Abstract
LAMP is a cell wall-directed monoclonal antibody (mAb) that recognizes a β-(1,3)-glucan epitope. It has primarily been used in the immunolocalization of callose in vascular plant cell wall research. It was generated against a brown seaweed storage polysaccharide, laminarin, although it has not often been applied in algal research. We conducted in vitro (glycome profiling of cell wall extracts) and in situ (immunolabeling of sections) studies on the brown seaweeds Fucus vesiculosus (Fucales) and Laminaria digitata (Laminariales). Although glycome profiling did not give a positive signal with the LAMP mAb, this antibody clearly detected the presence of the β-(1,3)-glucan in situ, showing that this epitope is a constituent of these brown algal cell walls. In F. vesiculosus, the β-(1,3)-glucan epitope was present throughout the cell walls in all thallus parts; in L. digitata, the epitope was restricted to the sieve plates of the conductive elements. The sieve plate walls also stained with aniline blue, a fluorochrome used as a probe for callose. Enzymatic digestion with an endo-β-(1,3)-glucanase removed the ability of the LAMP mAb to label the cell walls. Thus, β-(1,3)-glucans are structural polysaccharides of F. vesiculosus cell walls and are integral components of the sieve plates in these brown seaweeds, reminiscent of plant callose.
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Abbreviations
- AIR:
-
Alcohol insoluble residue
- CCRC:
-
Complex Carbohydrate Research Center
- ELISA:
-
Enzyme-linked immunosorbent assay
- FCSPs:
-
Fucose-containing sulfated polysaccharides
- Fuc:
-
Fucose
- Gal:
-
Galactose
- Glc:
-
Glucose
- GulA:
-
Guluronic acid
- KPBS:
-
Potassium phosphate buffered saline
- mAb:
-
Monoclonal antibody
- Man:
-
Mannose
- ManA:
-
Mannuronic acid
- PBST:
-
Phosphate buffered saline tween
- TEM:
-
Transmission electron microscopy
- TMB:
-
3,3′,5,5′-Tetramethylbenzidine
- Xyl:
-
Xylose
References
Ale MT, Mikkelsen JD, Meyer AS (2011) Important determinants for fucoidan bioactivity: a critical review of structure-function relations and extraction methods for fucose-containing sulfated polysaccharides from brown seaweeds. Mar Drugs 9(10):2106–2130. doi:10.3390/md9102106
Altaner CM, Tokareva EN, Jarvis MC, Harris PJ (2010) Distribution of (1→4)-β-galactans, arabinogalactan proteins, xylans and (1→3)-β-glucans in tracheid cell walls of softwoods. Tree Physiol 30(6):782–793. doi:10.1093/treephys/tpq021
Aspinall GO, Kessler G (1957) The structure of callose from the grape vine. J Soc Chem Ind Lond 1957:1296
Audibert L, Fauchon M, Blanc N, Hauchard D, Gall EA (2010) Phenolic compounds in the brown seaweed Ascophyllum nodosum: distribution and radical-scavenging activities. Phytochem Anal 21:399–405. doi:10.1002/pca.1210
Avci U, Pattathil S, Hahn MG (2012) Immunological approaches to plant cell wall biomass characterization: immunolocalization of glycan epitopes. In: Himmel ME (ed) Biomass conversion: methods and protocols, vol 908. Methods in molecular biology. Humana, pp 73–82. doi:10.1007/978-1-61779-956-3_7
Baldauf SL (2008) An overview of the phylogeny and diversity of eukaryotes. J Syst Evol 46(3):263–273. doi:10.3724/SP.J.1002.2008.08060
Baurain D, Brinkmann H, Petersen J, Rodríguez-Ezpeleta N, Stechmann A, Demoulin V, Roger AJ, Burger G, Lang BF, Philippe H (2010) Phylogenetic evidence for separate acquisition of plastids in Cryptophytes, Haptophytes, and Stramenopiles. Mol Biol Evol 27(7):1698–1709. doi:10.1093/molbev/msq059
