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Phototaxis and chemotaxis of brown algal swarmers

Journal of Plant Research volume 130, pages 443–453 (2017)Cite this article

Abstract

Brown algae exhibit three patterns of sexual reproduction: isogamy, anisogamy, and oogamy. Unicellular swarmers including gametes and zoospores bear two heterogenous flagella, an anterior flagellum with mastigonemes (fine tripartite hairs) and a posterior one. In seawater, these flagellates usually receive physico-chemical signals for finding partners and good habitats. It is well known that brown algal swarmers change their swimming direction depending on blue light (phototaxis), and male gametes do so, based on the sex pheromones from female gametes (chemotaxis). In recent years, the comparative analysis of chemotaxis in isogamy, anisogamy, and oogamy has been conducted. In this paper, we focused on the phototaxis and chemotaxis of brown algal gametes comparing the current knowledge with our recent studies.

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References

  • Amsler CD, Neushul M (1989) Chemotactic effects of nutrients on spores of the kelps Macrocytis pyrifera and Pterygophora california. Mar Biol 102:557–564

    CAS  Article  Google Scholar 

  • Amsler CD, Neushul M (1990) Nutrient stimulation of spore settlement in the kelps Pterygophora californica and Macrocystis pyrifera. Mar Biol 107:297–304

    CAS  Article  Google Scholar 

  • Amsler CD, Reed DC, Neushul M (1992) The microclimate inhabited by macroalgal propagules. Br Phycol J 27:253–270

    Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Baldauf SL (2003) The deep roots of eukaryotes. Science 300:1703–1706

    CAS  PubMed  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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Brokaw CL, Kamiya R (1987) Bending patterns of Chlamydomonas flagella: IV. Mutants with defects in inner and outer dynein arms indicate differences in dynein arm function. Cell Motil Cytoskeleton 8:68–75

    CAS  PubMed  Article  Google Scholar 

  • Brokaw CJ, Josslin R, Bobrow L (1974) Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa. Biochem Biophys Res Commun 58:795–800

    CAS  PubMed  Article  Google Scholar 

  • Cardullo RA, Herrick SB, Peterson MJ, Dangott LJ (1994) Speract receptors are localized on sea urchin flagella using a fluorescent peptide analog. Dev Biol 162:600–607

    CAS  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  • Dring MJ (1988) Photocontrol of development in algae. Annu Rev Plant Physiol Plant Mol Biol 39:199–207

    Article  Google Scholar 

  • Dring MJ, Lüning K (1975) A photoperiodic response mediated by blue light in the brown alga Scytosiphon lomentaria. Planta 125:25–32

    CAS  PubMed  Article  Google Scholar 

  • Feinleib MEH, Curry GM (1971) The relationship between stimulus intensity and oriented phototactic response (topotaxis) in Chlamydomonas. Physiol Plant 25:346–352

    Article  Google Scholar 

  • Fletcher RL, Callow ME (1992) The settlement, attachment and establishment of marine algal spores. Br Phycol J 27:303–329

    Article  Google Scholar 

  • Flores-Moya A, Posudin YI, Fernández JA, Figueroa FL, Kawai H (2002) Photomovement of the swarmers of the brown algae Scytosiphon lomentaria and Petalonia fascia: effect of photon irradiance, spectral composition and UV dose. J Photochem Photobiol B 66:134–140

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Fu G, Nagasato C, Ito T, Müller DG, Motomura T (2013) Ultrastructural analysis of flagellar development in plurilocular sporangia of Ectocarpus siliculosus (Phaeophyceae). Protoplasma 250:261–272

    PubMed  Article  Google Scholar 

  • Fu G, Kinoshita N, Nagasato C, Motomura T (2014a) Fertilization of brown algae: flagellar function in phototaxis and chemotaxis. In: Sawada H, Inoue N, Iwano M (eds) Sexual reproduction in animals and plants. Springer, Tokyo, pp 359–367

    Chapter  Google Scholar 

  • Fu G, Nagasato C, Oka S, Cock JM, Motomura T (2014b) Proteomics analysis of heterogeneous flagella in brown algae (Stramenopiles). Protist 165:662–675

    CAS  PubMed  Article  Google Scholar 

  • Fu G, Nagasato C, Yamagishi T, Kawai H, Okuda K, Takao Y, Horiguchi T, Motomura T (2016) Ubiquitous distribution of helmchrome in phototactic swarmers of the stramenopiles. Protoplasma 253:929–941

    CAS  PubMed  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

    CAS  Article  Google Scholar 

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

    Google Scholar 

  • Gibbons IR (1981) Cilia and flagella of eukaryotes. J Cell Biol 91(suppl):107s–124s

