Planta

, Volume 243, Issue 2, pp 337–354 | Cite as

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

  • Sandra Cristina Raimundo
  • Utku Avci
  • Christina Hopper
  • Sivakumar Pattathil
  • Michael G. Hahn
  • Zoë A. Popper
Original Article

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.

Keywords

Brown seaweed Cell wall Galactans Glycome profiling Monoclonal antibodies 3-Linked glucan 

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

Notes

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.

Supplementary material

425_2015_2412_MOESM1_ESM.docx (21 kb)
Supplementary material 1 (DOCX 22 kb)

References

  1. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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
  4. 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 PubMedCrossRefGoogle Scholar
  5. Bold HC, Wynne MJ (1978) Introduction to the algae: structure and reproduction. Prentice-Hall biological sciences. Prentice-Hall Inc, New JerseyGoogle Scholar
  6. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  7. 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 PubMedCrossRefGoogle Scholar
  8. 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 PubMedCrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 PubMedCrossRefGoogle Scholar
  11. 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):529–535PubMedCrossRefGoogle Scholar
  12. 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 PubMedCrossRefGoogle Scholar
  13. 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
  14. 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 PubMedCrossRefGoogle Scholar
  15. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  16. 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 PubMedCrossRefGoogle Scholar
  17. 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
  18. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  19. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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):99–115PubMedCrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 PubMedCrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 PubMedCrossRefGoogle Scholar
  27. Farmer JB, Williams JL (1898) Contributions to our knowledge of the Fucaceae: their life-history and cytology. Philos Trans R Soc Ser B 190:623–645CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. Fry SC (2000) The growing plant cell wall: chemical and metabolic analysis. Blackburn Press, CaldwellGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. Graham LE, Wilcox LW (2000) Algae. Prentice Hall Inc, New YorkGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 PubMedCrossRefGoogle Scholar
  34. Haug A (1964) Composition and properties of alginates. Norwegian Institute of Technology, TrondheimGoogle Scholar
  35. 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 PubMedCrossRefGoogle Scholar
  36. 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 PubMedCrossRefGoogle Scholar
  37. 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):29–36Google Scholar
  38. 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 161:1117–1126PubMedCentralPubMedCrossRefGoogle Scholar
  39. Kloareg B (1984) Isolation and analysis of cell walls of the brown marine algae Pelvetia canaliculata and Ascophyllum nodosum. Physiol Veg 22(1):47–56Google Scholar
  40. Kloareg B, Quatrano RS (1988) Structure of cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315Google Scholar
  41. 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 PubMedCrossRefGoogle Scholar
  42. Kochert G (1978) Sexual pheromones in algae and fungi. Annu Rev Plant Physiol 29:461–486. doi: 10.1146/annurev.pp.29.060178.002333 CrossRefGoogle Scholar
  43. 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 PubMedCrossRefGoogle Scholar
  44. 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 CrossRefGoogle Scholar
  45. Lamport DTA (2013) Preparation of arabinogalactan glycoproteins from plant tissue. Bioprotocol 3(19):1–5Google Scholar
  46. 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 PubMedCrossRefGoogle Scholar
  47. Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytol 169(3):479–492PubMedCrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. Lee RE (2008) Phycology, 4th edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  51. 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 PubMedCrossRefGoogle Scholar
  52. Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13(8):1671–1695. doi: 10.3390/molecules13081671 PubMedCrossRefGoogle Scholar
  53. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  56. McCully ME (1968) Histological studies on the genus Fucus II. Histology of the reproductive tissues. Protoplasma 66(1–2):205–230CrossRefGoogle Scholar
  57. 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 263–281Google Scholar
  58. 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 PubMedCrossRefGoogle Scholar
  59. 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):1–9PubMedCrossRefGoogle Scholar
  60. 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 PubMedCrossRefGoogle Scholar
  61. Mian AJ, Percival E (1973) Carbohydrates of the brown seaweeds Himanthalia lorea, Bifurcaria bifurcata, and Padina pavonia. Carbohydr Res 26(1):133–146CrossRefGoogle Scholar
  62. 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 PubMedCrossRefGoogle Scholar
  63. Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11(3):266–277. doi: 10.1016/j.pbi.2008.03.006 PubMedCrossRefGoogle Scholar
  64. 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 PubMedCrossRefGoogle Scholar
  65. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  66. 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
  67. 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 PubMedCrossRefGoogle Scholar
  68. 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):635–641Google Scholar
  69. 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;2Google Scholar
  70. 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):21770–21776PubMedGoogle Scholar
  71. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. 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 PubMedCrossRefGoogle Scholar
  74. 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 CrossRefGoogle Scholar
  75. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  76. 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 PubMedCrossRefGoogle Scholar
  77. 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 245–254CrossRefGoogle Scholar
  78. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  79. 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 PubMedCrossRefGoogle Scholar
  80. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  81. Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648PubMedCrossRefGoogle Scholar
  82. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  83. 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 101:804–811PubMedCrossRefGoogle Scholar
  84. 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 CrossRefGoogle Scholar
  85. 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 PubMedCrossRefGoogle Scholar
  86. 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 PubMedCrossRefGoogle Scholar
  87. 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 PubMedCrossRefGoogle Scholar
  88. 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
  89. Team RDC (2011) A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  90. 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):340–346PubMedCentralPubMedCrossRefGoogle Scholar
  91. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  92. Usov AI, Bilan MI (2009) Fucoidans—sulfated polysaccharides of brown algae. Russ Chem Rev 78(8):785–799CrossRefGoogle Scholar
  93. 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 PubMedCrossRefGoogle Scholar
  94. 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 PubMedCrossRefGoogle Scholar
  95. 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 PubMedCrossRefGoogle Scholar
  96. 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 CrossRefGoogle Scholar
  97. 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 CrossRefGoogle Scholar
  98. 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 PubMedCrossRefGoogle Scholar
  99. 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 CrossRefGoogle Scholar
  100. 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 CrossRefGoogle Scholar
  101. Yariv J, Rapport MM, Graf L (1962) The interaction of glycosides and saccharides with antibody to the corresponding phenylazo glycosides. Biochem J 35:383–388CrossRefGoogle Scholar
  102. Yariv J, Lis H, Katchalski E (1967) Precipitation of arabic acid and some polysaccharides by glycosylphenylazo dyes. Biochem J 105(1):1C–2CPubMedCentralPubMedCrossRefGoogle Scholar
  103. 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 PubMedCrossRefGoogle Scholar
  104. 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 CrossRefGoogle Scholar
  105. 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 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Sandra Cristina Raimundo
    • 1
    • 2
  • Utku Avci
    • 2
  • Christina Hopper
    • 2
  • Sivakumar Pattathil
    • 2
  • Michael G. Hahn
    • 2
  • Zoë A. Popper
    • 1
  1. 1.Botany and Plant Science and Ryan Institute for Environmental, Marine and Energy Research, School of Natural SciencesNational University of Ireland GalwayGalwayIreland
  2. 2.Complex Carbohydrate Research CenterUniversity of GeorgiaAthensUSA

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