Characterization of cell wall polysaccharides of the coencocytic green seaweed bryopsis plumosa (bryopsidaceae, chlorophyta) from the argentine coast

Journal of Phycology

Volumn 48, Issue 2, 2012, Pages 326-335

  Ciancia, Marina ^a,e   Alberghina, Josefina ^a   Arata, Paula Ximena ^a   Benavides, Hugo ^b   Leliaert, Frederik ^c   Verbruggen, Heroen ^c   Estevez, Jose Manuel ^d,e  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INSTITUTO NACIONAL DE INVESTIGACIÓN Y DESARROLLO PESQUERO INIDEP   (Argentina)

^c GHENT UNIVERSITY   (Belgium)

^d INSTITUTO DE FISIOLOGÍA   (Argentina)

^e Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Bryopsis plumose; Cell wall; Green seaweed; Pyruvylated galactan sulfate; Sulfated polysaccharides

Indexed keywords

BRYOPSIDACEAE; BRYOPSIS; BRYOPSIS PLUMOSA; CAULERPALES; CHLOROPHYTA; CODIUM;

EID: 84859429050     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2012.01131.x     Document Type: Article

References (68)

1. Agardh, C. A. 1823. Species algarum rite cognitae, cum synonimus, differentiis specificis et descriptionibus succintis. I. (Fucoideae, Florideae, Ulvoideae). ex offcina Berlingiana, Greifwald, Lundae (Lund, Sweden), i+531 pp.
2. Ahmed, A. E. R. & Labavitch, J. M. 1977. A simplified method for accurate determination of cell wall uronide content. J. Food Biochem. 1:61-365.
3. Bilan, M. I., Vinogradova, E. V., Shashkov, A. S. & Usov, A. I. 2006. Isolation and preliminary characterization of a highly pyruvylated galactan from Codium yezoense (Bryopsidales, Chlorophyta). Bot. Mar. 49:259-62.
4. Bilan, M. I., Vinogradova, E. V., Shashkov, A. S. & Usov, A. I. 2007. Structure of a highly pyruvylated galactan sulfate from the pacific green alga Codium yezoense (Bryopsidales, Chlorophyta). Carbohydr. Res. 342:586-96.
5. Bock, K. & Pedersen, C. 1983. Carbon-13 nuclear magnetic resonance data for monosaccharides. Adv. Carbohydr. Chem. Biochem. 41:27-66.
6. Boraso de Zaixso, A. L. 2004. Marine Chlorophyta of Argentina. Hist. Nat. (Seg. Ser.) 3:95-119.
7. Cassolato, J. E. F., Noseda, M. D., Pujol, C. A., Pellizzari, F. M., Damonte, E. B. & Duarte, M. A. R. 2008. Chemical structure and antiviral activity of the sulfated heterorhamnan isolated from the green seaweed Gayralia oxysperma. Carbohydr. Res. 343:3085-95.
8. Chanzy, H. D., Grosrenaud, A., Vuong, R. & Mackie, W. 1984. The crystalline polymorphism of mannan in plant cell walls and after recrystallisation. Planta 161:320-9.
9. Chiovitti, A., Bacic, A., Craik, D. J., Munro, S. L. A., Kraft, G. T. & Liao, M.-L. 1997. Cell-wall polysaccharides from Australian red algae of the family Solieriaceae (Gigartinales, Rhodophyta): novel, highly pyruvated carrageenans from the genus Callophycus. Carbohydr. Res. 299:229-43.
10. Ciancia, M., Quintana, I., Vizcarguenaga, M. I., Kasulin, L., Dios, A., Estevez, J. M. & Cerezo, A. S. 2007. Polysaccharides from the green seaweeds Codium fragile and C. vermilara with controversial effects on hemostasis. Int. J. Biol. Macromol. 41:641-9.
11. Ciucanu, I. & Kerek, K. 1984. A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res. 134:209-17.
12. Coll Cunillera, J. F. 1976. Algas marinhas bentonicas do Uruguai. Thesis, Departamento de Botanica do Instituto de Biociencias de Universidad de Sao Paulo, Brasil, 191 pp.