    CAS  PubMed  Article  Google Scholar 

  • Gibbons BH, Gibbons IR (1973) The effect of partial extraction of dynein arms on the movement of reactivated sea-urchin sperm. J Cell Sci 13:337–357

    CAS  PubMed  Google Scholar 

  • Glantz ST, Carpenter EJ, Melkonian M, Gardner KH, Boyden ES, Wong GK, Chow BY (2016) Functional and topological diversity of LOV domain photoreceptors. PNAS 113:E1442–E1451. doi:10.1073/pnas.1509428113

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Guerrero A, Nishigaki T, Carneiro J, Yoshiro T, Wood CD, Darszon A (2010) Tuning sperm chemotaxis by calcium burst timing. Dev Biol 334:52–65

    Article  CAS  Google Scholar 

  • Häder D-P (1988) Ecological consequences of photomovement in microorganisms. J Photochem Photobiol B 1:385–414

    Article  Google Scholar 

  • Häder D-P, Colombetti G, Lenci F, Quaglia M (1981) Phototaxis in the flagellates, Euglena gracilis and Ochromonas danica. Arch Microbiol 130:78–82

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Holwill MEJ, Sleigh MA (1967) Propulsion by hispid flagella. J Exp Biol 47:267–276

    CAS  PubMed  Google Scholar 

  • Inaba K (2003) Molecular architecture of the sperm flagella: molecules for motility and signaling. Zool Sci 20:1043–1056

    CAS  PubMed  Article  Google Scholar 

  • Inaba K (2011) Sperm flagella: comparative and phylogenetic perspectives of protein components. Mol Hum Reprod 17:524–538

    CAS  PubMed  Article  Google Scholar 

  • Jaenicke L, Starr RC (1996) The lurlenes, a new class of plastoquinone-related mating pheromones from Chlamydomonas allensworthii (Chlorophyceae). Eur J Biochem 241:581–585

    CAS  PubMed  Article  Google Scholar 

  • Jahn TL, Landman MD, Fonseca JR (1964) The mechanism of locomotion of flagellates. II. Function of the mastigonemes of Ochromonas. J Protozool 11:291–296

    Article  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 5:109–117

    CAS  PubMed  Article  Google Scholar 

  • Kaupp UB, Kashikar ND, Weyand I (2008) Mechanisms of sperm chemotaxis. Annu Rev Physiol 70:93–117

    CAS  PubMed  Article  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 (1992a) A summary of the morphology of chloroplasts and flagellated cells in the Phaeophyceae. Korean J Phycol 7:33–43

    Google Scholar 

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

    Article  Google Scholar 

  • Kawai H, Kreimer G (2000) Sensory mechanisms: light perception and taxis in algae. In: Leadbeater B, Green J (eds) The flagellates: unity, diversity and evolution. Taylor and Francis, London, pp 124–146

    Google Scholar 

  • Kawai H, Müller DG, Fölster E, Häder D-P (1990) Phototactic responses in the gametes of the brown alga, Ectocarpus siliculosus. Planta 182:292–297

    CAS  PubMed  Article  Google Scholar 

  • Kawai H, Kubota M, Kondo T, Watanabe M (1991) Action spectra for phototaxis in zoospores of the brown alga Pseudochorda gracilis. Protoplasma 161:17–22

    Article  Google Scholar 

  • Kinoshita N, Fu G, Ito T, Motomura T (2016a) Three-dimensional organization of flagellar basal apparatus in Ectocarpus gametes. Phycol Res 64:19–25

    Article  Google Scholar 

  • Kinoshita N, Nagasato C, Motomura T (2016b) Chemotactic movement in sperm of the oogamous brown alga, Saccharina japonica and Fucus distichus. Protoplasma. doi:10.1007/s00709-016-0974-y

    PubMed  Google Scholar 

  • Kinoshita N, Shiba K, Inaba K, Fu G, Nagasato C, Motomura T (2016c) Flagellar waveforms of gametes in the brown alga, Ectocarpus siliculosus. Eur J Phycol 51:139–148

    Article  Google Scholar 

  • Kinoshita N, Tanaka A, Nagasato C, Motomura T (2016d) Chemotaxis in the anisogamous brown alga Mutimo cylindricus. Phycologia 55:359–364

    Article  Google Scholar 

  • Kitayama T, Kawai H, Yoshida T (1992) Dominance of female gametophytes in field populations of Cutleria cylindrica (Cutleriales, Phaeophyceae) in the Tsugaru Strait, Japan. Phycologia 31:449–461

    Article  Google Scholar 

  • Kochert G (1978) Sexual pheromones in algae and fungi. Annu Rev Plant Physiol 29:461–486

    CAS  Article  Google Scholar 

  • Kreimer G, Kawai H, Müller DG, Melkonian M (1991) Reflective properties of the stigma in male gametes of Ectocarpus siliculosus (Phaeophyceae) studied by confocal laser scanning microscopy. J Phycol 27:268–276