Beattie A, Hirst EL, Percival E (1961) Studies on the metabolism of the Chrysophyceae. Comparative structural investigations on leucosin (chrysolaminarin) separated from diatoms and laminarin from the brown algae. Biochem J 79:531–537
Bold HC, Wynne MJ (1978) Introduction to the algae: structure and reproduction. Prentice-Hall biological sciences. Prentice-Hall, New Jersey
Charrier B, Le Bail A, Reviers B (2012) Plant Proteus: brown algal morphological plasticity and underlying developmental mechanisms. Trends Plant Sci 17(8):468–477. doi:10.1016/j.tplants.2012.03.003
Chevolot L, Mulloy B, Ratiskol J, Foucault A, Colliec-Jouault S (2001) A disaccharide repeat unit is the major structure in fucoidans from two species of brown algae. Carbohydr Res 330(4):529–535. doi:10.1016/S0008-6215(00)00314-1
Chowdhury J, Henderson M, Schweizer P, Burton RA, Fincher GB, Little A (2014) Differential accumulation of callose, arabinoxylan and cellulose in nonpenetrated versus penetrated papillae on leaves of barley infected with Blumeria graminis f. sp. hordei. New Phytol 204:650–660. doi:10.1111/nph.12974
Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury J-M, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collén J, Corre E, Silva C, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, Gachon CMM, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Küpper FC, Lang D, Le Bail A, Leblanc C, Lerouge P, Lohr M, Lopez PJ, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli CA, Nelson DR, Nyvall-Collén P, Peters AF, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing SA, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder DC, Ségurens B, Strittmatter M, Tonon T, Tregear JW, Valentin K, Von Dassow P, Yamagishi T, Van de Peer Y, Wincker P (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621. doi:10.1038/nature09016
Coelho SM, Scornet D, Rousvoal S, Peters NT, Dartevelle L, Peters AF, Cock JM (2012) Ectocarpus: a model organism for the brown algae. Cold Spring Harb Protoc 2012(2):193–198. doi:10.1101/pdb.emo065821
Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG (2007) Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot 58(15–16):4027–4035. doi:10.1093/jxb/erm259
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(6):1203–1216. doi:10.1093/aob/mcu096
Domozych DS (2012) The quest for a four-dimensional imaging in plant cell biology: it’s just a matter of time. Ann Bot 110(2):461–474. doi:10.1093/aob/mcs107
Domozych DS, Lambiasse L (2009) Cell-wall development and bipolar growth in the desmid Penium margaritaceum (Zygnematophyceae, Streptophyta). Asymmetry in a symmetric world. J Phycol 45(4):879–893. doi:10.1111/j.1529-8817.2009.00713.x
Domozych DS, Serfis A, Kiemle SN, Gretz MR (2007) The structure and biochemistry of charophycean cell walls: I. Pectins of Penium margaritaceum. Protoplasma 230(1–2):99–115. doi:10.1007/s00709-006-0197-8
Domozych DS, Brechka H, Britton A, Toso M (2011) Cell wall growth and modulation dynamics in a model unicellular green alga—Penium margaritaceum: live cell labeling with monoclonal antibodies. J Bot 2011:1–8. doi:10.1155/2011/632165, Article ID 632165
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356
