Variation in storage α-glucans of the Porphyridiales (Rhodophyta)

Plant and Cell Physiology

Volumn 49, Issue 1, 2008, Pages 103-116

  Shimonaga, Takahiro ^a   Konishi, Mai ^a   Oyama, Yasunori ^a   Fujiwara, Shoko ^a   Satoh, Aya ^b   Fujita, Naoko ^b   Colleoni, Christophe ^c   Buléon, Alain ^d   Putaux, Jean Luc ^e   Ball, Steven G ^c   Yokoyama, Akiko ^f   Hara, Yoshiaki ^f   Nakamura, Yasunori ^b   Tsuzuki, Mikio ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b AKITA PREFECTURAL UNIVERSITY   (Japan)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^d CEMAGREF   (France)

^e CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^f YAMAGATA UNIVERSITY   (Japan)

Author keywords

Amylose; Floridean starch; Glycogen; Porphyridiales; Rhodophyta; Semi amylopectin

Indexed keywords

GLUCAN;

ARTICLE; CHEMISTRY; CONFORMATION; METABOLISM; RED ALGA; ULTRASTRUCTURE;

ALGAE, RED; CARBOHYDRATE CONFORMATION; GLUCANS;

ALGAE; CYANIDIUM CALDARIUM; GALDIERIA SULPHURARIA; PORPHYRIDIALES; PORPHYRIDIUM; PORPHYRIDIUM PURPUREUM; PORPHYRIDIUM SORDIDUM; RHODELLA VIOLACEA; RHODOPHYTA; RHODOSORUS MARINUS;

EID: 38349097636     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcm172     Document Type: Article

References (54)

