Planta

, Volume 236, Issue 4, pp 1013–1026 | Cite as

Ultrastructural study of plasmodesmata in the brown alga Dictyota dichotoma (Dictyotales, Phaeophyceae)

  • Makoto Terauchi
  • Chikako Nagasato
  • Naoko Kajimura
  • Yoshinobu Mineyuki
  • Kazuo Okuda
  • Christos Katsaros
  • Taizo Motomura
Original Article

Abstract

Plasmodesmata are intercellular bridges that directly connect the cytoplasm of neighboring cells and play a crucial role in cell-to-cell communication and cell development in multicellular plants. Although brown algae (Phaeophyceae, Heterokontophyta) are phylogenetically distant to land plants, they nevertheless possess a complex multicellular organization that includes plasmodesmata. In this study, the ultrastructure and formation of plasmodesmata in the brown alga Dictyota dichotoma were studied using transmission electron microscopy and electron tomography with rapid freezing and freeze substitution. D. dichotoma possesses plasma membrane-lined, simple plasmodesmata without internal endoplasmic reticulum (desmotubule). This structure differs from those in land plants. Plasmodesmata were clustered in regions with thin cell walls and formed pit fields. Fine proteinaceous “internal bridges” were observed in the cavity. Ultrastructural observations of cytokinesis in D. dichotoma showed that plasmodesmata formation began at an early stage of cell division with the formation of tubular pre-plasmodesmata within membranous sacs of the cytokinetic diaphragm. Clusters of pre-plasmodesmata formed the future pit field. As cytokinesis proceeded, electron-dense material extended from the outer surface of the mid region of the pre-plasmodesmata and finally formed the nascent cell wall. From these results, we suggest that pre-plasmodesmata are associated with cell wall development during cytokinesis in D. dichotoma.

Keywords

Brown algae Cell wall Cytokinesis Dictyota dichotoma Electron tomography Pit field Plasmodesmata 