Enquist-Newman M, Faust AM, Bravo DD, Santos CN, Raisner RM, Hanel A, Sarvabhowman P, Le C, Regitsky DD, Cooper SR, Peereboom L, Clark A, Martinez Y, Goldsmith J, Cho MY, Donohoue PD, Luo L, Lamberson B, Tamrakar P, Kim EJ, Villari JL, Gill A, Tripathi SA, Karamchedu P, Paredes CJ, Rajgarhia V, Kotlar HK, Bailey RB, Miller DJ, Ohler NL, Swimmer C, Yoshikuni Y (2014) Efficient ethanol production from brown macroalgae sugars by a specific yeast platform. Nature 505(7482):239–243. doi:10.1038/nature12771
Estevez JM, Leonardi PI, Alberghina JS (2008) Cell wall carbohydrate epitopes in the green alga Oedogonium bharuchae F. minor (Oedogoniales, Chlorophyta). J Phycol 44(5):1257–1268. doi:10.1111/j.1529-8817.2008.00568.x
Estevez JM, Fernández PV, Kasulin L, Dupree P, Ciancia M (2009) Chemical and in situ characterization of macromolecular components of the cell walls from the green seaweed Codium fragile. Glycobiology 19(3):212–228. doi:10.1093/glycob/cwn101
Evans NA, Hoyne PA, Stone BA (1984) Characteristics and specificity of the interaction of a fluorochrome from aniline blue (sirofluor) with polysaccharides. Carbohydr Res 4(3):215–230. doi:10.1016/0144-8617(84)90012-2
Falter C, Zwikowics C, Eggert D, Blümke A, Naumann M, Wolff K, Ellinger D, Reimer R, Voigt CA (2015) Glucanocellulosic ethanol: the undiscovered biofuel potential in energy crops and marine biomass. Scie Rep 5:13722. doi:10.1038/srep13722
Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206(3):452–460. doi:10.1007/s004250050421
Fernández PV, Ciancia M, Miravalles AB, Estevez JM (2010) Cell-wall polymer mapping in the coenocytic macroalga Codium vermilara (Bryopsidales, Chlorophyta). J Phycol 46(3):456–465. doi:10.1111/j.1529-8817.2010.00821.x
Geitmann A, Hudák J, Vennigerholz F, Walles B (1995) Immunogold localization of pectin and callose in pollen grains and pollen tubes of Brugmansia suaveolens—implications for the self-incompatibility reaction. J Plant Physiol 147(2):225–235. doi:10.1016/S0176-1617(11)81509-9
Graham LE, Wilcox LW (2000) Algae. Prentice Hall, New York
Green JR, Stafford CJ, Jones JL, Wright PJ, Callow JA (1993) Binding of monoclonal antibodies to vegetative tissue and fucose-containing polysaccharides of Fucus serratus L. New Phytol 124(3):397–408. doi:10.1111/j.1469-8137.1993.tb03830.x
Guibet M, Boulenguer P, Mazoyer J, Kervarec N, Antonopoulos A, Lafosse M, Helbert W (2008) Composition and distribution of carrabiose moieties in hybrid k-/i-carrageenans using carrageenases. Biomacromolecules 9(1):408–415. doi:10.1021/bm701109r
Haug A (1964) Composition and properties of alginates. Norwegian Institute of Technology, Trondheim
Herburger K, Holzinger A (2015) Localization and quantification of callose in the streptophyte green algae Zygnema and Klebsormidium: correlation with desiccation tolerance. Plant Cell Physiol 56(11):2259–2270. doi:10.1093/pcp/pcv139
Hibberd DJ, Norris RE (1984) Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta Divisio Nova, Chlorarachniophyceae Classis Nova). J Phycol 20(2):310–330. doi:10.1111/j.0022-3646.1984.00310.x
Humbel BM, Konomi M, Takagi T, Kamasawa N, Ishijima SA, Osumi M (2001) In situ localization of β-glucans in the cell wall of Schizosaccharomyces pombe. Yeast 18:433–444
Jones JL, Callow JA, Green JR (1988) Monoclonal antibodies to sperm surface antigens of the brown alga Fucus serratus exhibit region-, gamete-, species- and genus-preferentical binding. Planta 176(3):298–306. doi:10.1007/BF00395410
Kadam SU, O’Donnel CP, Rai DK, Hossain MB, Burgess CM, Walsh D, Tiwari BK (2015) Laminarin from Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborea: ultrasound assisted extraction, characterization and bioactivity. Mar Drugs 13:4270–4280. doi:10.3390/md13074270
