Skip to main content

Convergent Evolution of Starch Metabolism in Cyanobacteria and Archaeplastida

  • Chapter
  • First Online:
Evolutionary Biology
  • 2051 Accesses

Abstract

It is widely accepted that Archaeplastida phylum comprising Glaucophyta, Rhodophyta, and Chloroplastida originates from a unique endosymbiosis event, called primary plastid endosymbiosis, between a cyanobacterium and a eukaryotic cell. In addition to acquiring oxygenic photosynthesis, the three sister lineages gained the ability to synthesize a novel semi-crystalline storage polysaccharide: starch. In Archaeplastida, several lines of evidence reveal that the transition from glycogen synthesis to starch accumulation results in the recruitment of an isoamylase (ISA)-type debranching enzyme. The latter removes short-branched glucan chains, which prevent amylopectin crystallization. Recently, a small group of unicellular diazotrophic cyanobacteria, possibly the closest relative of the ancestral plastid, have been reported accumulating starch-like granules composed of both amylose and amylopectin fractions instead of glycogen particles. In order to understand starch metabolism in this particular group of cyanobacteria, a random mutagenesis was carried out on the unicellular starch-accumulating Cyanobacterium sp. CLg1. Throughout iodine crystal vapors screening, fourteen mutant strains have substituted starch granules by that of glycogen particles. Interestingly, such as in plants, all mutant strains were impaired in an isoamylase-type debranching enzyme activity. However, phylogenetic analyses point out that the critical step for starch crystallization in Archaeplastida did not evolve from the cyanobacterial isoamylase/glgX gene, but from another pathogenic bacteria. Based on this work, it appears that the transition from glycogen to starch has evolved independently in both cyanobacteria and Archaeplastida by following a common glucan trimming mechanism.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ball SG, Colleoni C, Arias MC (2015a) The transition from glycogen to starch metabolism in cyanobacteria and eukaryotes. In: Nakamura Y (ed) Starch: metabolism and structure. Springer, Berlin, pp 93–158

    Google Scholar 

  • Ball SG, Colleoni C Kadouche D et al (2015b) Toward an understanding of the function of Chlamydiales in plastid endosymbiosis. Biochim Biophys Acta 1847:495–504

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bergman B, Gallon JR, Rai AN et al (1997) N2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19:139–185

    Article  CAS  Google Scholar 

  • Bertoft E, Laohaphatanalert K, Piyachomkwan K, Sriroth K (2010) The fine structure of cassava starch amylopectin. Part 2: building block structure of clusters. Int J Biol Macromol 47:325–335

    Google Scholar 

  • Bertoft E (2004) On the nature of categories of chains in amylopectin and their connection to the super helix model. Carbohydr Polym 57:211–224

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Burris RH (1991) Nitrogenase. J Biol Chem 266:9339–9342

    CAS  PubMed  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C et al (2009) The carbohydrate-active enzymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:D233–D238

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cenci U, Chabi M, Ducatez M, Tirtiaux C, Nirmal-Raj J, Utsumi Y, Kobayashi D, Sasaki S, Suzuki E, Nakamura Y, Putaux JL, Roussel X, Durand-Terrasson A, Bhattacharya D, Vercoutter-Edouart AS, Maes E, Arias MC, Palcic M, Sim L, Ball SG, Colleoni C (2013) Convergent evolution of polysaccharide debranching defines a common mechanism for starch accumulation in cyanobacteria and plants. Plant Cell 25:3961–3975

    Google Scholar 

  • Colleoni C, Suzuki E (2012) Storage polysaccharide metabolism in cyanobacteria. Essential reviews in experimental biology: starch: origins, structure and metabolism, vol 5 (Chap. 5)

    Google Scholar 

  • Compaore J, Stal LJ (2010) Oxygen and the light-dark cycle of nitrogenase activity in two unicellular cyanobacteria. Environ Microbiol 12:54–62

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Correns C (1901) Bastarde zwischen maisrassen mit besonder berucksichtung der Xenien. Bibl Bot 53:1–161

    Google Scholar 

  • Criscuolo A, Gribaldo S (2011) Large-scale phylogenomic analyses indicate a deep origin of primary plastids within cyanobacteria. Mol Biol Evol 28:3019–3032

    Article  CAS  PubMed  Google Scholar 

  • Dauvillée D, Kinderf IS, Li Z et al (2005) Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187:1465–1473

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deschamps P, Colleoni C, Nakamura Y et al (2008a) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25:536–548

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eme L, Sharpe SC, Brown MW et al (2014) On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb Perspect Biol 6

    Google Scholar 

  • Facon M, Lin Q, Azzaz AM et al (2013) Distinct functional properties of isoamylase-type starch debranching enzymes in monocot and dicot leaves. Plant Physiol 163:1363–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falcón 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Falcón LI, Magallón S, Castillo A (2010) Dating the cyanobacterial ancestor of the chloroplast. ISME J 4:777–783

    Article  PubMed  Google Scholar 

  • Hardy TA, Roach PJ (1993) Control of yeast glycogen synthase-2 by COOH-terminal phosphorylation. J Biol Chem 268:23799–23805

    CAS  PubMed  Google Scholar 

  • Hizukuri S (1986) Polymodal distribution of the chain lengths of amylopectin and its significance. Carbohydr Res 147:342–347

    Google Scholar 

  • Iglesias AA, Ballicora MA, Sesma JI et al (2006) Domain swapping between a cyanobacterial and a plant subunit ADP-glucose pyrophosphorylase. Plant Cell Physiol 47:523–530

