al (1996) Isolation and characterization of glycogen synthase in Dictyostelium discoideum. Dev Genet 19:350–364
Wilson WA, Roach PJ, Montero M et al (2010) Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev 34:952–985
Wisecaver JH, Hackett JD (2011) Dinoflagellate genome evolution. Annu Rev Microbiol 65:369–387
Wolf A, Kramer R, Morbach S (2003) Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress. Mol Microbiol 49:1119–1134
Wyatt JT, Silvey JK (1969) Nitrogen fixation by gloeocapsa. Science 165:908–909
Xu Y, Guerra LT, Li Z et al (2013) Altered carbohydrate metabolism in glycogen synthase mutants of Synechococcus sp. strain PCC 7002: cell factories for soluble sugars. Metab Eng 16:56–67
Yoo SH, Spalding MH, Jane JL (2002) Characterization of cyanobacterial glycogen isolated from the wild type and from a mutant lacking of branching enzyme. Carbohydr Res 337:2195–2203
Yoo SH, Lee BH, Moon Y et al (2014) Glycogen synthase isoforms in Synechocystis sp. PCC6803: identification of different roles to produce glycogen by targeted mutagenesis. PLoS One 9:e91524
Yoon HS, Hackett JD, Pinto G et al (2002) The single, ancient origin of chromist plastids. Proc Natl Acad Sci U S A 99:15507–15512
Yoon HS, Hackett JD, Ciniglia C et al (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818
Yoon HS, Müller KM, Stheath RG et al (2006) Defining the major lineages of red algae (Rhodophyta). J Phycol 42:482–492
Yoshikawa H, Nagashima M, Morimoto K et al (2003) Freeze-fracture and cytochemical studies on the in vitro cyst form of reptilian Blastocystis pythoni. J Eukaryot Microbiol 50:70–75
Yu S, Pedersen M (1993) Alpha-1,4-glucan lyase, a new class of starch/glycogen-degrading enzyme. II. Subcellular localization and partial amino-acid sequence. Planta 191:137–142
Yu S, Bojsen K, Svensson B et al (1999) alpha-1,4-glucan lyases producing 1,5-anhydro-D-fructose from starch and glycogen have sequence similarity to alpha-glucosidases. Biochim Biophys Acta 1433:1–15
Yu TS, Kofler H, Hausler RE et al (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13:1907–1918
Zea CJ, Pohl NL (2004) General assay for sugar nucleotidyltransferases using electrospray ionization mass spectrometry. Anal Biochem 328:196–202
Zona R, Chang-Pi-Hin F, O’Donohue MJ et al (2004) Bioinformatics of the glycoside hydrolase family 57 and identification of catalytic residues in amylopullulanase from Thermococcus hydrothermalis. Eur J Biochem 271:2863–2872
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer Japan
About this chapter
Cite this chapter
Ball, S., Colleoni, C., Arias, M.C. (2015). The Transition from Glycogen to Starch Metabolism in Cyanobacteria and Eukaryotes. In: Nakamura, Y. (eds) Starch. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55495-0_4
Download citation
DOI: https://doi.org/10.1007/978-4-431-55495-0_4
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-55494-3
Online ISBN: 978-4-431-55495-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)