Kauss H (1989) Fluorometric measurement of callose and other 1,3-β-glucans. p127–136. In: Linskens HF, Jackson JF (eds) Plant fibers. Modern methods of plant analysis. New series, vol 10. Springer Press, Berlin
Kauss H (1996) Callose synthesis. In: Smallwood M, Knox JP, Bowles DJ (eds) Membranes: specialized functions in plants. BIOS Scientific Publishers, Guildford, pp 77–92
Kim D-S, Park Y-H (1985) Uronic acid composition, block structure and some related properties of alginic acid (3) on alginic acid prepared from Sargassum ringgoldianum. J Korean Fish Soc 18(1):29–36
Kloareg B, Quatrano RS (1988) Structure of cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315
Knoblauch J, Drobnitch TS, Peters WS, Knoblauch M (2016) In situ-microscopy reveals reversible cell wall swelling in kelp sieve tubes: one mechanism for turgor generation and flow control? Plant Cell Environ 39(8):1727–1736. doi:10.1111/pce.12736
Knox JP (1997) The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int Rev Cytol 171:79–120. doi:10.1016/S0074-7696(08)62586-3
Knox JP, Benitez-Alfonso Y (2014) Roles and regulation of plant cell walls surrounding plasmodesmata. Curr Opin Plant Biol 22:93–100. doi:10.1016/j.pbi.2014.09.009
Kropf DL, Kloareg B, Quatrano RS (1988) Cell wall is required for fixation of the embryonic axis in Fucus zygotes. Science 239(4836):187–190. doi:10.1126/science.3336780
Lahaye M, Jegou D, Buleon A (1994) Chemical characteristics of insoluble glucans from the cell wall of the marine green alga Ulva lactuca (L.) Thuret. Carbohydr Res 262(1):115–125. doi:10.1016/0008-6215(94)84008-3
Lechat H, Amat M, Mazoyer J, Buléon A, Lahaye M (2000) Structure and distribution of glucomannan and sulfated glucan in the cell walls of the red alga Kappaphycus alvarezii (Gigartinales, Rhodophyta). J Phycol 36(5):891–902. doi:10.1046/j.1529-8817.2000.00056.x
Lee RE (2008) Phycology, 4th edn. Cambridge University Press, Cambridge
Lee KJD, Marcus SE, Knox JP (2011) Cell wall biology: perspectives from cell wall imaging. Mol Plant 4(2):212–219. doi:10.1093/mp/ssq075
Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13(8):1671–1695. doi:10.3390/molecules13081671
Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge
Ludwig M, Gibbs SP (1989) Evidence that the nucleomorphs of Chlorarachnion reptans (Chlorarachniophyceae) are vestigial nuclei: morphology, division and DNA-DAPI fluorescence. J Phycol 25(2):385–394. doi:10.1111/j.1529-8817.1989.tb00135.x
Mabeau S, Kloareg B (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(9):1573–1580. doi:10.1093/jxb/38.9.1573
Masuko T, Minami A, Iwasaki N, Majima T, Nishimura S-I, Lee YC (2005) Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal Biochem 339(1):69–72. doi:10.1016/j.ab.2004.12.001
McCully ME (1965) A note on the structure of the cell walls of the brown alga Fucus. Can J Bot 43(8):1001–1004. doi:10.1139/b65-114
McCully ME, Goff LJ, Adshead PC (1980) Preparation of algae for light microscopy. In: Gantt E (ed) Handbook of phycological methods: developmental and cytological methods. Cambridge University Press, Cambridge, pp 263–281
McFadden GI, Gilson PR, Hofmann CJB, Adcock GJ, Maier UG (1994) Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc Natl Acad Sci U S A 91(9):3690–3694
McFadden GI, Gilson PR, Sims IM (1997) Preliminary characterization of carbohydrate stores from chlorarachniophytes (Division: Chlorarachniophyta). Phycol Res 45(3):145–151. doi:10.1111/j.1440-1835.1997.tb00087.x