13. Collins, F. S. 1928. The Green Algae of North America and Suppl. G. E. Stechert and Co., New York, 400 pp.
14. Dodgson, K. S. & Price, R. G. 1962. A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem. J. 84:106-10.
15. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. 1956. Colorimetric method of determination of sugars and related substances. Anal. Chem. 28:350-6.
16. Dunn, E. K., Shoue, D. A., Huang, X., Kline, R. E., MacKay, A. L., Carpita, N. C., Taylor, I. E. P. & Mandoli, D. F. 2007. Spectroscopic and biochemical analysis of regions of the cell wall of the unicellular 'mannan weed', Acetabularia acetabulum. Plant Cell Physiol. 48:122-33.
17. Estevez, J. M., Kasulin, L., Fernández, P. V., Dupree, P. & Ciancia, M. 2009. Chemical and in situ characterization of macromolecular components of the complex cell walls from the coencocytic green alga Codium fragile. Glycobiology 19:212-22.
18. Farias, E. H. C., Pomin, V. H., Valente, A. P., Nader, H. B., Rocha, H. A. O. & Mourao, P. A. S. 2008. A preponderantly 4-sulfated, 3-linked galactan from the green alga Codium isthmocladum. Glycobiology 18:250-9.
19. Feldmann, J. 1937. Les algues marines de la Cote des Alberes. I-III. Cyanophycées, Chlorophycées, Phaeophycées. Rev. Algol. 9:141-329 + lám.
20. Fernández, P. V., Ciancia, M. & Estevez, J. M. 2011. Cell wall variability in the green seaweed Codium vermilara (Bryopsidales, Chlorophyta) from the Argentine coast. J. Phycol. 48:802-10.
21. Fernández, P. V., Ciancia, M., Miravalles, A. B. & Estevez, J. M. 2010. Cell wall polymer mapping in the coenocytic macroalga Codium vermilara (Bryopsidales, Chlorophyta). J. Phycol. 46:556-65.
22. Filisetti-Cozzi, T. M. C. C. & Carpita, N. C. 1991. Measurement of uronic acids without interference from neutral sugars. Anal. Biochem. 197:157-62.
23. Flores, M. L., Cerezo, A. S. & Stortz, C. A. 2000. Studies on the skeletal cell wall of the cystocarpic stage of the red seaweeds Iridaea undulosa B. Part II. Fractionation of the cell wall and methylation analysis of the inner core-fibrillar polysaccharides. Int. J. Biol. Macromol. 27:21-7.
24. Fritsch, F. E. 1956. The Structure and Reproduction of the Algae I. Cambridge University Press, Cambridge, UK, 791 pp.
25. Fukushi, Y., Otsuru, O. & Maeda, M. 1988. The chemical structure of the D-xylan from the main cell wall constituents of Bryopsis maxima. Carbohydr. Res. 182:313-20.
26. Guiry, M. D. & Guiry, G. M. 2011. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. (accessed 8 June 2011).
27. Harvey, W. H. 1858. Nereis boreali-americana III. Chlorospermeae. Smithson. Contrib. Knowledge 10:1-140 14 pls.
28. Huizing, H. J. & Rietema, H. 1975. Xylan and mannan as cell wall constituents of different stages in the life-histories of some siphoneous green algae. Br. Phycol. J. 10:13-6.
29. Huizing, H. J., Rietema, H. & Sietsma, J. H. 1979. Cell wall constituents of several siphoneous green algae in relation to morphology and taxonomy. Br. Phycol. J. 14:25-32.
30. Kaihou, S., Hayashi, T., Otsuru, O. & Maeda, M. 1993. Studies on the cell-wall mannan of the siphonous green algae, Codium latum. Carbohydr. Res. 240:207-18.