    Article  CAS  PubMed  Google Scholar 

  • Inouchi N, Glover DV, Fuwa H (1987) Chain length distribution of amylopectins of several single mutants and the normal counterpart, and sugary-1 phytoglycogen in maize (Zea mays). Starch 39:259–266

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins PJ, Cameron RE, Donald AM (1993) A universal feature in the structure of starch granules from different botanical sources. Starch 45:415–420

    Google Scholar 

  • 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 USA 102:11131–11136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kubo A, Rahman S, Utsumi Y et al (2005) Complementation of sugary-1 phenotype in rice endosperm with the wheat isoamylase1 gene supports a direct role for isoamylase1 in amylopectin biosynthesis. Plant Physiol 137:43–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsson J, Nylander JA, Bergman B (2011) Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol 11:187

    Article  PubMed  PubMed Central  Google Scholar 

  • Latysheva N, Junker VL, Palmer WJ et al (2012) The evolution of nitrogen fixation in cyanobacteria. Bioinformatics 28:603–606

    Article  CAS  PubMed  Google Scholar 

  • Li B, Lopes JS, Foster PG et al (2014) Compositional biases among synonymous substitutions cause conflict between gene and protein trees for plastid origins. Mol Biol Evol 31:1697–1709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li SC, Chen CM, Goldstein JL et al (2010) Glycogen storage disease type IV: novel mutations and molecular characterization of a heterogeneous disorder. J Inherit Metab Dis 33(Suppl 3):S83–S90

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Martin W, Rujan T, Richly E et al (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melendez R, Melendez-Hevia E, Canela EI (1999) The fractal structure of glycogen: a clever solution to optimize cell metabolism. Biophys J 77:1327–1332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melendez R, Melendez-Hevia E, Cascante M (1997) How did glycogen structure evolve to satisfy the requirement for rapid mobilization of glucose? A problem of physical constraints in structure building. J Mol Evol 45:446–455

    Article  CAS  PubMed  Google Scholar 

  • Melendez R, Melendez-Hevia E, Mas F et al (1998) Physical constraints in the synthesis of glycogen that influence its structural homogeneity: a two-dimensional approach. Biophys J 75:106–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melendez-Hevia E, Waddell TG, Shelton ED (1993) Optimization of molecular design in the evolution of metabolism: the glycogen molecule. Biochem J 295(Pt 2):477–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moses SW, Parvari R (2002) The variable presentations of glycogen storage disease type IV: a review of clinical, enzymatic and molecular studies. Curr Mol Med 2:177–188

    Article  CAS  PubMed  Google Scholar 

  • Mouille G, Maddelein ML, Libessart N et al (1996) Preamylopectin processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8:1353–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Nakayama A, Yamamoto K, Tabata S (2001) Identification of the catalytic residues of bifunctional glycogen debranching enzyme. J Biol Chem 276:28824–28828

    Article  CAS  PubMed  Google Scholar 

  • Nelson OE, Rines HW (1962) The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 9:297–300

    Article  CAS  PubMed  Google Scholar 

  • Ochoa de Alda JA, Esteban R, Diago ML et al (2014) The plastid ancestor originated among one of the major cyanobacterial lineages. Nat Commun 5:4937

    Article  CAS  PubMed  Google Scholar 

  • Oyama Y, Izumo A, Fujiwara S et al (2006) Granule-bound starch synthase cDNA in Chlorella kessleri 11h: cloning and regulation of expression by CO(2) concentration. Planta 224:646–654

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Prechtl J, Kneip C, Lockhart P et al (2004) Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol Biol Evol 21:1477–1481

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Baracaldo P, Ridgwell A, Raven JA (2014) A neoproterozoic transition in the marine nitrogen cycle. Curr Biol 24:652–657

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schneegurt MA, Sherman DM, Sherman LA (1997) Composition of the carbohydrate granules of the cyanobacterium, Cyanothece sp. strain ATCC 51142. Arch Microbiol 167:89–98

    Article  CAS  Google Scholar 

  • Singh PK (1973) Nitrogen fixation by the unicellular blue-green alga Aphanothece. Arch Mikrobiol 92:59–62

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Streb S, Zeeman SC (2014) Replacement of the endogenous starch debranching enzymes ISA1 and ISA2 of Arabidopsis with the rice orthologs reveals a degree of functional conservation during starch synthesis. PLoS One 9:e92174

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Suzuki E, Umeda K, Nihei S et al (2007) Role of the GlgX protein in glycogen metabolism of the cyanobacterium, Synechococcus elongatus PCC 7942. Biochim Biophys Acta 1770:763–773

    Article  CAS  PubMed  Google Scholar 

  • van de Wal M, D’Hulst C, Vincken JP et al (1998) Amylose is synthesized in vitro by extension of and cleavage from amylopectin. J Biol Chem 273:22232–22240

    Article  PubMed  Google Scholar 

  • Viola R, Nyvall P, Pedersen M (2001) The unique features of starch metabolism in red algae. Proc Biol Sci 268:1417–1422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson WA, Roach PJ, Montero M et al (2010) Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev 34:952–985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyatt JT, Silvey JK (1969) Nitrogen fixation by gloeocapsa. Science 165:908–909

    Article  CAS  PubMed  Google Scholar 

  • Yoon HS, Hackett JD, Ciniglia C et al (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christophe Colleoni .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Colleoni, C., Cenci, U. (2016). Convergent Evolution of Starch Metabolism in Cyanobacteria and Archaeplastida. In: Pontarotti, P. (eds) Evolutionary Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-41324-2_4

Download citation

Publish with us

Policies and ethics