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Inverse relationship of Ca2+-dependent flagellar response between animal sperm and prasinophyte algae

Abstract

Symmetry/asymmetry conversion of eukaryotic flagellar waveform is caused by the changes in intracellular Ca2+. Animal sperm flagella show symmetric or asymmetric waveform at lower or higher concentration of intracellular Ca2+, respectively. In Chlamydomonas, high Ca2+ induces conversion of flagellar waveform from asymmetric to symmetry, resulting in the backward movement. This mirror image relationship between animal sperm and Chlamydomonas could be explained by the distinct calcium sensors used to regulate the outer arm dyneins (Inaba 2015). Here we analyze the flagellar Ca2+-response of the prasinophyte Pterosperma cristatum, which shows backward movement by undulating four flagella, the appearance similar to animal sperm. The moving path of Pterosperma shows relatively straight in artificial seawater (ASW) or ASW in the presence of a Ca2+ ionophore A23187, whereas it becomes circular in a low Ca2+ solution. Analysis of flagellar waveform reveals symmetric or asymmetric waveform propagation in ASW or a low Ca2+ solution, respectively. These patterns of flagellar responses are completely opposite to those in sperm flagella of the sea urchin Anthocidaris crassispina, supporting the idea previously proposed that the difference in flagellar response to Ca2+ attributes to the evolutional innovation of calcium sensors of outer arm dynein in opisthokont or bikont lineage.

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References

  • Bannai H, Yoshimura M, Takahashi K, Shingyoji C (2000) Calcium regulation of microtubule sliding in reactivated sea urchin sperm flagella. J Cell Sci 113:831–839

    CAS  PubMed  Google Scholar 

  • Brokaw CJ (1991) Microtubule sliding in swimming sperm flagella: direct and indirect measurements on sea urchin and tunicate spermatozoa. J Cell Biol 114:1210–1217

    Article  Google Scholar 

  • Brumley DR, Wan KY, Polin M, Goldstein RE (2014) Flagellar synchronization through direct hydrodynamic interactions. eLIFE 3:e02750

    Article  PubMed  PubMed Central  Google Scholar 

  • Casey DM, Inaba K, Pazour GJ, Takada S, Wakabayashi K, Wilkerson CG, Kamiya R, Witman GB (2003) DC3, the 21-kDa subunit of the outer dynein arm-docking complex (ODA-DC), is a novel EF-hand protein important for assembly of both the outer arm and the ODA-DC. Mol Biol Cell 14:3650–3663

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Hori T, Moestrup Ø (1987) Ultrastructure of the flagellar apparatus in Pyraminonas octopus (Prasinophyceae) I. Axoneme structure and numbering of peripheral doublet/triplets. Protoplasma 138:137–148

    Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Inaba K (2007) Molecular basis of sperm flagellar axonemes: structural and evolutionary aspects. Ann N Y Acad Sci 1101:506–526

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  • Inaba K (2015) Calcium sensors of ciliary outer arm dynein: functions and phylogenetic considerations for eukaryotic evolution. Cilia 4:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Inaba K, Kutomi O, Shiba K, Cosson J (2015) Sperm guidance: comparison with motility regulation in bikont species. In: Cosson J, (ed) Flagellar Mechanics and Sperm Guidance. Bentham Science Publishers

  • Inouye I, Hori T (1991) High-speed video analysis of the flagellar beat and swimming patterns of algae: possible evolutionary trends in green algae. Protoplasma 164:54–69

    Article  Google Scholar 

  • Inouye I, Hori T, Chihara M (1990) Absolute configuration analysis of the flagellar apparatus of Pterosperma cristatum (Prasinophyceae) and consideration of its phylogenetic position. J Phycol 26:329–344

    Article  Google Scholar 

  • Kamiya R, Okamoto M (1985) A mutant of Chlamydomonas reinhardtii that lacks the flagellar outer dynein arm but can swim. J Cell Sci 74:181–191

    CAS  PubMed  Google Scholar 

  • King SM (2000) The dynein microtubule motor. Biochim Biophys Acta 1496:60–75

    CAS  Article  PubMed  Google Scholar 

  • King SM, Patel-King RS (1995) Identification of a Ca2+-binding light chain within Chlamydomonas outer arm dynein. J Cell Sci 108:3757–3764