1. Adl, S.M., Simpson, A.G., Farmer, M.A., Andersen, R.A., Anderson, O.R., et al. (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52: 399-451.
2. Aizawa, K. and Miyachi, S. (1984) Carbonic anhydrase located on the cell surface increases the affinity for inorganic carbon in photosynthesis of Dunaliella tertiolecta. FEBS Lett. 173: 41-44.
3. Ball, S.G. (1998) Regulation of starch biosynthesis. In The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Edited by Rochaix, J.-D., Goldschmidt-Clermont, M. and Merchant, S. pp. 549-567. Kluwer Academic Publishers, Dordrecht.
4. Ball, S.G. and Morell, M.K. (2003) From bacterial glycogen to starch: understanding the biosynthesis of the plant starch granule. Annu. Rev. Plant. Biol. 54: 207-233.
5. Baunsgaard, L., Lutken, H., Mikkelsen, R., Glaring, M.A., Pham, T.T. and Blennow, A. (2005) A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated alpha-glucans and is involved in starch degradation in Arabidopsis. Plant J. 41: 595-605.
6. Bergmeyer, H.U., Bernt, E., Schmidt, F. and Stock, H. (1974) Determination with hexokinase and glucose-6-phosphate dehydrogenase. In Methods of Enzymatic Analysis. Vol. 3. Edited by Bergmeyer, H.U. pp. 1196-1201. Academic Press, New York.
7. Buléon, A., Gallant, D.J., Bouchet, B., Mouille, G., d'Hulst, C., Kossmann, J. and Ball, S. (1997) Starch from A to C. Plant Physiol. 115: 949-957.
8. Coppin, A., Varre, J.S., Lienard, L., Dauvillee, D., Guerardel, Y., Soyer-Gobillard, M.O., Buléon, A., Ball, S. and Tomavo, S. (2005) 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.
9. Deschamps, P., Haferkamp, I., Dauvillée, D., Haebel, S., Steup, M., et al. (2006) Nature of the periplastidial pathway of starch synthesis in the cryptophyte Guillardia theta. Eukaryot. Cell 5: 954-963.
10. Deschamps, P., Colleoni, C., Nakamura, Y., Suzuki, E., Putaux, J.L., Buléon, A., Haebel, S., Ritte, G., Steup, M., Falcón, L.I., Moreira, D., Loffelhardt, W., Raj, J.N., Plancke, C., d'Hulst, C., Dauvillée, D. and Ball, S. (in press) Metabolic Symbiosis and the Birth of the Plant Kingdom. Mol. Biol. Evol.
11. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Anal. Chem. 28: 350-356.
12. Edner, C., Li, J., Albrecht, T., Mahlow, S., Hejazi, M., Hussain, H., Kaplan, F., Guy, C., Smith, S.M., Steup, M. and Ritte, G. (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial beta-amylases. Plant Physiol. 145: 17-28.
13. Fujita, N., Kubo, A., Suh, D.S., Wong, K.S, Jane, J.L., Ozawa, K., Takaiwa, F., Inaba, Y. and Nakamura, Y. (2003) Antisense inhibition of isoamylase alters the structure of amylopectin and the physicochemical properties of starch in rice endosperm. Plant Cell Physiol. 44: 607-618.
14. Gamborg, O.L., Miller, R.A. and Ojima, K. (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50: 151-158.
15. Hara, Y., Yokoyama, A. and Kim, J.H. (2000) Systematic relationship of unicellular red algae: from the phenetics to the phylogeny. Algae 15: 7-11.
16. Hizukuri, S., Takeda, Y., Yasuda, Y. and Suzuki, A. (1981) Multibranched nature of amylose and action of debranching enzymes. Carbohydr. Res. 94: 205-213.
17. 2 concentration during growth: comparison of structure and properties of pyrenoid and stroma starch. Plant Sci. 172: 1138-1147.
18. Karsten, U., West, J.A., Zuccarello, G.C., Engbrodt, R., Yokoyama, A., Hara, Y. and Brodie, J. (2003) Low molecular weight carbohydrates of the Bangiophycidae (Rhodophyta). J. Phycol. 39: 584-589.
19. Karsten, U., West, J.A., Zuccarello, G.C., Nixdorf, O., Barrow, K.D. and King, R.J. (1999) Low molecular weight carbohydrate patterns in the Bangiophyceae (Rhodophyta). J. Phycol. 35: 967-976.
20. Kubo, A., Fujita, N., Harada, K., Matsuda, T., Satoh, H. and Nakamura, Y. (1999) The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol. 121: 399-409.
21. Manners, D.J. and Sturgeon, R.J. (1982) Reserve carbohydrate of red algae, fungi, and lichens. In Encyclopedia of Plant Physiology. New Series No. 13AI. Edited by Loewus, F.A. and Tanner, W. pp. 472-514. Springer-Verlag, Berlin.
22. Manners, D.J. and Wright, A. (1962) α-1,4-Glucosans. Part XIV. The interaction of concanavalin-A with glycogens. J. Chem. Soc. 4592-4595.
23. Matsuzaki, M., Misumi, O., Shin, I.T., Maruyama, S., Takahara, M., et al. (2004) Genome sequence of the ultrasmall unicellular red algae Cyanidioschyzon merolae 10D. Nature 428: 653-657.
24. McCracken, D.A. and Cain, J.R. (1981) Amylose in floridean starch. New Phytol. 88: 67-71.
25. Meeuse, B.J.D., Andries, M. and Wood, J.A. (1960) Floridean starch. J. Exp. Bot. 11: 129-140.
26. Minoda, A., Sakagami, R., Yagisawa, F., Kuroiwa, T. and Tanaka, K. (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol. 45: 667-671.
27. Moreira, D., Le Guyader, H. and Phillippe, H. (2000) The origin of red algae and the evolution of chloroplasts. Nature 405: 69-72.
28. Nagashima, H., Nakamura, S., Nishizawa, K. and Hori, T. (1971) Enzymic synthesis of floridean starch in a red alga, Serraticardia maxima. Plant Cell Physiol. 12: 243-253.
