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Ultrastructural analysis of flagellar development in plurilocular sporangia of Ectocarpus siliculosus (Phaeophyceae)

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Abstract

Flagellar development in the plurilocular zoidangia of sporophytes of the brown alga Ectocarpus siliculosus was analyzed in detail using transmission electron microscopy and electron tomography. A series of cell divisions in the plurilocular zoidangia produced the spore-mother cells. In these cells, the centrioles differentiated into flagellar basal bodies with basal plates at their distal ends and attached to the plasma membrane. The plasma membrane formed a depression (flagellar pocket) into where the flagella elongated and in which variously sized vesicles and cytoplasmic fragments accumulated. The anterior and posterior flagella started elongating simultaneously, and the vesicles and cytoplasmic fragments in the flagellar pocket fused to the flagellar membranes. The two flagella (anterior and posterior) could be clearly distinguished from each other at the initial stage of their development by differences in length, diameter and the appendage flagellar rootlets. Flagella continued to elongate in the flagellar pocket and maintained their mutually parallel arrangement as the flagellar pocket gradually changed position. In mature zoids, the basal part of the posterior flagellum (paraflagellar body) characteristically became swollen and faced the eyespot region. Electron dense materials accumulated between the axoneme and the flagellar membrane, and crystallized materials could also be observed in the swollen region. Before liberation of the zoospores from the plurilocular zoidangia, mastigoneme attachment was restricted to the distal region of the anterior flagellum. Structures just below the flagellar membrane that connected to the mastigonemes were clearly visible by electron tomography.

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Abbreviations

TEM:

Transmission electron microscope

ET:

Electron tomography

MT:

Microtubule

EDM:

Electron-dense materials

CM:

Crystallized materials

References

  • Andersen RA (2004) Biology and systematics of heterokont and haptophyte algae. Am J Bot 91:1508–1522

    Article  PubMed  Google Scholar 

  • Baker JRJ, Evans LV (1973a) The ship-fouling alga Ectocarpus. I. Ultrastructure and cytochemistry of plurilocular reproductive stages. Protoplasma 77:1–13

    Article  CAS  Google Scholar 

  • Baker JRJ, Evans LV (1973b) The ship-fouling alga Ectocarpus. II. Ultrastructure of the unilocular reproductive stages. Protoplasma 77:181–189

    Article  Google Scholar 

  • Beech PL, Heimann K, Melkonian M (1991) Development of the flagellar apparatus during the cell cycle in unicellular algae. Protoplasma 164:23–37

    Article  Google Scholar 

  • Bouck GB (1969) Extracellular microtubules. The origin, structure, and attachment of flagellar hairs in Fucus and Ascophyllum antherozoids. J Cell Biol 40:446–460

    Article  PubMed  CAS  Google Scholar 

  • Bui KH, Pigino G, Ishikawa T (2011) Three-dimensional structural analysis of eukaryotic flagella/cilia by electron cryo-tomography. J Synchrotron Radiat 18:2–5

    Article  PubMed  CAS  Google Scholar 

  • Chang P, Stearns T (2000) δ-tubulin and ε-tubulin: two new human centrosomal tubulins reveal new aspects of centrosome structure and function. Nat Cell Biol 2:30–35

    Article  PubMed  CAS  Google Scholar 

  • Clayton MN (1989) Brown algae and chromophyte phylogeny. In: Green JC, Leadbeater BSC and Diver WL (eds) The chromophyte alge: problems and perspectives. Clarendon Press, Oxford. pp 229–254

  • Cock MJ, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury JM, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JHF, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collén J, Corre E, Silva CD, 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 J, Valentin L, Von Dassow P, Yamagishi T, Van de Peer Y, Wincker P (2010) The Ectocarpus genome and the independent evolution of multicellularity in the brown algae. Nature 465:617–621

    Article  PubMed  CAS  Google Scholar 

  • Cole DG, Snell WJ (2009) SnapShot: intraflagellar transport. Cell 137(4):784–784

    Article  PubMed  CAS  Google Scholar 

  • Coleman AW (1988) The autofluorescent flagellum: a new phylogenetic enigma. J Phycol 24:118–120

    Article  Google Scholar 

  • Fujita S, Iseki M, Yoshikawa S, Makino Y, Watanabe M, Motomura T, Kawai H, Murakami A (2005) Identification and characterization of a fluorescent flagellar protein from the brown alga Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae): a flavoprotein homologous to Old Yellow Enzyme. Eur J Phycol 40:159–167

    Article  CAS  Google Scholar 

  • Geller A, Müller DG (1981) Analysis of the flagellar beat pattern of male Ectocarpus siliculosus gametes (Phaeophyta) in relation to chemotactic stimulation by female cells. J Exp Biol 92:53–66

    Google Scholar 

  • Green JC, Leadbeater BSC and Diver WL (1989) The chromophyte algae: problems and perspectives. Oxford Science Publications, Oxford. p. 429

  • Henry EC, Cole KM (1982a) Ultrastructure of swarmers in the Laminariales (Phaeophyceae). I. Zoospores. J Phycol 18:550–569