31. Knutsen, S. H. & Grasdalen, H. 1987. Characterization of water extractable polysaccharides from Norwegian Furcellaria lumbricalis (Huds) Lamour. (Gigartinales, Rhodophyceae) by IR and NMR spectroscopy. Bot. Mar. 30:497-505.
32. Koepsell, H. J. & Sharpe, E. S. 1952. Microdetermination of pyruvic and α-ketoglutaric acids. Arch. Biochem. Biophys. 38:443-9.
33. Koster, J. 1941. Quelques observations sur les Bryopsis du Golfe de Naples. Blumea 4:225-358.
34. Krishnamurthy, K. V. 1999. Transmission electron microscopic cytochemistry. In Krishnamurthy, K. V. [Ed.] Methods in Cell Wall Cytochemistry. CRC Press, Boca Raton, Florida, pp. 177-226.
35. Lahaye, M. & Robic, A. 2007. Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765-74.
36. Lamb, D. W. & Zechman, F. W. 2006. Phylogenetic analyses of the Bryopsidales (Ulvophyceae, Chlorophyta) based on RUBISCO large subunit gene sequences. J. Phycol. 42:669-78.
37. Lourenço, S. O., Barberino, E., De-Paula, J. C., da S. Pereira, L. O. & Lanfer Marquez, U. M. 2002. Amino acid composition, protein content, and calculation of nitrogen-to-protein conversion factors for nineteen tropical seaweeds. Phycol. Res. 50:233-41.
38. Love, J. & Percival, E. 1964a. The polysaccharides of the green seaweed Codium fragile: part II. The water-soluble sulphated polysaccharides. J. Chem. Soc. 1964:3338-45.
39. Love, J. & Percival, E. 1964b. The polysaccharides of the green seaweed Codium fragile: part III. A β-1, 4-linked mannan. J. Chem. Soc. 1964:3345-50.
40. Lowry, O. H., Rosenbrough, N. J. & Farr, A. L. 1951. Protein measurements with the Folin phenol reagent. J. Biol. Chem. 193:265-75.
41. Luft, J. H. 1971. Ruthenium red and violet. I. Chemistry, purification, methods of use for electron microscopy and mechanism of action. Anat. Rec. 171:347-68.
42. Mackie, W. 1969. The degree of polymerization of xylan in the cell wall of the green seaweed Penicillus dumetosus. Carbohydr. Res. 9:247-9.
43. Mackie, I. M. & Percival, E. 1959. The constitution of xylan from the green seaweed Caulerpa filiformis. J. Chem. Soc. 1959:1151-6.
44. Maeda, M., Fukushi-Fujikura, Y. & Otsuru, O. 1990. Cellulose in the cell wall of the siphonous green alga, Bryopsis maxima. Carbohydr. Res. 201:91-9.
45. Mao, W.-J., Fang, F., Li, H.-Y., Qi, X.-H., Sun, H.-H., Chen, Y. & Guo, S.-D. 2008. Heparinoid-active two sulfated polysaccharides isolated from marine green algae Monostroma nitidum. Carbohyd. Polym. 74:834-9.
46. Mao, W., Li, H., Li, Y., Zhang, H., Qi, X., Sun, H., Chen, Y. & Guo, S. 2009. Chemical characteristic and anticoagulant activity of the sulfated polysaccharide isolated from Monostroma latissimum (Chlorophyta). Int. J. Biol. Macromol. 44:70-4.
47. Medlin, L. 1984. Short note on changes in the abundance and occurrence of six macroalgal species along the Texas coast of the Gulf of Mexico. Contrib. Mar. Sci. 27:85-91.
48. Morrison, I. M. 1988. Hydrolysis of plant cell walls with trifluoroacetic acid. Phytochemistry 27:1097-101.
49. Ohta, Y., Lee, J.-B., Hayashi, K. & Hayashi, T. 2009. Isolation of sulfated galactan from Codium fragile and its antiviral effect. Biol. Pharmacol. Bull. 32:892-8.
50. Olivier, S. R., Bastida, R. & Torti, M. 1970. Las comunidades bentónicas de los alrededores de Mar del Plata (Argentina). Actas IV Congreso Latinoamericano de Zoología (Caracas, Venezuela) 11:559-93.
