Abstract
Main conclusion
This work investigated a correlation between the three-dimensional architecture and compound–components of the brown algal cell wall. Calcium greatly contributes to the cell wall integrity.
Brown algae have a unique cell wall consisting of alginate, cellulose, and sulfated polysaccharides. However, the relationship between the architecture and the composition of the cell wall is poorly understood. Here, we investigated the architecture of the cell wall and the effect of extracellular calcium in the sporophyte and gametophyte of the model brown alga, Ectocarpus siliculosus (Dillwyn) Lyngbye, using transmission electron microscopy, histochemical, and immunohistochemical studies. The lateral cell wall of vegetative cells of the sporophyte thalli had multilayered architecture containing electron-dense and negatively stained fibrils. Electron tomographic analysis showed that the amount of the electron-dense fibrils and the junctions was different between inner and outer layers, and between the perpendicular and tangential directions of the cell wall. By immersing the gametophyte thalli in the low-calcium (one-eighth of the normal concentration) artificial seawater medium, the fibrous layers of the lateral cell wall of vegetative cells became swollen. Destruction of cell wall integrity was also induced by the addition of sorbitol. The results demonstrated that electron-dense fibrils were composed of alginate-calcium fibrous gels, and electron negatively stained fibrils were crystalline cellulose microfibrils. It was concluded that the spatial arrangement of electron-dense fibrils was different between the layers and between the directions of the cell wall, and calcium was necessary for maintaining the fibrous layers in the cell wall. This study provides insights into the design principle of the brown algal cell wall.
Similar content being viewed by others
References
Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with Image J. Biophotonics Int 11:36–42
Agrawal GK, Jwa NS, Lebrun MH, Job D, Rakwal R (2010) Plant secretome: unlocking secrets of the secreted proteins. Proteomics 10:799–827
Aithal A, Sharma A, Joshi S, Raghava GPS, Varshney GC (2012) PolysacDB: a database of microbial polysaccharide antigens and their antibodies. PLoS One 7:e34613. doi:10.1371/journal.pone.0034613
Albenne C, Canut H, Hoffmann L, Jamet E (2014) Plant cell wall proteins: a large body of data, but what about runaways? Proteomes 2:224–242
Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 21:203–222
Bisgrove SR, Kropf DL (2001) Cell wall deposition during morphogenesis in Fucoid algae. Planta 212:648–658
Burns AR, Oliveira L, Bisalputra T (1982) A histochemical study of bud initiation in the brown alga Sphacelaria furcigera. New Phytol 92:297–307
Callow ME, Coughlan SJ, Evans LV (1978) The role of Golgi bodies in polysaccharide sulphation in Fucus zygotes. J Cell Sci 32:337–356
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30
Chi E-S, Henry EC, Kawai H, Okuda K (1999) Immunogold-labeling analysis of alginate distributions in the cell walls of chromophyte algae. Phycol Res 47:53–60
Cronshaw J, Myers A, Preston RD (1958) A chemical and physical investigation of the cell walls of some marine algae. Biochim Biophys Acta 27:89–103
Deniaud-Bouët E, Kervarec N, Michel G, Tonon T, Kloareg B, Hervé C (2014) Chemical and enzymatic fractionation of cell walls from Fucales: insights into the structure of the extracellular matrix of brown algae. Ann Bot 114:1203–1216
Evans LV, Holligan MS (1972) Correlated light and electron microscope studies on brown algae I. Localization of alginic acid and sulfated polysaccharides in Dictyota. New Phytol 71:1161–1172
Fu G, Nagasato C, Ito T, Müller DG, Motomura T (2013) Ultrastructural analysis of flagellar development in plurilocular sporangia of Ectocarpus siliculosus (Phaeophyceae). Protoplasma 250:261–272
Fu G, Nagasato C, Oka S, Cock JM, Motomura T (2014) Proteomics analysis of heterogeneous flagella in brown algae (Stramenopiles). Protist 165:662–675
Gacesa P, Wusteman FS (1990) Plate assay for simultaneous detection of alginate lyases and determination of substrate specificity. Appl Environ Microbiol 56:2265–2267
Gschloessl B, Guermeur Y, Cock J (2008) HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinform 9:393
Haug A, Larsen B, Smidsrød O (1974) Uronic acid sequence in alginate from different sources. Carbohydr Res 32:217–225
Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155
Inoue A, Takadono K, Nishiyama R, Tajima K, Kobayashi T, Ojima T (2014) Characterization of an alginate lyase, FlAlyA, from Flavobacterium sp. strain UMI-01 and its expression in Escherichia coli. Mar Drugs 12:4693–4712
Katsaros C, Karyophyllis D, Galatis B (2002) Cortical F-actin underlies cellulose microfibril patterning in brown algal cells. Phycologia 41:178–183
Kloareg B, Mabeau S (1987) Isolation and analysis of the cell walls of brown algae: Fucus spiralis, F. ceranoides, F. vesiculosus, F. serratus, Bifurcaria bifurcata and Laminaria digitata. J Exp Bot 38:1573–1580