    Article  Google Scholar 

  • Henry EC, Cole KM (1982b) Ultrastructure of swarmers in the Laminariales (Phaeophyceae). II. Sperms. J Phycol 18:550–569

    Article  Google Scholar 

  • Hoyer-Fender S (2010) Centriole maturation and transformation to basal body. Semin Cell Dev Biol 21(2):142–147

    Article  PubMed  Google Scholar 

  • Kawai H (1988) A flavin-like autofluorescent substance in the posterior flagellum of golden and brown algae. J Phycol 24:114–117

    Article  Google Scholar 

  • Kawai H (1992) Green flagellar autofluorescence in brown algal swarmers and their phototactic responses. Bot Mag Tokyo 105:171–184

    Article  Google Scholar 

  • Kawai H, Inouye I (1989) Flagellar autofluorescence in forty four chlorophyll c-containing algae. J Phycol 28:222–227

    Article  Google Scholar 

  • Kremer J, Mastronarde DN (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71–76

    Article  PubMed  CAS  Google Scholar 

  • La Claire JW II, West JA (1978) Light and electron microscopic studies of growth and reproduction in Cutleria (Phaeophyta). I. Gametogenesis in the female plant of C. hancockii. Protoplasma 97:93–110

    Article  Google Scholar 

  • La Claire JW II, West JA (1979) Light and electron microscopic studies of growth and reproduction in Cutleria (Phaeophyta). II. Gametogenesis in the male plant of C. hancockii. Protoplasma 97:93–110

    Article  Google Scholar 

  • Lacomble S, Vaughan S, Gadelha C, Morphew MK, Shaw MK, McIntosh JR, Gull K (2009) Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. J Cell Sci 122:1081–1090

    Article  PubMed  CAS  Google Scholar 

  • Lange BM, Gull K (1995) A molecular marker for centriole maturation in the mammalian cell cycle. J Cell Biol 130:919–927

    Article  PubMed  CAS  Google Scholar 

  • Lofthouse PF, Capon B (1975) Ultrastructural changes accompanying mitosporogenesis in Ectocarpus parvus. Protoplasma 84:83–99

    Article  PubMed  CAS  Google Scholar 

  • Loiseaux S (1973) Ultrastructure of zoidogenesis in unilocular zoidocysts of several brown algae. J Phycol 9:277–289

    Google Scholar 

  • Loiseaux S, West JA (1970) Brown algal mastigonemes: comparative ultrastructure. Trans Am Microsc Soc 89:524–532

    Article  Google Scholar 

  • Maier I (1997a) The fine structure of the male gamete of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae). I. General structure of the cell. Eur J Phycol 32:241–25

    Article  Google Scholar 

  • Maier I (1997b) The fine structure of the male gamete of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae). II. The flagellar apparatus. Eur J Phycol 32:255–266

    Article  Google Scholar 

  • Manton I (1964) A contribution towards understanding of ‘the primitive fucoid’. New Phytol 63:244–254

    Article  Google Scholar 

  • Manton I, Clarke B (1950) Electron microscope observation on the spermatozoids of Fucus. Nature 166:973–974

    Article  PubMed  CAS  Google Scholar 

  • Manton I, Clarke B (1951) Electron microscope observations on the zoospores of Pylaiella and Laminaria. J Exp Bot 2:242–243

    Article  Google Scholar 

  • Manton I, Clarke B (1956) Observations with the electron microscope on the internal structure of the spermatozoids of Fucus. J Exp Bot 7:416–329

    Article  Google Scholar 

  • Manton I, Clarke B, Greenwood AD (1953) Further observations with the electron microscope on spermatozoids in the brown algae. J Exp Bot 4:319–329

    Article  Google Scholar 

  • Markey DR, Bouck GB (1977) Mastigoneme attachment in Ochromonas. J Ultrastruct Res 59:173–177

    Article  PubMed  CAS  Google Scholar 

  • Markey DR, Wilce RT (1975) The ultrastructure of reproduction in the brown alga Pylaiella littoralis. I. Mitosis and cytokinesis in the plurilocular gametangia. Protoplasma 85:219–241

    Article  PubMed  CAS  Google Scholar 

  • Markey DR, Wilce RT (1976a) The ultrastructure of reproduction in the brown alga Pylaiella littoralis. II. Zoosporogenesis in the unilocular sporangia. Protoplasma 88:147–173

    Article  Google Scholar 

  • Markey DR, Wilce RT (1976b) The ultrastructure of reproduction in the brown alga Pylaiella littoralis. III. Later stages of gametogenesis in the plurilocular gamtangia. Protoplasma 88:175–186

    Article  Google Scholar 

  • Marshall WF (2002) Size control in dynamic organelles. Trends Cell Biol 12(9):414–419

    Article  PubMed  CAS  Google Scholar 

  • Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120:343–352

    Article  PubMed  CAS  Google Scholar 

  • Matsunaga S, Uchida H, IsekiM WM, Murakami A (2010) Flagellar motions in phototactic steering in a brown algal swarmer. Photochem Photobiol 86:374–381