Meikle PJ, Bonig I, Hoogenraad NJ, Clarke AE, Stone BA (1991) The location of (1→3)-β-glucans in the walls of pollen tubes of Nicotiana alata using a (1→3)-β-glucan-specific monoclonal antibody. Planta 185(1):1–8. doi:10.1007/BF00194507
Meikle PJ, Hoogenraad NJ, Bonig I, Clarke AE, Stone BA (1994) A (1→3, 1→4)-β-glucan-specific monoclonal antibody and its use in the quantification and immunocytochemical location of (1→3, 1→4)-β-glucans. Plant J 5(1):1–9. doi:10.1046/j.1365-313X.1994.5010001.x
Mian AJ, Percival E (1973) Carbohydrates of the brown seaweeds Himanthalia lorea, Bifurcaria bifurcata, and Padina pavonia. Carbohydr Res 26(1):133–146
Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010a) The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol 188(1):82–97. doi:10.1111/j.1469-8137.2010.03374.x
Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010b) Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol 188(1):67–81. doi:10.1111/j.1469-8137.2010.03345.x
Moller I, Sørensen I, Bernal AJ, Blaukopf C, Lee K, Øbro J, Pettolino F, Roberts A, Mikkelsen JD, Knox JP, Bacic A, Willats WGT (2007) High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J 50(6):1118–1128. doi:10.1111/j.1365-313X.2007.03114.x
Moller I, Marcus SE, Haeger A, Verhertbruggen Y, Verhoef R, Schols H, Ulvskov P, Mikkelsen JD, Knox JP, Willats W (2008) High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchical clustering of their carbohydrate microarray binding profiles. Glycoconj J 25(1):37–48. doi:10.1007/s10719-007-9059-7
Moller IE, Pettolino FA, Hart C, Lampugnani ER, Willats WGT, Bacic A (2012) Glycan profiling of plant cell wall polymers using microarrays. J Vis Exp 70(e4238):1–9. doi:10.3791/4238
Mollet J-C, Leroux C, Dardelle F, Lehner A (2013) Cell wall composition, biosynthesis and remodeling during pollen tube growth. Plants 2(1):107–147. doi:10.3390/plants2010107
Moss BL (1983) Sieve elements in the Fucales. New Phytol 93(3):433–437
Naylor GL, Russel-Wells B (1934) On the presence of cellulose and its distribution in the cell-walls of brown and red algae. Ann Bot 48(3):635–641
Niklas KJ (2004) The cell walls that bind the tree of life. Bioscience 54(9):831–841. doi:10.1641/0006-3568(2004)054[0831:TCWTBT]2.0.CO;2
Nitschke U, Stengel DB (2015) A new HPLC method for the detection of iodine applied to natural samples of edible seaweeds and commercial seaweed food products. Food Chem 172:326–334. doi:10.1016/j.foodchem.2014.09.030
Nitschke U, Dixneuf S, Ruth AA, Schmid M, Stengel DB (2013) Molecular iodine (I2) emission from two Laminaria species (Phaeophyceae) and impact of irradiance and temperature on I2 emission into air and iodide release into seawater from Laminaria digitata. Mar Environ Res 92:102–109. doi:10.1016/j.marenvres.2013.09.006
Norton TA, Melkonian M, Andersen RA (1996) Algal biodiversity. Phycologica 35(4):308–326. doi:10.2216/i0031-8884-35-4-308.1
Novotny AM, Forman M (1975) The composition and development of cell walls of Fucus embryos. Planta 122:67–78
Park EP, Díaz-Moreno SM, Davis DJ, Wilkop TE, Bulone V, Drakakaki G (2015) Endosidin 7 specifically arrests late cytokinesis and inhibits callose biosynthesis, revealing distinct trafficking events during cell plate maturation. Plant Physiol 165(3):1019–1034. doi:10.1104/pp.114.241497