    Article  Google Scholar 

  • Lindemann CB (2004) Testing the geometric clutch hypothesis. Biol Cell 96:681–690

    PubMed  Article  Google Scholar 

  • Lipinska AP, D’hondt S, Damme EJV, Clerck OD (2013) Uncovering the genetic basis for early isogamete differentiation: a case study of Ectocarpus siliculosus. BMC Genom 14:909

    Article  CAS  Google Scholar 

  • Lipinska AP, Damme EJV, Clerck OD (2016) Molecular evolution of candidate male reproductive genes in the brown algal model Ectocarpus. BMC Evol Biol 16:5

    PubMed  PubMed Central  Article  CAS  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 

  • Luthringer R, Cormier A, Ahmed S, Peters AF, Cock JM, Coelho SM (2014) Sexual dimorphism in the brown algae. Perspect Phycol 1:11–25

    Article  Google Scholar 

  • Maier I (1993) Gamete orientation and induction of gametogenesis by pheromone in algae and plants. Plant Cell Environ 16:891–907

    CAS  Article  Google Scholar 

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

    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 32:241–253

    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 

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

    CAS  Article  Google Scholar 

  • Maier I, Müller DG (1982) Antheridium fine structure and spermatozoid release in Laminaria digitata. Phycologia 21:1–8

    Article  Google Scholar 

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

    CAS  Article  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, Schmid CE (1995) An immunofluorescence study on lectin binding sites in gametes of Ectocarpus siliculosus (Ectocarpales, Phaeophyceae). Phycol Res 43: 33–42

    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

    CAS  Article  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 B 86:374–381

    CAS  Article  Google Scholar 

  • Mizuno K, Shiba K, Okai M, Takahashi Y, Shitaka Y, Oiwa K, Tanokura M, Inaba K (2012) Calaxin drives sperm chemotaxis by Ca2+-mediated direct modulation of a dynein motor. Proc Natl Acad Sci USA 109:20497–20502

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Morel-Laurens N (1987) Calcium control of phototactic orientation in Chlamydomorias reinhardtii: sign and strength of response. Photochem Photobiol 45:119–128

    CAS  PubMed  Article  Google Scholar 

  • Müller DG (1977) Sexual reproduction in British Ectocarpus siliculosus (Phaeophyta). Br Phycol J 12:131–136

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Müller DG (1979) Olefinic hydrocarbons in seawater: Signal molecules for sexual reproduction in brown algae. Pure Appl Chem 51:1885–1891

    Article  Google Scholar 

  • Müller DG, Falk H (1973) Flagellar structure of the gametes of Ectocarpus siliculosus (Phaeophyta) as revealed by negative staining. Archiv für Mikrobiol 91:313–322

    Article  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

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  • Nagasato C, Motomura T, Ichimura T (1998) Selective disappearance of maternal centrioles after fertilization in the anisogamous brown alga Cutleria cylindrica (Cutleriales, Phaeophyceae): paternal inheritance of centrioles is universal in the brown algae. Phycol Res 46:191–198

    Article  Google Scholar 

  • Nishigaki T, Chiba K, Hoshi M (2000) A 130-kDa membrane protein of sperm flagella is the receptor for asterosaps, sperm-activating peptides of starfish Asterias amurensis. Dev Biol 219:154–162

    CAS  PubMed  Article  Google Scholar 

  • Nozaki H, Yamada TK, Takahashi F, Matsuzaki R, Nakada T (2014) New “missing link” genus of the colonial volvocine green algae gives insights into the evolution of oogamy. BMC Evol Biol 14:37

    PubMed  PubMed Central  Article  Google Scholar 

  • Nultsch W, Häder D-P (1988) Photomovement in motile microorganisms. II. Photochem Photobiol 47:837–869

    CAS  PubMed  Article  Google Scholar 

  • O’Kelly CJ (1989) The evolutionary origin of the brown algae: information from studies of motile cell structure. In: Green JC, Leadbeater BSC, Diver WL (eds) The chromophyte algae: problems and perspectives, systematics association special, 38. Clarendon Press, Oxford, pp 256–278

    Google Scholar 

  • 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 

  • Pearson GA, Serrão EA, Dring MJ, Schmid R (2004) Blue- and green-light signals for gamete release in the brown alga, Silvetia compressa. Oecologia 138:193–201

    PubMed  Article  Google Scholar 

  • Reed DC, Laur DR, Ebeling AW (1988) Variation in algal dispersal and recruitment: the importance of episodic events. Ecol Monogr 58:321–335

    Article  Google Scholar 

  • Schmid CE (1993) Cell-cell-recognition during fertilization in Ectocarpus siliculosus (Phaeophyceae). Hydrobiologia 261:437–443