    CAS  PubMed  Google Scholar 

  • Martin B, Melkonian M (1994) Flagellar hairs in prasinophytes (Chlorophyta): ultrastructure and distribution on the flagellar surface. J Phycol 30:659–678

    Article  Google Scholar 

  • Mitchell D (2007) The evolution of eukaryotic cilia and flagella as motile and sensory organelles. In: Jekely G (ed) Origins and evolution of eukaryotic endomembranes and cytoskeleton. Eurekah.com

  • Mitchell DR, Rosenbaum JL (1985) A motile Chlamydomonas flagellar mutant that lacks outer dynein arms. J Cell Biol 100(4):1228–1234

    CAS  Article  PubMed  Google Scholar 

  • Mizuno K, Padma P, Konno A, Satouh Y, Ogawa K, Inaba K (2009) A novel neuronal calcium sensor family protein, calaxin, is a potential Ca2+-dependent regulator for the outer arm dynein of metazoan cilia and flagella. Biol Cell 101:91–103

    CAS  Article  PubMed  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  Article  PubMed  PubMed Central  Google Scholar 

  • Namdeo S, Khaderi SN, den Toonder JMJ, Onck PR (2011) Swimming direction reversal of flagella through ciliary motion of mastigonemesa). Biomicrofluidics 5:034108

    CAS  Article  PubMed Central  Google Scholar 

  • Porter ME, Sale WS (2000) The 9 + 2 Axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J Cell Biol 151:37–42

    Article  PubMed Central  Google Scholar 

  • Shingyoji C, Gibbons IR, Murakami A, Takahashi K (1991) Effect of imposed head vibration on the stability and waveform of flagellar beating in sea urchin spermatozoa. J Exp Biol 156:63–80

    CAS  PubMed  Google Scholar 

  • Sleigh MA (1991) Mechanisms of flagellar propulsion. A biologist’s view of the relation between structure, motion, and fluid mechanics. Protoplasma 164:54–69

    Article  Google Scholar 

  • Smith EF, Yang P (2004) The radial spokes and central apparatus: mechano-chemical transducers that regulate flagellar motility. Cell Motil Cytoskeleton 57:8–17

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Tamm SL (2014) Cilia and the life of ctenophores. Invertebr Biol 133:1–46

  • Throndsen J (1988) Cymbomonas Schiller (Prasinophyceae) reinvestigated by light and electron microscopy. Arch Protistenk 136:327–336

    Article  Google Scholar 

  • Wakabayashi K, Yagi T, Kamiya R (1997) Ca2+-dependent waveform conversion in the flagellar axoneme of Chlamydomonas mutants lacking the central-pair/radial spoke system. Cell Motil Cytoskeleton 38(1):22–28

    CAS  Article  PubMed  Google Scholar 

  • Witman GB, Carlson K, Berliner J, Rosenbaum JL (1972) Chlamydomonas flagella. I. Isolation and electrophoretic analysis of microtubules, matrix, membranes, and mastigonemes. J Cell Biol 54:507–539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank National Institute for Environmental Studies (NIES) for providing a strain of Pterosperma cristatum (NIES-626). This work was supported in part by Grant-in-Aid 15H01201 for Scientific Research on Innovative Areas and 22370023 for Scientific Research (B) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT).

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Correspondence to Kazuo Inaba.

Electronic supplementary material

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Movie S1. Flagellar movement of the sea urchin A. crassispina sperm. Five hundred frames were recorded per second. The movie plays at 0.06× speed. (MOV 644 KB)

Movie S2. Flagellar movement of the prasinophyte P. cristatum. Five hundred frames were recorded per second. The movie plays at 0.06× speed. (MOV 222 KB)

Movie S3. Turn movement of the prasinophyte P. cristatum. Five hundred frames were recorded per second. The movie plays at 0.06× speed. (MOV 171 KB)

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Shiba, K., Inaba, K. Inverse relationship of Ca2+-dependent flagellar response between animal sperm and prasinophyte algae. J Plant Res 130, 465–473 (2017). https://doi.org/10.1007/s10265-017-0931-7

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  • DOI: https://doi.org/10.1007/s10265-017-0931-7

Keywords

  • Calaxin
  • Cilia
  • Dynein
  • Opisthokont
  • Prasinophyte
  • Sperm flagella