Patankar MS, Oehninger S, Barnett T, Williams RL, Clark GF (1993) A revised structure for fucoidan may explain some of its biological activities. J Biol Chem 268(29):21770–21776
Pattathil S, Avci U, Baldwin D, Swennes AG, McGill JA, Popper Z, Booten T, Albert A, Davis RH, Chennareddy C, Dong R, O’Shea B, Rossi R, Leoff C, Freshour G, Narra R, O’Neill M, York WS, Hahn MG (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153(2):514–525. doi:10.1104/pp.109.151985
Pattathil S, Avci U, Miller JS, Hahn MG (2012) Immunological approaches to plant cell wall and biomass characterization: glycome profiling. In: Himmel ME (ed) Biomass conversion: methods and protocols, vol 908. Methods in molecular biology. Humana, pp 61–72. doi:10.1007/978-1-61779-956-3_6
Pattathil S, Avci U, Zhang T, Cardenas CL, Hahn MG (2015) Immunological approaches to biomass characterization and utilization. Front Bioeng Biotechnol 3:173. doi:10.3389/fbioe.2015.00173
Patterson DJ (1999) The diversity of Eukaryotes. Am Nat 154(S4):S96–S124. doi:10.1086/303287
Pennington W (1937) The secondary thickening of Fucus. New Phytol 36:267–279
Percival E (1979) The polysaccharides of green, red and brown seaweeds—their basic structure, biosynthesis and function. Br Phycol J 14(2):103–117. doi:10.1080/00071617900650121
Popper ZA, Michel G, Hervé C, Domozych DS, Willats WGT, Tuohy MG, Kloareg B, Stengel DB (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62:567–590. doi:10.1146/annurev-arplant-042110-103809
Quatrano RS, Stevens PT (1976) Cell wall assembly in Fucus zygotes. I. Characterization of the polysaccharide components. Plant Physiol 58(2):224–231. doi:10.1104/pp.58.2.224
Rabanal M, Ponce NMA, Navarro DA, Gómez RM, Stortz CA (2014) The system of fucoidans from the brown seaweed Dictyota dichotoma: chemical analysis and antiviral activity. Carbohydr Polym 101:804–811. doi:10.1016/j.carbpol.2013.10.019
Radford JE, Vesk M, Overall RL (1998) Callose deposition in plasmodesmata. Protoplasma 201(1–2):30–37. doi:10.1007/BF01280708
Raimundo SC, Avci U, Hopper C, Pattathil S, Hahn MG, Popper ZA (2016) Immunolocalization of cell wall carbohydrate epitopes in seaweeds: presence of land plant epitopes in Fucus vesiculosus L. (Phaeophyceae). Planta 243(2):337–354. doi:10.1007/s00425-015-2412-3
Read SM, Currie G, Bacic A (1996) Analysis of the structural heterogeneity of laminarin by electrospray-ionisation-mass spectrometry. Carbohydr Res 281(2):187–201. doi:10.1016/0008-6215(95)00350-9
Rioux L-E, Turgeon SL, Beaulieu M (2007) Characterization of polysaccharides extracted from brown seaweeds. Carbohydr Polym 69(3):530–537. doi:10.1016/j.carbpol.2007.01.009
Ropartz D, Giuliani A, Hervé C, Geairon A, Jam M, Czjzek M, Rogniaux H (2015) High-energy photon activation tandem mass spectrometry provides unprecedented insights into the structure of highly sulfated oligosaccharides extracted from macroalgal cell walls. Anal Chem 87(2):1042–1049. doi:10.1021/ac5036007
Schaal G, Leclerc J-C, Droual G, Leroux C, Riera P (2016) Biodiversity and trophic structure of invertebrate assemblages associated with understorey red algae in a Laminaria digitata bed. Mar Biol Res 12(5):513–523. doi:10.1080/17451000.2016.1164318
Schiel DR, Foster MS (2006) The population biology of large brown seaweeds: ecological consequences of multiphase life histories in dynamic coastal environments. Annu Rev Ecol Evol Syst 37:343–372. doi:10.1146/annurev.ecolsys.37.091305.110251
Schmitz K, Lobban CS (1976) A survey of translocation in Laminariales (Phaeophyceae). Mar Biol 36(3):207–216
