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Immunolocalization of cell wall carbohydrate epitopes in seaweeds: presence of land plant epitopes in Fucus vesiculosus L. (Phaeophyceae)

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Abstract

Main conclusion

Land plant cell wall glycan epitopes are present in Fucus vesiculosus. RG-I/AG mAbs recognize distinct glycan epitopes in structurally different galactans, and 3-linked glucans are also present in the cell walls.

Cell wall-directed monoclonal antibodies (mAbs) have given increased knowledge of fundamental land plant processes but are not extensively used to study seaweeds. We profiled the brown seaweed Fucus vesiculosus glycome employing 155 mAbs that recognize predominantly vascular plant cell wall glycan components. The resulting profile was used to inform in situ labeling studies. Several of the mAbs recognized and bound to epitopes present in different thallus parts of Fucus vesiculosus. Antibodies recognizing arabinogalactan epitopes were divided into four groups based on their immunolocalization patterns. Group 1 bound to the stipe, blade, and receptacles. Group 2 bound to the antheridia, oogonia and paraphyses. Group 3 recognized antheridia cell walls and Group 4 localized on the antheridia inner wall and oogonia mesochite. This study reveals that epitopes present in vascular plant cell walls are also present in brown seaweeds. Furthermore, the diverse in situ localization patterns of the RG-I/AG clade mAbs suggest that these mAbs likely detect distinct epitopes present in structurally different galactans. In addition, 3-linked glucans were also detected throughout the cell walls of the algal tissues, using the β-glucan-directed LAMP mAb. Our results give insights into cell wall evolution, and diversify the available tools for the study of brown seaweed cell walls.

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Abbreviations

AG-3:

Arabinogalactan-3

AGP:

Arabinogalactan protein

AIR:

Alcohol insoluble residue

Ara:

Arabinose

ELISA:

Enzyme-linked immunosorbent assay

FCSPs:

Fucose-containing sulphated polysaccharides

Fuc:

Fucose

Gal:

Galactose

GC/MS:

Gas chromatography/mass spectrometry

Glc:

Glucose

GulA:

Guluronic acid

KPBS:

Potassium phosphate buffered saline

mAb:

Monoclonal antibody

Man:

Mannose

ManA:

Mannuronic acid

RG-I:

Rhamnogalacturonan I

RG-I/AG:

Rhamnogalacturonan I/arabinogalactan

TMB:

3,3′,5,5′-Tetramethylbenzidine

TMS:

Per-O-trimethylsilyl

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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. Methods in molecular biology, vol 908. Humana Press, New York, pp 73–82. doi:10.1007/978-1-61779-956-3_7

    Chapter  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bold HC, Wynne MJ (1978) Introduction to the algae: structure and reproduction. Prentice-Hall biological sciences. Prentice-Hall Inc, New Jersey

    Google Scholar 

  • Buckeridge MS (2010) Seed cell wall storage polysaccharides: models to understand cell wall biosynthesis and degradation. Plant Physiol 154(3):1017–1023. doi:10.1104/pp.110.158642

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344(14):1879–1900. doi:10.1016/j.carres.2009.05.021

    Article  CAS  PubMed  Google Scholar 

  • Cardozo KHM, Guaratini T, Barros MP, Falcão VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E (2007) Metabolites from algae with economical impact. Comp Biochem Physiol C Toxicol Pharmacol 146(1–2):60–78. doi:10.1016/j.cbpc.2006.05.007

    Article  PubMed  CAS  Google Scholar 

  • Carpita NC (1984) Fractionation of hemicelluloses from maize cell walls with increasing concentrations of alkali. Phytochemistry 23(5):1089–1093. doi:10.1016/S0031-9422(00)82615-1

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury J-M, Badger JH, Beszteri B et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621. doi:10.1038/nature09016

    Article  CAS  PubMed  Google Scholar 

  • 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 2:193–198. doi:10.1101/pdb.emo065821

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Coimbra S, Costa M, Jones B, Mendes MA, Pereira LG (2009) Pollen grain development is compromised in Arabidopsis agp6agp11 null mutants. J Exp Bot 60(11):3133–3142. doi:10.1093/jxb/erp148

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Coimbra S, Costa ML, Mendes MA, Pereira AM, Pinto J, Pereira LG (2010) Early germination of Arabidopsis pollen in a double null mutant for the arabinogalactan protein genes AGP6 and AGP11. Sex Plant Reprod 23(3):199–205. doi:10.1007/s00497-010-0136-x

    Article  CAS  PubMed  Google Scholar 

  • Conchie J, Percival EGV (1950) Fucoidin part II. The hydrolysis of a methylated fucoidin prepared from Fucus vesiculosus. J Chem Soc. doi:10.1039/JR9500000827

    Google Scholar 

  • Deniaud-Bouët E, Kervarec N, Michel G, Tonon T, Kloareg B, Hervé C (2014) Chemical and enzimatic 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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  CAS  Google Scholar 

