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.
Similar content being viewed by others
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
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
Brumley DR, Wan KY, Polin M, Goldstein RE (2014) Flagellar synchronization through direct hydrodynamic interactions. eLIFE 3:e02750
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
Gibbons IR (1981) Cilia and flagella of eukaryotes. J Cell Biol 91:107s–124s
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
Inaba K (2003) Molecular architecture of the sperm flagella: molecules for motility and signaling. Zool Sci 20:1043–1056
Inaba K (2007) Molecular basis of sperm flagellar axonemes: structural and evolutionary aspects. Ann N Y Acad Sci 1101:506–526
Inaba K (2011) Sperm flagella: comparative and phylogenetic perspectives of protein components. Mol Hum Reprod 17:524–538
Inaba K (2015) Calcium sensors of ciliary outer arm dynein: functions and phylogenetic considerations for eukaryotic evolution. Cilia 4:6
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
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
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
King SM (2000) The dynein microtubule motor. Biochim Biophys Acta 1496:60–75
King SM, Patel-King RS (1995) Identification of a Ca2+-binding light chain within Chlamydomonas outer arm dynein. J Cell Sci 108:3757–3764
Martin B, Melkonian M (1994) Flagellar hairs in prasinophytes (Chlorophyta): ultrastructure and distribution on the flagellar surface. J Phycol 30:659–678
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
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
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
Namdeo S, Khaderi SN, den Toonder JMJ, Onck PR (2011) Swimming direction reversal of flagella through ciliary motion of mastigonemesa). Biomicrofluidics 5:034108
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
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
Sleigh MA (1991) Mechanisms of flagellar propulsion. A biologist’s view of the relation between structure, motion, and fluid mechanics. Protoplasma 164:54–69
Smith EF, Yang P (2004) The radial spokes and central apparatus: mechano-chemical transducers that regulate flagellar motility. Cell Motil Cytoskeleton 57:8–17
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
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
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)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-017-0931-7