    Article  PubMed  CAS  Google Scholar 

  • McIntosh R, Nicastro D, Mastronarde D (2005) New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol 15:43–51

    Article  PubMed  CAS  Google Scholar 

  • Melkonian M, Reize IB, Preisig HR (1987) Maturation of a flagellum/basal body requires more than one cell cycle in algal flagellates: studies on Nephroselmis olivacea (Prasinophyceae). In: Wiessner W, Robinson DG, Star RC (eds) Algal development. Springer, Berlin, pp 102–103

    Chapter  Google Scholar 

  • Motomura T (1993) Ultrastructural and immunofluorescence studies of zoosporogenesis in Laminaria angustata. Sci Pap Inst Alg Res Fac Sci Hokkaido Univ 9:1–32

    Google Scholar 

  • Müller D, Falk H (1973) Flagellar structure of the gametes of Ectocarpus siticulosus (Phaeophyta) as revealed by negative staining. Arch Mikrobiol 91:313–322

    Article  Google Scholar 

  • Müller DG, Maier I, Müller H (1987) Flagellum autofluorescence and photoaccumulation in heterokont algae. Photochem Photobiol 46(6):1003–1008

    Article  Google Scholar 

  • Nagasato C, Motomura T (2002) Influence of the centrosome in cytokinesis of brown algae: polyspermic zygotes of Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). J Cell Sci 115:2541–2548

    PubMed  CAS  Google Scholar 

  • Nicastro D (2006) The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313:944–948

    Article  PubMed  CAS  Google Scholar 

  • Nicastro D, McIntosh JR, Baumeister W (2005) 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proc Natl Acad Sci USA 102:15889–15894

    Article  PubMed  CAS  Google Scholar 

  • O’Kelly CJ (1989) The evolutionary origin of the brown algae: information from studies of motile cell ultrastructure. In: Green JC, Leadbeater BSC and Diver WL (eds) The chromophyte alge: problems and perspectives. Oxford University Press, Oxford. pp. 255–278

  • O’Kelly CJ, Floyd GL (1984) The absolute configuration of the flagellar apparatus in zoospores from two species of Laminariales (Phaeophyceae). Protoplasma 123:18–25

    Article  Google Scholar 

  • Oda T, Hirokawa N, Kikkawa M (2007) Three-dimensional structures of the flagellar dynein-microtubule complex by cryoelectron microscopy. J Cell Biol 177:243–252

    Article  PubMed  CAS  Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Cultures and collections of algae. Japanese Society of Plant Physiologists, Hakone, pp 63–75

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electronmicroscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Rosenbaum JL, Witman GB (2002) Intraflagellar transport. Nat Rev Mol Cell Biol 3:813–825

    Article  PubMed  CAS  Google Scholar 

  • Schoppmeier J, Lechtreck KF (2003) Flagellar regeneration in Spermatozopsis sililis (Chlorophyta). J Phycol 39:918–922

    Article  Google Scholar 

  • Toth R (1974) Sporangial structure and zoosporogenesis in Chorda tomentosa (Laminariales). J Phycol 10:170–185

    Google Scholar 

  • Toth R, Markey DR (1973) Synaptonemal complexes in brown algae. Nature 243:236–237

    Article  PubMed  CAS  Google Scholar 

  • Ueki C, Nagasto C, Motomura T, Saga N (2008) Reexamination of the pit plugs and the characteristic membranous structures in Porphyra yezoensis (Bangiales, Rhodophyta). Phycol 47:5–11

    Article  Google Scholar 

  • Vorobjev IA, Nedezhdina ES (1987) The centrosome and its role in the organization of microtubules. Int Rev Cytol 106:227–229

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Graduate School of Environmental Science, Hokkaido University, Sapporo, 060-0810, Japan

    Gang Fu

  2. Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran, 051-0003, Japan

    Gang Fu, Chikako Nagasato & Taizo Motomura

  3. Electron Microscope Laboratory, Research Faculty of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan

    Toshiaki Ito

  4. Fachbereich Biologie, Universität Konstanz, 78457, Konstanz, Germany

    Dieter G. Müller

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  1. Gang Fu
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  2. Chikako Nagasato
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  3. Toshiaki Ito
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  4. Dieter G. Müller
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  5. Taizo Motomura
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Correspondence to Taizo Motomura.

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Handling Editor: Tsuneyoshi Kuroiwa

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Supplementary Fig. 1

a, b Vesicles in the flagellar lumen (arrows). Arrowheads indicate the flagellar membrane (JPEG 39 kb)

High resolution (TIFF 1441 kb)

Paraflagellar body of the posterior flagellum. The video is composed of 60 adjacent slices (each 1.2-nm thickness) from a dual-axis tomogram corresponding to a paraflagellar body. Regular arrangement of crystalized materials can be detected. Scale bars = 50 nm. (MP4 220 kb)

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Fu, G., Nagasato, C., Ito, T. et al. Ultrastructural analysis of flagellar development in plurilocular sporangia of Ectocarpus siliculosus (Phaeophyceae). Protoplasma 250, 261–272 (2013). https://doi.org/10.1007/s00709-012-0405-7

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