  • Eardly DD, Sutton CW, Hempel WM, Reed DC, Ebeling AW (1990) Monoclonal antibodies specific for sulfated polysaccharides on the surface of Macrocystis pyrifera (Phaeophyceae). J Phycol 26(1):54–62. doi:10.1111/j.0022-3646.1990.00054.x

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Farmer JB, Williams JL (1898) Contributions to our knowledge of the Fucaceae: their life-history and cytology. Philos Trans R Soc Ser B 190:623–645

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fry SC (2000) The growing plant cell wall: chemical and metabolic analysis. Blackburn Press, Caldwell

    Google Scholar 

  • García-Ríos V, Ríos-Leal E, Robledo D, Freile-Pelegrin Y (2012) Polysaccharides composition from tropical brown seaweeds. Phycol Res 60(4):305–315. doi:10.1111/j.1440-1835.2012.00661.x

    Article  CAS  Google Scholar 

  • Graham LE, Wilcox LW (2000) Algae. Prentice Hall Inc, New York

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Haug A (1964) Composition and properties of alginates. Norwegian Institute of Technology, Trondheim

    Google Scholar 

  • 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-preferential binding. Planta 176(3):298–306. doi:10.1007/BF00395410

    Article  CAS  PubMed  Google Scholar 

  • Jones JL, Callow JA, Green JR (1990) The molecular nature of Fucus serratus sperm surface antigens recognised by monoclonal antibodies FS1 to FS12. Planta 182(1):64–71. doi:10.1007/BF00239985

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kitazawa K, Tryfona T, Yoshimi Y, Hayashi Y, Kawauchi S, Antonov L, Tanaka H, Takahashi T, Kaneko S, Dupree P, Tsumuraya Y, Kotake T (2013) β-Galactosyl Yariv reagent binds to the β-1,3-galactan of arabinogalactan proteins. Plant Physiol 161:1117–1126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kloareg B (1984) Isolation and analysis of cell walls of the brown marine algae Pelvetia canaliculata and Ascophyllum nodosum. Physiol Veg 22(1):47–56

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kochert G (1978) Sexual pheromones in algae and fungi. Annu Rev Plant Physiol 29:461–486. doi:10.1146/annurev.pp.29.060178.002333

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lamport DTA (2013) Preparation of arabinogalactan glycoproteins from plant tissue. Bioprotocol 3(19):1–5

    Google Scholar 

  • Lamport DTA, Várnai P (2012) Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol 197(1):58–64. doi:10.1111/nph.12005

    Article  PubMed  CAS  Google Scholar 

  • Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytol 169(3):479–492

    Article  CAS  PubMed  Google Scholar 

  • Lau JM, McNeil M, Darvill AG, Albersheim P (1985) Structure of the backbone of rhamnogalacturonan I, a pectic polysaccharide in the primary cell walls of plants. Carbohydr Res 137:111–125. doi:10.1016/0008-6215(85)85153-3

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lee RE (2008) Phycology, 4th edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13(8):1671–1695. doi:10.3390/molecules13081671

    Article  CAS  PubMed  Google Scholar 

  • Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122(1):3–10. doi:10.1104/pp.122.1.3

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McCully ME (1968) Histological studies on the genus Fucus II. Histology of the reproductive tissues. Protoplasma 66(1–2):205–230

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Merkle RK, Poppe I (1994) Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry. Methods Enzymol 230:1–15. doi:10.1016/0076-6879(94)30003-8

    Article  CAS  PubMed  Google Scholar 

  • Mian AJ, Percival E (1973) Carbohydrates of the brown seaweeds Himanthalia lorea, Bifurcaria bifurcata, and Padina pavonia. Carbohydr Res 26(1):133–146

    Article  CAS  Google Scholar 

  • Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010) 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

    Article  CAS  PubMed  Google Scholar 

  • Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11(3):266–277. doi:10.1016/j.pbi.2008.03.006

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Müller DG, Gassmann G (1985) Sexual reproduction and the role of sperm attractants in monoecious species of the brown algae order Fucales (Fucus, Hesperophycus, Pelvetia and Pelvetiopsis). J Plant Physiol 118(5):401–408. doi:10.1016/S0176-1617(85)80200-5

    Article  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

  • 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

    CAS  PubMed  Google Scholar 

  • 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, O’Narra R, 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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. Methods in molecular biology, vol 908. Humana Press, New York, pp 61–72. doi:10.1007/978-1-61779-956-3_6

    Chapter  Google Scholar 

  • Pennell RI, Knox JP, Scofield GN, Selvendran RR, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108(5):1967–1977. doi:10.1083/jcb.108.5.1967

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pereira AM, Masiero S, Nobre MS, Costa ML, Solís M-T, Testillano PS, Sprunck S, Coimbra S (2014) Differential expression patterns of Arabinogalactan Proteins in Arabidopsis thaliana reproductive tissues. J Exp Bot 65(18):5459–5471. doi:10.1093/jxb/eru300

    Article  PubMed Central  PubMed  Google Scholar 

  • Popper ZA (2008) Evolution and diversity of green plant cell walls. Curr Opin Plant Biol 11(3):286–292. doi:10.1016/j.pbi.2008.02.012