Abbreviations

PD

Plasmodesmata

ER

Endoplasmic reticulum

PPD

Pre-plasmodesmata

TEM

Transmission electron microscopy

References

  1. Badelt K, White RG, Overall RL, Vesk M (1994) Ultrastructural specializations of the cell-wall sleeve around plasmodesmata. Am J Bot 81:1422–1427CrossRefGoogle Scholar
  2. Bisalputra T (1966) Electron microscopic study of the protoplasmic continuity in certain brown algae. Can J Bot 44:89–93CrossRefGoogle Scholar
  3. Blackman LM, Overall RL (1998) Immunolocalisation of the cytoskeleton to plasmodesmata of Chara corallina. Plant J 14:733–741CrossRefGoogle Scholar
  4. Botha CEJ, Cross RHM (2000) Towards reconciliation of structure with function in plasmodesmata—who is the gatekeeper? Micron 31:713–721PubMedCrossRefGoogle Scholar
  5. Botha CEJ, Hartley BJ, Cross RHM (1993) The ultrastructure and computer-enhanced digital image analysis of plasmodesmata at the kranz mesophyll-bundle sheath interface of Themeda triandra var. imberbis (Retz) A. Camus in conventionally-fixed blades. Ann Bot 72:255–261CrossRefGoogle Scholar
  6. Carrington JC, Kasschau KD, Mahajan SK, Schaad MC (1996) Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8:1669–1681PubMedGoogle Scholar
  7. 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 47:53–60CrossRefGoogle Scholar
  8. Citovsky V (1993) Probing plasmodesmatal transport with plant viruses. Plant Physiol 102:1071–1076PubMedGoogle Scholar
  9. Cook ME, Graham LE, Botha CEJ, Lavin CA (1997) Comparative ultrastructure of plasmodesmata of Chara and selected bryophytes: toward an elucidation of the evolutionary origin of plant plasmodesmata. Am J Bot 84:1169–1178PubMedCrossRefGoogle Scholar
  10. Ding B, Haudenshield JS, Hull RJ, Wolf S, Beachy RN, Lucas WJ (1992a) Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell 4:915–928PubMedGoogle Scholar
  11. Ding B, Turgeon R, Parthasarathy MV (1992b) Substructure of freeze-substituted plasmodesmata. Protoplasma 169:28–41CrossRefGoogle Scholar
  12. Ehlers K, Kollmann R (2001) Primary and secondary plasmodesmata: structure, origin, and functioning. Protoplasma 216:1–30PubMedCrossRefGoogle Scholar
  13. Epel BL (2009) Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host β-1, 3-glucanases. Semin Cell Dev Biol 20:1074–1081PubMedCrossRefGoogle Scholar
  14. Faulkner C, Maule A (2010) Opportunities and successes in the search for plasmodesmal proteins. Protoplasma 248:27–38PubMedCrossRefGoogle Scholar
  15. Faulkner CR, Blackman LM, Cordwell SJ, Overall RL (2005) Proteomic identification of putative plasmodesmatal proteins from Chara corallina. Proteomics 5:2866–2875PubMedCrossRefGoogle Scholar
  16. Faulkner C, Akman OE, Bell K, Jefree C, Oparka KJ (2008) Peeking into pit fields: a multiple twinning model of secondary plasmodesmata formation. Plant Cell 20:1504–1508PubMedCrossRefGoogle Scholar
  17. Fernandez-Calvino L, Faulkner C, Walshaw J, Saalbach G, Bayer E, Benitez-Alfonso Y, Maule A (2011) Arabidopsis plasmodesmal proteome. PLoS One 6:1–13Google Scholar
  18. Franceschi VR, Ding B, Lucas WJ (1994) Mechanism of plasmodesmata formation in characean algae in relation to evolution of intercellular communication in higher plants. Planta 192:347–358CrossRefGoogle Scholar
  19. Fraster TW, Gunning BES (1969) The ultrastructure of plasmodesmata in the filamentous green alga, Bulbochaete hiloensis (Nordst.) Tiffany. Planta 88:244–254CrossRefGoogle Scholar
  20. Gestel KV, Slegers H, von Witsch M, Samaj J, Baluska F, Verbelen JP (2003) Immunological evidence for the presence of plant homologues of the actin related protein Arp3 in tobacco and maize: subcellular localization to actin-enriched pit fields and emerging root hairs. Protoplasma 222:45–52PubMedCrossRefGoogle Scholar
  21. Haas TJ, Otegui MS (2007) Electron tomography in plant cell biology. J Integr Plant Biol 49:1091–1099CrossRefGoogle Scholar
  22. Hepler PK (1982) Endoplasmic reticulum in formation of the cell plate and plasmodesmata. Protoplasma 111:121–123CrossRefGoogle Scholar
