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Chemotactic movement in sperm of the oogamous brown algae, Saccharina japonica and Fucus distichus

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Abstract

In oogamous species of brown algae such as Saccharina japonica and Fucus distichus, the sperm possess an unusual long posterior flagellum, which oscillates actively and produces a propulsive force during swimming. In this study, we quantitatively analyzed the effect of chemotactic responses on sperm swimming and flagellar waveforms by high-speed video recordings. We found that the thigmotactic response to the chemo-attractant was not enhanced during chemotactic swimming and that the swimming velocity of sperm did not decrease. As concentration of the chemo-attractant decreased, the sperm performed drastic U-turn movements, which was caused by a rapid and large bend of the posterior flagellum. Unilateral bending of the posterior flagellum when sensing a decrease in the concentration of the chemo-attractant may be a common response in male gametes during fertilization of brown algae both oogamous and isogamous species.

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References

  • Böhmer M, Van Q, Weyand I, Hagen V, Beyermann M, Matsumoto M, Hoshi M, Hildebrand E, Kaupp UB (2005) Ca2+ spikes in the flagellum control chemotactic behavior of sperm. EMBO 24:2741–2752

    Article  Google Scholar 

  • Boland W (1995) The chemistry of gamete attraction: chemical structures, biosynthesis, and (a)biotic degradation of algal pheromones. Proc Natl Acad Sci U S A 92:37–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brokaw CJ (1979) Calcium-induced asymmetrical beating of triton-demembranated sea urchin sperm flagella. J Cell Biol 82:401–411

    Article  CAS  PubMed  Google Scholar 

  • Frenkel J, Vyverman W, Pohnert G (2014) Pheromone signaling during sexual reproduction in algae. Plant J 79:632–644

    Article  CAS  PubMed  Google Scholar 

  • Fu G, Nagasato C, Yamagishi T, Kawai H, Okuda K, Takao Y, Horiguchi T, Motomura T (2015) Ubiquitous distribution of helmchrome in phototactic swarmers of the stramenopiles. Protoplasma. doi:10.1007/s00709-015-0857-7

    PubMed  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 

  • Gibbons BH, Gibbons IR (1980) Calcium-induced quiescence in reactivated sea urchin sperm. J Cell Biol 84:13–27

    Article  CAS  PubMed  Google Scholar 

  • Guerrero A, Nishigaki T, Carneiro J, Tatsu Y, Wood CD, Darszon A (2010) Tuning sperm chemotaxis by calcium burst timing. Dev Biol 344:52–65

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Higashiyama T, Takeuchi H (2015) The mechanism and key molecules involved in pollen tube guidance. Annu Rev Plant Biol 66:393–413

    Article  CAS  PubMed  Google Scholar 

  • Kambara Y, Shiba K, Yoshida M, Sato C, Kitajima K, Shingyoji C (2011) Mechanism regulating Ca2+-dependent mechanosensory behaviour in sea urchin spermatozoa. Cell Struct Funct 36:69–82

    Article  CAS  PubMed  Google Scholar 

  • Kaup UB (2010) Olfactory signallyng in vertebrates and insects: differences and commonalities. Nat Rev 11:188–200

    Google Scholar 

  • Kaupp UB, Solzin J, Hildebrand E, Brown JE, Helbig A, Hagen V, Beyermann M, Pampaloni F, Weyand I (2003) The signal flow and motor response controlling chemotaxis of sea urchin sperm. Nat Cell Biol 5:109–17

    Article  CAS  PubMed  Google Scholar 

  • Kawai H (1992) A summary of the morphology of chloroplasts and flagellated cells in the Phaeophyceae. Korean J Phycol 7:33–43

    Google Scholar 

  • Kawai H, Motomura T, Okuda K (2005) Isolation and purification techniques for macroalgae. In: Andersen AA (ed) Algal culturing techniques. Elsevier Academic Press, London, pp 133–143

    Google Scholar 

  • Kinoshita N, Shiba K, Inaba K, Fu G, Nagasato C, Motomura T (2015) Flagellar Waveforms of gametes in the brown alga, Ectocarpus siliculosus. Eur J Phycol. doi:10.1080/09670262.2015.1109144

    Google Scholar 

  • Lüning K (1981) Egg release in gametophytes of Laminaria saccharina: induction by darkness and inhibition by blue light and UV. Br Phycol J 16:379–393

    Article  Google Scholar 

  • Lüning K, Dring MJ (1972) Reproduction induced by blue light in female gametophytes of Laminaria saccharina. Planta 104:252–256

    Article  PubMed  Google Scholar 

  • Lüning K, Dring MJ (1975) Reproduction, growth and photosynthesis of gametophytes of Laminaria saccharina grown in blue and red light. Mar Biol 29:195–200

    Article  Google Scholar 

  • Maier I (1995) Brown algal pheromones. In: Round FE, Chapman DJ (eds) Progress in phycological research 11: 51–102. Biopress, Bristol, pp 51–102

    Google Scholar 

  • Maier I, Calenberg M (1994) Effect of extracellular Ca2+ and Ca2+ antagonists on the movement and chemoorientation of male gametes of Ectocarpus siliculosus (Phaeophyceae). Bot Acta 107:451–460