29. Nakamura, Y., Kubo, A., Shimamune, T., Matsuda, T., Harada, K. and Satoh, H. (1997) Correlation between activities of starch debranching enzyme and α-polyglucan structure in endosperms of sugary-1 mutants of rice. Plant J. 12: 143-153.
30. Nakamura, Y. (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant Cell Physiol. 43: 718-725.
31. Nakamura, Y., Takahashi, J., Sakurai, A., et al. (2005) Some cyanobacteria synthesize semi-amylopectin type α-polyglucans instead of glycogen. Plant Cell Physiol. 46: 539-545.
32. Nyvall, P., Pelloux, J., Davies, H.V., Pedersén, M. and Viola, R. (1999) Purification and characterization of a novel starch synthase selective for 5′-diphosphate glucose from the red alga Gracilaria tenuistipitata. Planta 209: 143-152.
33. O'Shea, M.G. and Morell, M.K. (1996) High resolution slab gel electrophoresis of 8-amino-1,3,6-pyrenetrisufonic acid (APTS) tagged oligosaccharides using a DNA sequencer. Electrophoresis 17: 497-503.
34. 2 concentration. Planta 224: 646-654.
35. Patron, N.J. and Keeling, P.J. (2005) Common evolutionary origin of starch biosynthetic enzymes in green and red algae. J. Phycol. 41: 1131-1141.
36. Peat, S., Turvey, J.R. and Evans, J.M. (1959) The structure of floridean starch. Part II. Enzymic hydrolysis and other studies. J. Chem. Soc. 3341-3344.
37. Plancke, C., Colleoni, C., Deschamps, P., Dauvillée, D., Nakamura, Y., Haebel, S., Ritte, G., Steup, M., Buléon, A., Putaux, J.L., Dupeyre, D., d'Hulst, C., Ral, J.P., Loffelhardt, W. and Ball, S.G. (in press) The pathway of cytosolic starch synthesis in the model glaucophyte. Cyanophora paradoxa. Eukaryot. Cell.
38. Putaux, J.L., Molina-Boisseau, S., Momaur, T. and Dufresne, A. (2003) Platelet nanocrystals resulting from the acid hydrolysis of waxy maize starch granules. Biomacromolecules 4: 1198-1202.
39. Ragan, M.A., Bird, C.J., Rice, E.L., Gutell, R.R., Murphy, C.A. and Singh, R.A. (1994) A molecular phylogeny of the marine red algae (Rhodophyta) based on the nuclear small-subunit rRNA gene. Proc. Natl Acad. Sci. USA 91: 7276-7280.
40. Ral, J.-P., Derelle, E., Ferraz, C., Wattebled, F., Farinas, B., et al. (2004) Starch division and partitioning: a mechanism for granule propagation and maintenance in the picophytoplanktonic green alga Ostreococcus tauri. Plant Physiol. 136: 3333-3340.
41. Rodríguez-Ezpeleta, N., Brinkimann, H., Burey, S.C., Roure, B., Burger, G., Löffelhardt, W., Bohnert, H.J., Philippe, H. and Franz Lang, B. (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15: 1325-1330.
42. Sheath, R.G., Hellebust, J.A. and Sawa, T. (1981) Floridean starch metabolism of Porphyridium purpureum (Rhodophyta). III. Effects of darkness and metabolic inhibitors. Phycologia 20: 22-31.
43. Shimonaga, T., Fujiwara, S., Kaneko, M., Izumo, A., Nihei, S., Francisco, P.B., Jr., Satoh, A., Fujita, N., Nakamura, Y. and Tsuzuki, M. (2007) Variation in storage α-polyglucans of red algae: amylose- and amylopectin-types in Porphyridium and glycogen-type in Cyanidium. Mar. Biotechnol. 9: 192-202.
44. Starr, R.C. (1964) The culture collection of algae at Indiana University. Amer. J. Bot. 51: 1013-1044.
45. Stiller, J.W. and Hall, B.D. (1997) The origin of red algae: implication for plastid evolution. Proc. Natl Acad. Sci. USA 94: 4520-4525.
46. Sueoka, N., Chiang, K.S. and Kates, J.R. (1967) Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardtii. I. Isotopic transfer experiments with a strain producing eight zoospores. J. Mol. Biol. 25: 44-67.
47. Viola, R., Nyvall, P. and Pedersen, M. (2001) The unique features of starch metabolism in red algae. Proc. R. Soc. B: Biol. Sci. 268: 1417-1422.
48. Wakelin, J.H., Virgin, H.S. and Crystal, E. (1959) Development and comparison of two X-ray methods for determining the crystallinity of cotton cellulose. J. Appl. Phys. 30: 1654-1662.
49. Watanabe, M.M., Kasai, F. and Sudo, R. (1988) NIES-Collection List of Strains 2nd edn, Microalgae and Protozoa. Microbial Culture Collection, The National Institute for Environmental Studies, Tsukuba.
50. Yamaguchi, M., Kainuma, K. and French, D. (1979) Electron microscopic observations of waxy maize starch. J. Ultrastruct. Res. 69: 249-261.
51. Yoo, S.H., Spalding, M.H. and Jane, J.L. (2002) Characterization of cyanobacterial glycogen isolated from the wild type and from a mutant lacking of branching enzyme. Carbohydr. Res. 337: 2195-2203.
52. Yoon, H.S., Müller, K.M., Sheath, R.G., Ott, F.D. and Bhattacharya, D. (2006) Defining the major lineages of red algae (Rhodophyta). J. Phycol. 42: 482-492.
53. Yu, S., Blennow, A., Bojko, M., Madsen, F., Olsen, C.E. and Engelsen, S.B. (2002) Physico-chemical characterization of floridean starch of red algae. Starch/Stärke 54: 66-74.
54. Yu, S. and Pedersen, M. (1993) a-1,4-glucan lyase, new class of starch/ glycogen-debranching enzyme. II. Subcellular localization and partial amino-acid sequence. Planta 191: 137-142.