  23. Jo Y, Cho WK, Rim Y, Moon J, Chen XY, Chu H, Kim CY, Park ZY, Lucas WJ, Kim JY (2011) Plasmodesmal receptor-like kinases identified through analysis of rice cell wall extracted proteins. Protoplasma 248:191–203PubMedCrossRefGoogle Scholar
  24. Katsaros C, Galatis B (1985) Ultrastructural studies on thallus development in Dictyota dichotoma (Phaeophyta, Dictyotales). Eur J Phycol 20:263–276CrossRefGoogle Scholar
  25. Katsaros C, Galatis B (1988) Thallus development in Dictyopteris membranacea (Phaeophyta, Dictyotales). Br Phycol J 23:71–88CrossRefGoogle Scholar
  26. Katsaros C, Motomura T, Nagasato C, Galatis B (2009) Diaphragm development in cytokinetic vegetative cells of brown algae. Bot Mar 52:150–161CrossRefGoogle Scholar
  27. Kim JY (2005) Regulation of short-distance transport of RNA and protein. Curr Opin Plant Biol 8:45–52PubMedCrossRefGoogle Scholar
  28. 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 26:259–315Google Scholar
  29. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71–76PubMedCrossRefGoogle Scholar
  30. Kumar NM, Gilula NB (1996) The gap junction review communication channel. Cell 84:381–388PubMedCrossRefGoogle Scholar
  31. Kwiatkowska M, Maszewski J (1986) Changes in the occurrence and ultrastructure of plasmodesmata in antheridia of Chara vulgaris L. during different stages of spermatogenesis. Protoplasma 132:179–188CrossRefGoogle Scholar
  32. La Claire JW II (1981) Occurrence of plasmodesmata during infurrowing in a brown alga. Biol Cell 40:139–142Google Scholar
  33. Lough TJ, Shash K, Xoconostle-Cázares B, Hofstra KR, Beck DL, Balmori E, Forster RLS, Lucas WJ (1998) Molecular dissection of the mechanism by which Potexvirus triple gene block proteins mediate cell-to-cell transport of infectious RNA. MPMI 11:801–814CrossRefGoogle Scholar
  34. Lucas WJ, Wolf S (1993) Plasmodesmata: the intercellular organelles of green plants. Trends Cell Biol 3:308–315PubMedCrossRefGoogle Scholar
  35. Lucas WJ, Ding B, van den Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol 12:435–476CrossRefGoogle Scholar
  36. Makowski L, Caspar DL, Phillips WC, Baker TS, Goodenough DA (1984) Gap junction structures. VI. Variation and conservation in connexon conformation and packing. Biophys J 45:208–218PubMedCrossRefGoogle Scholar
  37. Marchant HJ (1976) Plasmodesmata in algae and fungi. In: Gunning BES, Robards TAW (eds) Intercellular communication in plants: studies on plasmodesmata. Springer, Berlin, pp 59–80CrossRefGoogle Scholar
  38. Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120:343–352PubMedCrossRefGoogle Scholar
  39. Maule AJ (2008) Plasmodesmata: structure, function and biogenesis. Curr Opin Plant Biol 11:680–686PubMedCrossRefGoogle Scholar
  40. Nagasato C, Motomura T (2002) Ultrastructural study on mitosis and cytokinesis in Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae) by freeze-substitution. Protoplasma 219:140–149PubMedCrossRefGoogle Scholar
  41. 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 45:404–412CrossRefGoogle Scholar
  42. 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 232:287–298PubMedCrossRefGoogle Scholar
  43. Otegui MS, Staehelin LA (2004) Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 218:501–515PubMedCrossRefGoogle Scholar
  44. Overall RL, Blackman LM (1996) A model of the macromolecular structure of plasmodesmata. Trends Plant Sci 1:307–311Google Scholar
  45. Pickett-Heaps JD (1967) Ultrastructure and differentiation in Chara sp. II. Mitosis. Aust J Biol Sci 20:883–894Google Scholar
  46. Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Proc. US Japan Conf. Hakone, Jap. Soc. Plant Physiol., pp 63–75Google Scholar
  47. Pueschel CM (1977) A freeze-etch study of the ultrastructure of red algal pit plugs. Protoplasma 91:15–30CrossRefGoogle Scholar
  48. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212PubMedCrossRefGoogle Scholar
  49. Robards AW (1968) A new interpretation of plasmodesmatal ultrastructure. Planta 82:200–210CrossRefGoogle Scholar