    Article  CAS  Google Scholar 

  • Maier I, Müller DG (1986) Sexual pheromones in algae. Biol Bull 170:145–175

    Article  CAS  Google Scholar 

  • Maier I, Müller DG (1990) Chemotaxis in Laminaria digitata (Phaeophyceae) I. Analysis of spermatozoid movement. J Exp Bot 41:869–876

    Article  Google Scholar 

  • Maier I, Wenden A, Clayton MN (1992) The movement of Hormosira banksii (Fucales, Phaeophyta) spermatozoids in response to sexual pheromone. J Exp Bot 43:1651–1657

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Motomura T, Sakai Y (1981) Effects of chelated iron in culture media on oogenesis in Laminaria angustata. Bull Jpn Soc Sci Fish 27:1535–1540

    Article  Google Scholar 

  • Motomura T, Sakai Y (1984) Ultrastructural studies of gametogenesis in Laminaria angustata (Laminariales, Phaeophyta) regulated by iron concentration in the medium. Phycologia 23:331–343

    Article  Google Scholar 

  • Müller DG (1978) Locomotive responses of male gametes to the species-specific sex attractant in Ectocarpus siliculosus (Phaeophyta). Arch Protistenkd 120:371–377

    Article  Google Scholar 

  • Müller DG, Jaenicke L (1973) Fucoserraten, the female sex attractant of Fucus serratus L. (phaeophyta). FEBS Lett 30:137–139

    Article  PubMed  Google Scholar 

  • Müller DG, Jaenickel L, Donike M, Akintobi T (1971) Sex attractant in a brown alga: chemical structure. Science 171:815–817

    Article  PubMed  Google Scholar 

  • Müller DG, Gassmann G, Lüning K (1979) Isolation of a spermatozoid-releasing and -attracting substance from female gametophytes of Laminaria digitata. Nature 279:430–431

    Article  PubMed  Google Scholar 

  • Nagasato C, Motomura T, Ichimura T (1999) Influence of centriole behavior on the first spindle formation in zygotes of the brown alga Fucus distichus (Fucales, Phaeophyceae). Dev Biol 208:200–209

    Article  CAS  PubMed  Google Scholar 

  • Provasoli L (1963) Growing marine seaweeds. In: De Virville D, Feldman J (eds) Proceedings of the fourth international seaweed symposium. Pergamon Press, Oxford, pp 9–17

    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 Physiology, Hakone, pp 63–75

    Google Scholar 

  • Shiba K, Baba SA, Inoue T, Yoshida M (2008) Ca2+ bursts occur around a local minimal concentration of attractant and trigger sperm chemotactic response. Proc Natl Acad Sci U S A 105:19312–19317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silberfeld T, Leigh JW, Verbruggen H, Cruaud C, de Reviers B, Rousseau F (2010) A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the “brown algal crown radiation”. Mol Phylogenet Evol 56:659–674

    Article  CAS  PubMed  Google Scholar 

  • Tatewaki M, Wang XY, Wakana I (1989) A simple method of red seaweed axenic culture by spore-washing. Jpn J Phycol 37:150–152

    Google Scholar 

  • Wakana I, Abe M (1992) Artificial insemination ‘regulated by EDTA’ in the monoecious brown alga Fucus evanescens. Plant Cell Physiol 33:569–575

    CAS  Google Scholar 

  • Wynne MJ, Loiseaux S (1976) Recent advances in life history studies of the Phaeophyta. Phycologia 15:435–452

    Article  Google Scholar 

  • Yoshida M (2014) Sperm chemotaxis: the first authentication events between conspecific before fertileization. In: Sawada H, Inoue N, Iwano M (eds) Sexual reproduction in animals and plants. Springer Open, Tokyo, pp 3–11

    Chapter  Google Scholar 

  • Yoshida M, Yoshida K (2011) Sperm chemotaxis and regulation of flagellar movement by Ca2+. Mol Hum Reprod 17:457–465

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We sincerely thank Drs. Kogiku Shiba and Kazuo Inaba of the Shimoda Marine Research Center, University of Tsukuba, who kindly provided many valuable comments.

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Authors and Affiliations

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

    Nana Kinoshita

  2. Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran, 051-0013, Hokkaido, Japan

    Chikako Nagasato & Taizo Motomura

Authors
  1. Nana Kinoshita
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  2. Chikako Nagasato
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  3. Taizo Motomura
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Corresponding author

Correspondence to Taizo Motomura.

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The authors declare that they have no conflict of interest.

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Handling Editor: Tsuneyoshi Kuroiwa

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Sup. Movie 1

Release of sperm by S. japonica. (AVI 6356 kb)

Sup. Movie 2

Abnormal sperm lacking AF in S. japonica. (AVI 3605 kb)

Sup. Movie 3

U-turn by S. japonica sperm. (AVI 1843 kb)

Sup. Movie 4

U-turn by F. distichus sperm. (AVI 11065 kb)

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Kinoshita, N., Nagasato, C. & Motomura, T. Chemotactic movement in sperm of the oogamous brown algae, Saccharina japonica and Fucus distichus . Protoplasma 254, 547–555 (2017). https://doi.org/10.1007/s00709-016-0974-y

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  • DOI: https://doi.org/10.1007/s00709-016-0974-y

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