    Article  Google Scholar 

  • Schmid CE, Schroer N, Müller DG (1994) Female gamete membrane glycoproteins potentially involved in gamete recognition in Ectocarpus siliculosus (Phaeophyceae). Plant Sci 102:61–67

    CAS  Article  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 USA 105:19312–19317

    CAS  PubMed  PubMed Central  Article  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

    CAS  PubMed  Article  Google Scholar 

  • Singh S, Lowe DG, Thorpe DS, Rodriguez H, Kuang W-J, Dangott LJ, Chinkers M, Goeddel DV, Garbers DL (1988) Membrane guanylate cyclase is a cell-surface receptor with homology to protein kinases. Nature 334:708–712

    CAS  PubMed  Article  Google Scholar 

  • Starr RC, Marner FJ, Jaenicke L (1995) Chemoattraction of male gametes by a pheromone produced by female gametes of Chlamydomonas. Proc Natl Acad Sci USA 92:641–645

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Takahashi F (2016) Blue-light-regulated transcription factor, Aureochrome, in photosynthetic stramenopiles. J Plant Res 129:189–197

    CAS  PubMed  Article  Google Scholar 

  • Takahashi T, Watanabe M (1993) Photosynthesis modulates the sign of phototaxis of wild-type Chlamydomonas reinhardtii. Effects of red background illumination and 3-(3′,4′-dichlorophenyl)-1,1-dimethylurea. FEBS Lett 336:516–520

    CAS  PubMed  Article  Google Scholar 

  • Teves ME, Guidobaldi HA, Unates DR, Sanchez R, Miska W, Publicover SJ, Morales Garcia AA, Giojalas LC (2009) Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS One 4:e8211

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Togashi T, Bartelt JL (2011) Evolution of anisogamy and related phenomena in marine green algae. In: Togashi T, Cox PA (eds) The evolution of anisogamy: a fundamental phenomenon underlying sexual selection. Cambridge University Press, Cambridge, pp 194–242

    Chapter  Google Scholar 

  • Wakabayashi K, Misawa Y, Mochiji S, Kamiya R (2011) Reduction–oxidation poise regulates the sign of phototaxis in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 108:11280–11284

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ward GE, Brokaw CJ, Garbers DL, Vacquier VD (1985) Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from the egg jelly layer. J Cell Biol 101:2324–2329

    CAS  PubMed  Article  Google Scholar 

  • Wood CD, Nishigaki T, Furuta T, Baba SA, Darszon A (2005) Real-time analysis of the role of Ca2+ in flagellar movement and motility in single sea urchin sperm. J Cell Biol 169:725–731

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    Article  Google Scholar 

  • Yamagishi T, Motomura T, Nagasato C, Kato A, Kawai H (2007) A tubular mastigoneme-related protein Ocm1 isolated from the flagellum of a chromophyte alga Ochromonas danica. J Phycol 43:519–527

    CAS  Article  Google Scholar 

  • Yamagishi T, Motomura T, Nagasato C, Kato A, Kawai H (2009) Novel proteins comprising the stramenopile tripartite mastigoneme in Ochromonas danica (Chrysophyceae). J Phycol 45:1100–1105

    CAS  Article  Google Scholar 

  • Yamanouchi S (1912) The life history of Cutleria. Contr Hull Bot Lab163. Bot Gaz 54:441–502

    Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • Yoshida M, Inaba K, Ishida K, Morisawa M (1994) Calcium and cyclic AMP mediate sperm activation, but Ca2+ alone contributes sperm chemotaxis in ascidian, Ciona savignyi. Dev Growth Differ 36:589–595

    CAS  Article  Google Scholar 

  • Yoshida M, Ishikawa M, Izumi H, De Santis R, Morisawa M (2003) Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm. Proc Natl Acad Sci USA 100:149–154

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

We sincerely thank Dr. Makoto Terauchi, Kobe University, and Dr. Tatsuya Togashi, Chiba University, for helpful discussions. We also thank Drs. Kogiku Shiba and Kazuo Inaba of the Shimoda Marine Research Center, University of Tsukuba, for their many valuable comments. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

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

    Nana Kinoshita

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

    Chikako Nagasato & Taizo Motomura

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  1. Nana Kinoshita
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  2. Chikako Nagasato
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Correspondence to Taizo Motomura.

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Kinoshita, N., Nagasato, C. & Motomura, T. Phototaxis and chemotaxis of brown algal swarmers. J Plant Res 130, 443–453 (2017). https://doi.org/10.1007/s10265-017-0914-8

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Keywords

  • Brown algae
  • Calcium
  • Chemotaxis
  • Flagella
  • Gametes
  • Phototaxis