51. Papenfuss, G. F. 1964. Problems in the taxonomy and geographical distribution of Antarctic marine algae. In Carrick, R., Holdgate, M. & Prevost, J. [Eds.] Biologie Antarctique. Hermann, Paris, pp. 155-60.
52. Parma, A., Pascual, M. & Sar, E. 1987. Clave para el reconocimiento de los géneros de algas macrofitas del intermareal rocoso bonaerense. Ser. Tec. Didáct. Mus. La Plata 15:1-27.
53. Percival, E. & McDowell, R. H. 1981. Algal walls. Composition and biosynthesis. In Tanner, W. & Loewus, F. A. [Eds.] Encyclopedia of Plant Physiology, 13B vol. Springer, Berlin, pp. 277-316.
54. 13C-n.m.r. spectroscopy of synthetic monosulphated methyl α-d-galactopyranosides. Carbohydr. Res. 179:411-8.
55. Sar, E., Pascual, M. & Parma, A. 1984. Consideraciones ecológicas sobre las algas del litoral rocoso bonaerense. Rev. Mus. La Plata (Nueva Ser.) Secc. Bot. 13:143-7.
56. Saunders, G. W. & Kucera, H. 2010. An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogam. Algol. 31:487-528.
57. Setchell, W. A. & Gardner, N. L. 1920. The marine algae of the Pacific coast of North America II. Chlorophyceae. Univ. Calif. Publ. Bot. 8:156-63.
58. Siddhanta, A. K., Shanmugam, M., Mody, K. H., Goswami, A. M. & Ramabat, B. K. 1999. Sulphated polysaccharides of Codium dwarkense Boergs. from the west coast of India: chemical composition and blood anticoagulant activity. Int. J. Biol. Macromol. 26:151-4.
59. Song, H., Zhang, Q., Zhang, Z. & Wang, J. 2010. In vitro antioxidant activity of polysaccharides extracted from Bryopsis plumosa. Carbohydr. Polym. 80:1057-61.
60. Stevenson, T. T. & Furneaux, R. H. 1991. Chemical methods for the analysis of sulphated galactans from red algae. Carbohydr. Res. 210:277-98.
61. Taylor, W. R. 1937. Marine Algae of Northeastern Coast of North America. University of Michigan Press, Ann Arbor, Michigan, 427 pp.
62. Verbruggen, H., Ashworth, M., LoDuca, S. T., Vlaeminck, C., Cocquyt, C., Sauvage, T., Zechman, F. W., et al. 2009a. A multi-locus time-calibrated phylogeny of the siphonous green algae. Mol. Phylogenet. Evol. 50:642-53.
63. Verbruggen, H., Leliaert, F., Maggs, C. A., Shimada, S., Schils, T., Provan, J., Booth, D., et al. 2007. Species boundaries and phylogenetic relationships within the green algal genus Codium (Bryopsidales) based on plastid DNA sequences. Mol. Phylogenet. Evol. 44:240-54.
64. Verbruggen, H., Tyberghein, L., Pauly, K., Vlaeminch, C., Van Nieuwenhuyze, K., Kooistra, W. H. C. F., Leliaert, F. & De Clerck, O. 2009b. Macroecology meets macroevolution: evolutionary niche dynamics in the seaweed Halimeda. Glob. Ecol. Biogeogr. 18:393-405.
65. Wutz, M. & Zetsche, K. 1976. Zur Biochimie und Regulation des Heteromorphen Generationswechsels der Grünalge. Planta 129:211-6.
66. Yale Dawson, E., Acleto y, C. & Foldvik, N. 1964. The seaweeds of Peru. Nova Hedwigia Beih. 13:1-111.
67. Yamagaki, T., Maeda, M., Kanazawa, K., Ishizuka, Y. & Nakanishi, H. 1997. Structural clarification of Caulerpa cell wall β-(1→3)-xylan by NMR spectroscopy. Biosci. Biotechnol. Biochem. 61:1077-80.
68. Zhang, H.-J., Mao, H.-J., Fang, F., Li, H.-Y., Sun, H.-H., Chen, Y. & Qi, X.-H. 2008. Chemical characteristics and anticoagulant activities of a sulfated polysaccharide and its fragments from Monostroma latissimum. Carbohydr. Polym. 71:428-34.