  50. Robards AW, Lucas WJ (1990) Plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 41:369–419CrossRefGoogle Scholar
  51. Sagi G, Katz A, Gelbart DG, Epel BL (2005) Class 1 reversibly glycosylated polypeptides are plasmodesmal-associated proteins delivered to plasmodesmata via the Golgi apparatus. Plant Cell 17:1788–1800PubMedCrossRefGoogle Scholar
  52. Samuels AL, Giddings TH, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357PubMedCrossRefGoogle Scholar
  53. Sato T (1968) Lead citrate stain in electron microscopy. J Electron Microsc 17:158–159Google Scholar
  54. Schmitz K (1981) Translocation. In: Lobban CS, Wynne MJ (eds) The biology of seaweeds. Blackwell Scientific Publications, Oxford, pp 534–558Google Scholar
  55. Schmitz K (1990) Algae. In: Behnke HD, Sjolund RD (eds) Sieve elements. Comparative structure, induction and development. Springer, Berlin, pp 1–18Google Scholar
  56. Schmitz K, Kuhn R (1982) Fine structure, distribution and frequency of plasmodesmata and pits in the cortex of Laminaria hyperborea and L. saccharina. Planta 154:385–392CrossRefGoogle Scholar
  57. Schmitz K, Srivastava L (1974) Fine structure and development of sieve tubes in Laminaria groenlandica Rosenv. Cytobiologie 10:66–87Google Scholar
  58. Schmitz K, Srivastava L (1975) On the fine structure of sieve tubes and the physiology of assimilate transport in Alaria marginata. Can J Bot 53:861–876CrossRefGoogle Scholar
  59. Schmitz K, Srivastava LM (1976) The fine structure of sieve elements of Nereocystis lutkeana. Am J Bot 63:679–693CrossRefGoogle Scholar
  60. Schoenwaelder MEA, Clayton MN (1999) The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161–166CrossRefGoogle Scholar
  61. Schopfer CR, Hepler PK (1991) Distribution of membranes and the cytoskeleton during cell plate formation in pollen mother cells of Tradescantia. J Cell Sci 100:717–728Google Scholar
  62. Scott J, Thomas J, Saunders B (1988) Primary pit connections in Compsopogon coeruleus (Balbis) Montagne (Compsopogonales, Rhodophyta). Phycologia 27:327–333CrossRefGoogle Scholar
  63. Segui-Simarro JM, Austin JR II, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16:836–856PubMedCrossRefGoogle Scholar
  64. Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ (2009) An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell 21:581–594PubMedCrossRefGoogle Scholar
  65. Staehelin LA, Hepler PK (1996) Cytokinesis in higher plants. Cell 84:821–824PubMedCrossRefGoogle Scholar
  66. Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol 6:180–190CrossRefGoogle Scholar
  67. Ueki C, Nagasto C, Motomura T, Saga N (2008) Reexamination of the pit plugs and the characteristic membranous structures in Porphyra yezoensis (Bangiales, Rhodophyta). Phycologia 47:5–11CrossRefGoogle Scholar
  68. Volk GM, Turgeon R, Beebe DU (1996) Secondary plasmodesmata formation in the minor-vein phloem of Cucumis melo L. and Cucurbita pepo L. Planta 199:425–432CrossRefGoogle Scholar
  69. White RG, Badelt K, Overall RL, Vesk M (1994) Actin associated with plasmodesmata. Protoplasma 180:169–184CrossRefGoogle Scholar
  70. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Makoto Terauchi
    • 1
    • 2
  • Chikako Nagasato
    • 2
  • Naoko Kajimura
    • 3
  • Yoshinobu Mineyuki
    • 4
  • Kazuo Okuda
    • 5
  • Christos Katsaros
    • 6
  • Taizo Motomura
    • 2
  1. 1.Graduate School of Environmental ScienceHokkaido UniversitySapporoJapan
  2. 2.Muroran Marine Station, Field Science Center for Northern BiosphereHokkaido UniversityMuroranJapan
  3. 3.Research Center for Ultra-High Voltage Electron MicroscopyOsaka UniversityOsakaJapan
  4. 4.Department of Life Science, Graduate School of Life ScienceUniversity of HyogoHimejiJapan
  5. 5.Graduate School of Kuroshio ScienceKochi UniversityKochiJapan
  6. 6.Department of Botany, Faculty of BiologyUniversity of AthensAthensGreece

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