Schmitz K, Srivastava LM (1976) The fine structure of sieve elements of Nereocystis lütkeana. Am J Bot 63(5):679–693
Schoenwaelder MEA (2008) The biology of phenolic containing vesicles. Algae 23(3):163–175
Schultze K, Janke K, Krüß A, Weidemann W (1990) The macrofauna and macroflora associated with Laminaria digitata and L. hyperborea at the island of Helgoland (German Bight, North Sea). Helgoländer Meeresunters 44:39–51
Smidsrød O, Glover RM, Whittington SG (1973) The relative extension of alginates having different chemical composition. Carbohydr Res 27:107–118
Smith AI (1939) The comparative histology of some of the Laminariales. Am J Bot 26(8):571–585
Smith MM, McCully ME (1978) A critical evaluation of the specificity of aniline blue induced fluorescence. Protoplasma 95:229–254
Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotechnol Adv 29(5):483–501. doi:10.1016/j.biotechadv.2011.05.016
Stiller JW, Huang J, Ding Q, Tian J, Goodwillie C (2009) Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genomics 10(484):1–16. doi:10.1186/1471-2164-10-484
Stone BA (2009) Chemistry of β-glucans. In: Bacic A, Fincher GB, Stone BA (eds) Chemistry, biochemistry, and biology of (1–3)-β-glucans and related polysaccharides. Academic, San Diego, pp 5–46. doi:10.1016/B978-0-12-373971-1.00002-9
Stone BA, Clarke AE (1992) Chemistry and physiology of higher plant (1,3)-β-glucans (callose). In: Stone BA, Clark A (eds) Chemistry and biology of (1,3)-β-glucans. La Trobe University Press, Bundoora, pp 365–429
Stone BA, Evans NA, Bonig I, Clarke AE (1984) The application of Sirofluor, a chemically defined fluorochrome from aniline blue for the histochemical detection of callose. Protoplasma 122(3):191–195. doi:10.1007/BF01281696
Suzuki E, Suzuki R (2013) Variations of storage polysaccharides in phototrophic microorganisms. J Appl Glycosci 60:21–27. doi:10.5458/jag.jag.JAG-2012_016
Sykes MG (1908) Anatomy and histology of Macrocystis pyrifera and Laminaria saccharina. Ann Bot 22(2):291–325
Tanaka A, Nagasato C, Uwai S, Motomura T, Kawai H (2007) Re-examination of ultrastructure of the stellate chloroplast organization in brown algae: structure and development of pyrenoids. Phycol Res 55(3):203–213. doi:10.1111/j.1440-1835.2007.00463.x
Team RDC (2011) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Tesson B, Charrier B (2014) Brown algal morphogenesis: atomic force microscopy as a tool to study the role of mechanical forces. Front Plant Sci 5(471):1–7. doi:10.3389/fpls.2014.00471
Torode TA, Marcus SE, Jam M, Tonon T, Blackburn RS, Hervé C, Knox JP (2015) Monoclonal antibodies directed to fucoidan preparations from brown algae. PLoS One 10(2):e0118366. doi:10.1371/journal.pone.0118366
Tsirigoti A, Beakes GW, Hervé C, Gachon CMM, Katsaros C (2015) Attachment, penetration and early host defense mechanisms during the infection of filamentous brown algae by Eurychasma dicksonii. Protoplasma 252(3):845–856. doi:10.1007/s00709-014-0721-1
Usov AI, Bilan MI (2009) Fucoidans—sulfated polysaccharides of brown algae. Russ Chem Rev 78(8):785–799
Van Went JL, Tammes PML (1973) Trumpet filaments in Laminaria digitata as an artefact. Acta Bot Neerlandica 22(2):112–119
Van Went JL, Van Aelst AC, Tammes PML (1973) Open plasmodesmata in sieve plates of Laminaria digitata. Acta Bot Neerlandica 22(2):120–123
Vreeland V (1970) Localization of a cell wall polysaccharide in a brown alga with labeled antibody. J Histochem Cytochem 18(5):371–373. doi:10.1177/18.5.371