    Article  CAS  PubMed  Google Scholar 

  • Popper ZA (2011) Extraction and detection of arabinogalactan proteins. In: Popper ZA (ed) The plant cell wall: methods and protocols. Methods in molecular biology, vol 715. Humana Press, Newyork, pp 245–254

    Chapter  Google Scholar 

  • Popper ZA, Tuohy MG (2010) Beyond the green: understanding the evolutionary puzzle of plant and algal cell walls. Plant Physiol 153(2):373–383. doi:10.1104/pp.110.158055

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill A, Hahn MG (1994) Generation of monoclonal antibodies against plant cell-wall polysaccharides. I. Characterization of a monoclonal antibody to a terminal α-(1 → 2)-linked fucosyl-containing epitope. Plant Physiol 104(2):699–710. doi:10.1104/pp.104.2.699

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161. doi:10.1146/annurev.arplant.58.032806.103801

    Article  CAS  PubMed  Google Scholar 

  • Steffan W, Kovác P, Albersheim P, Darvill A, Hahn MG (1995) Characterization of a monoclonal antibody that recognizes an arabinosylated (1,6)-β-d-galactan epitope in plant complex carbohydrates. Carbohydr Res 275(2):295–307. doi:10.1016/0008-6215(95)00174-R

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stiller JW, Huang J, Ding Q, Tian J, Goodwillie C (2009) Are algal genes in nonphotosynthetic protists evidence of historical plastid endosymbioses? BMC Genom. doi:10.1186/1471-2164-10-484

    Google Scholar 

  • Team RDC (2011) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Thornber JP, Northcote DH (1962) Changes in the chemical composition of a cambial cell during its differentiation into xylem and phloem tissues in trees. 3. Xylan, glucomannan and a-cellulose fractions. Biochem J 82(2):340–346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Usov AI, Bilan MI (2009) Fucoidans—sulfated polysaccharides of brown algae. Russ Chem Rev 78(8):785–799

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Vreeland V, Zablackis E, Doboszewski B, Laetsch WM (1987) Molecular markers for marine algal polysaccharides. Hydrobiologia 151–152(1):155–160. doi:10.1007/BF00046121

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wright PJ, Callow JA, Green JR (1995a) The Fucus (Phaeophyceae) sperm receptor for eggs. 2. Isolation of a binding-protein which partially activates eggs. J Phycol 31(4):592–600. doi:10.1111/j.1529-8817.1995.tb02555.x

    Article  CAS  Google Scholar 

  • Wright PJ, Green JR, Callow JA (1995b) The Fucus (Phaeophyceae) sperm receptor for egg. 1. Development and characteristics of a binding assay. J Phycol 31(4):584–591. doi:10.1111/j.1529-8817.1995.tb02554.x

    Article  Google Scholar 

  • Yariv J, Rapport MM, Graf L (1962) The interaction of glycosides and saccharides with antibody to the corresponding phenylazo glycosides. Biochem J 35:383–388

    Article  Google Scholar 

  • Yariv J, Lis H, Katchalski E (1967) Precipitation of arabic acid and some polysaccharides by glycosylphenylazo dyes. Biochem J 105(1):1C–2C

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • York WS, Darvill AG, Michael M, Stevenson TT, Albersheim P (1986) Isolation and characterization of plant cell walls and cell wall components. Methods Enzymol 118:3–40. doi:10.1016/0076-6879(86)18062-1

    Article  CAS  Google Scholar 

  • Zablackis E, Huang J, Müller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107(4):1129–1138. doi:10.1104/pp.107.4.1129

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The research presented in this manuscript is funded as part of 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 used in this work was supported by the US National Science Foundation Plant Genome Program (Awards DBI-0421683 and IOB-0923992 to M.G.H.). The monosaccharide composition analysis was supported by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, US Department of Energy (grant DE-FG02-93ER20097 to Parastoo Azadi) at the Complex Carbohydrate Research Center. The authors thank Dr Udo Nitschke (Botany and Plant Science, School of Natural Sciences, and Ryan Institute, NUI Galway) for helpful comments during the preparation of the manuscript.

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Authors and Affiliations

  1. Botany and Plant Science and Ryan Institute for Environmental, Marine and Energy Research, School of Natural Sciences, National University of Ireland Galway, Galway, Ireland

    Sandra Cristina Raimundo & Zoë A. Popper

  2. Complex Carbohydrate Research Center, University of Georgia, Athens, GA, 30602, USA

    Sandra Cristina Raimundo, Utku Avci, Christina Hopper, Sivakumar Pattathil & Michael G. Hahn

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  1. Sandra Cristina Raimundo
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  2. Utku Avci
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  3. Christina Hopper
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Correspondence to Sandra Cristina Raimundo.

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Raimundo, S.C., Avci, U., Hopper, C. et al. Immunolocalization of cell wall carbohydrate epitopes in seaweeds: presence of land plant epitopes in Fucus vesiculosus L. (Phaeophyceae). Planta 243, 337–354 (2016). https://doi.org/10.1007/s00425-015-2412-3

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