Kloareg B, Quatrano RS (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix of polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lynch MA, Staehelin LA (1992) Domain-specific and cell type-specific localization of two types of cell wall matrix polysaccharides in the clover root tip. J Cell Biol 118:467–479
Mariani P, Tolomio C, Braghetta P (1985) An ultrastructural approach to the adaptive role of the cell wall in the intertidal alga Fucus virsoides. Protoplasma 128:208–217
McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96:323–334
Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277
Morris VJ, Gromer A, Kirby AR (2009) Architecture of intracellular networks in plant matrices. Struct Chem 20:255–261
Nagasato C, Motomura T (2002) Ultrastructural study on mitosis and cytokinesis in Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae) by freeze substitution. Protoplasma 219:140–149
Nagasato C, Motomura T (2009) Effect of latrunculin B and brefeldin A on cytokinesis in the brown alga Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae). J Phycol 45:404–412
Nagasato C, Inoue A, Mizuno M, Kanazawa K, Ojima T, Okuda K, Motomura T (2010) Membrane fusion process and assembly of cell wall during cytokinesis in the brown alga, Silvetia babingtonii (Fucales, Phaeophyceae). Planta 232:287–298
Nagasato C, Kajimura N, Terauchi M, Mineyuki Y, Motomura T (2014) Electron tomographic analysis of cytokinesis in the brown alga Silvetia babingtonii (Fucales, Phaeophyceae). Protoplasma 251:1347–1357
Nakashima J, Mizuno T, Takabe K, Fujita M, Saiki H (1997) Direct visualization of lignifying secondary wall thickenings in Zinnia elegans cells in culture. Plant Cell Physiol 38:818–827
Novotny AM, Forman M (1974) The Relationship between changes in cell wall composition and the establishment of polarity in Fucus embryos. Dev Biol 40:162–173
Novotny AM, Forman M (1975) The composition and development of cell walls of Fucus embryos. Planta 122:67–78
Nyvall P, Corre E, Boisset C, Barbeyron T, Rousvoal S, Scornet D, Kloareg B, Boyen C (2003) Characterization of mannuronan C-5epimerase genes from the brown alga Laminaria digitata. Plant Physiol 133:726–735
Osborn M, Weber K (1982) Immunofluorescence and immunocytochemical procedures with affinity purified antibodies: tubulin-containing structures. In: Wilson L (ed) Methods in cell biology, vol 24. Academic Press, New York, pp 97–132
Parre E, Geitmann A (2005) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592
Picton JM, Steer MW (1983) Evidence for the role of Ca2+ ions in tip extension in pollen tubes. Protoplasma 115:11–17
Provasoli L (1963) Growing marine seaweeds. Proceedings of the 4th international Seaweed symposium. Pergamon Press, Oxford, pp 9–17
Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Japanese Society of Plant Physiologists, Hakone, pp 63–75
Quatrano RS, Stevens PT (1976) Cell wall assembly in Fucus zygotes. Plant Physiol 58:224–231
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Ruel K, Joseleau JP (1984) Use of enzyme-gold complexes for the ultrastructural localization of hemicelluloses in the plant cell wall. Histochemistry 81:573–580
Scheller HB, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289
Schoenwaelder MEA, Clayton MN (1999) The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161–166
Schüβler A, Hirn S, Katsaros C (2003) Cellulose synthesizing terminal complexes and morphogenesis in tip-growing cells of Syringoderma phinneyi (Phaeophyceae). Phycol Res 51:35–44
Spurr AR (1969) Low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Tamura H, Mine I, Okuda K (1996) Cellulose-synthesizing terminal complexes and microfibril structure in the brown alga Sphacelaria rigidula (Sphacelariales, Phaeophyceae). Phycol Res 44:63–68
Terauchi M, Nagasato C, Kajimura N, Mineyuki Y, Okuda K, Katsaros C, Motomura T (2012) Ultrastructural study of plasmodesmata in the brown alga Dictyota dichotoma (Dictyotales, Phaeophyceae). Planta 236:1013–1026
Wells B, McCann MC, Shedletzky E, Delmer D, Roberts K (1994) Structural features of cell walls from tomato cells adapted to grow on the herbicide 2,6 dichlorobenzonitrile. J Microsc 173:155–164
Wu X, Wang G, Fu X (2014) Variations in the chemical composition of Costaria costata during harvest. J Appl Phycol 26:2389–2396
Xu P, Donaldson LA, Gergely ZR, Staehelin LA (2007) Dual-axis electron tomography: a new approach for investigating the spatial organization of wood cellulose microfibrils. Wood Sci Technol 41:101–116
Acknowledgments
We express our thanks to Dr. K. Okuda, Kochi University, Japan, for providing the anti-alginate antibody, and Dr. S. Oka, Hokkaido University, Japan, for analysis with the LC-MS/MS. This study was supported by KAKENHI [Grant numbers 25291087, 26440160].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Terauchi, M., Nagasato, C., Inoue, A. et al. Distribution of alginate and cellulose and regulatory role of calcium in the cell wall of the brown alga Ectocarpus siliculosus (Ectocarpales, Phaeophyceae). Planta 244, 361–377 (2016). https://doi.org/10.1007/s00425-016-2516-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-016-2516-4