Vreeland V (1972) Immunocytochemical localization of the extracellular polysaccharide alginic acid in the brown seaweed, Fucus distichus. J Histochem Cytochem 20(5):358–367. doi:10.1177/20.5.358
Vreeland V, Slomich M, Laetsch WM (1984) Monoclonal antibodies as molecular probes for cell wall antigens of the brown alga, Fucus. Planta 162(6):506–517. doi:10.1007/BF00399916
Vreeland V, Zablackis E, Laetsch WM (1992) Monoclonal antibodies as molecular markers for the intracellular and cell wall distribution of carrageenan epitopes in Kappaphycus (Rhodophyta) during tissue development. J Phycol 28(3):328–342. doi:10.1111/j.0022-3646.1992.00328.x
Wargacki AJ, Leonard E, Win MN, Regitsky DD, Santos CNS, Kim PB, Cooper SR, Raisner RM, Herman A, Sivitz AB, Lakshmanaswamy A, Kashiyama Y, Baker D, Yoshikuni Y (2012) An engineered microbial platform for direct biofuel production from brown macroalgae. Science 335(6066):308–313. doi:10.1126/science.1214547
Willats WGT, Steele-King CG, McCartney L, Orfila C, Marcus SE, Knox JP (2000) Making and using antibody probes to study plant cell walls. Plant Physiol Biochem 38(1–2):27–36. doi:10.1016/S0981-9428(00)00170-4
Wood PJ, Fulcher RG (1984) Specific interaction of aniline blue with (1→3)-β-d-glucan. Carbohydr Polym 4(1):49–72. doi:10.1016/0144-8617(84)90044-4
Xie B, Wang X, Zhu M, Zhang Z, Hong Z (2011) CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant J 65(1):1–14. doi:10.1111/j.1365-313X.2010.04399.x
Yamaguchi T, Ikawa T, Nisizawa K (1966) Incorporation of radioactive carbon from H14CO3 − into sugar constituents by a brown alga, Eisenia bicyclis, during photosynthesis and its fate in the dark. Plant Cell Physiol 7(2):217–229
Yamanouchi S (1908) Sieve tubes in Laminariales. Bot Gaz 46(2):153–154
Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic Eukaryotes. Mol Biol Evol 21(5):809–818. doi:10.1093/molbev/msh075
Zavaliev R, Ueki S, Epel B, Citovsky V (2011) Biology of callose (β-1,3-glucan) turnover at plasmodesmata. Protoplasma 248(1):117–130. doi:10.1007/s00709-010-0247-0
Zhao D, Zhuo RX, Cheng SX (2012) Alginate modified nanostructured calcium carbonate with enhanced delivery efficiency for gene and drug delivery. Mol BioSyst 8(3):753–759. doi:10.1039/c1mb05337j
Acknowledgments
The authors thankfully acknowledge the technical support provided by Professor David Domozych (Skidmore Microscopy Imaging Center, Skidmore College) with the TEM and by Dr. Kerry Thompson (Center for Microscopy and Imaging, NUI Galway) with the aniline blue imaging. The authors thank Prof. Azeddine Driouich (Center for Plant Glycobiology, Université de Rouen, France) and Dr. Maria Tuohy (Biochemistry, NUI Galway) for helpful comments during the preparation of this manuscript. The financial support was provided by the Science Foundation Ireland (SFI) (Research Frontiers Programme, grant 11/RFP/EOB/3345 awarded to Z.A.P). The generation of the CCRC series of mAbs was supported by the US National Science Foundation Plant Genome Program (Awards DBI-0421683 and IOB-0923992 to M.G.H.).
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Raimundo, S.C., Pattathil, S., Eberhard, S. et al. β-1,3-Glucans are components of brown seaweed (Phaeophyceae) cell walls. Protoplasma 254, 997–1016 (2017). https://doi.org/10.1007/s00709-016-1007-6
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DOI: https://doi.org/10.1007/s00709-016-1007-6