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Removal of the block to self-fertilization by low-calcium artificial seawater in the ascidian Ciona intestinalis

Published online by Cambridge University Press:  10 June 2022

Shizuya Hashimoto ,
Keita Kinjo ,
Takako Saito Open the ORCID record for Takako Saito [Opens in a new window]  and
Hitoshi Sawada Open the ORCID record for Hitoshi Sawada [Opens in a new window]
Shizuya Hashimoto
Affiliation:
Graduate School of Science, Nagoya University, Nagoya, Aichi 464-8602, Japan
Keita Kinjo
Affiliation:
Department of Applied Sciences, Faculty of Agriculture, Shizuoka University, Shizuoka 422-8529, Japan
Takako Saito*
Affiliation:
Department of Applied Sciences, Faculty of Agriculture, Shizuoka University, Shizuoka 422-8529, Japan Shizuoka Institute for the Study of Marine Biology and Chemistry, Shizuoka University, Shizuoka 422-8529, Japan
Hitoshi Sawada*
Affiliation:
Graduate School of Science, Nagoya University, Nagoya, Aichi 464-8602, Japan Department of Food and Nutritional Environment, College of Human Life and Environment, Kinjo Gakuin University, Nagoya, Aichi 463-8521, Japan
*
Authors for correspondence: Hitoshi Sawada. Department of Food and Nutritional Environment, College of Human Life and Environment, Kinjo Gakuin University, Nagoya, Aichi 463-8521, Japan. Tel: +81 52 798 018. Fax: +81 52 798 0370. E-mail: [email protected] Takako Saito. Department of Applied Sciences, Faculty of Agriculture, Shizuoka University, Shizuoka 422-8529, Japan. Tel: +81 54 238 4150. E-mail: [email protected]
Authors for correspondence: Hitoshi Sawada. Department of Food and Nutritional Environment, College of Human Life and Environment, Kinjo Gakuin University, Nagoya, Aichi 463-8521, Japan. Tel: +81 52 798 018. Fax: +81 52 798 0370. E-mail: [email protected] Takako Saito. Department of Applied Sciences, Faculty of Agriculture, Shizuoka University, Shizuoka 422-8529, Japan. Tel: +81 54 238 4150. E-mail: [email protected]
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Summary

Ascidians (Urochordate) are hermaphroditic marine invertebrates that release sperm and eggs to the surrounding seawater. However, several ascidians, including Ciona intestinalis and Halocynthia roretzi, show strict self-sterility due to a self/nonself-recognition mechanism in the interaction between sperm and the vitelline coat (VC) of the eggs. We have previously reported that sperm intracellular Ca2+ level drastically increased immediately after sperm binding to the VC of self eggs but not nonself eggs in C. intestinalis type A, which was potently inhibited by lowering the external Ca2+ concentration, suggesting that sperm Ca2+ influx occurs after sperm self-recognition on the VC. Here, we investigated whether self-sterility was abolished by lowering the external Ca2+ concentration in C. intestinalis. The results showed that the block to self-fertilization was removed by low-Ca2+ (∼1 mM) seawater without decreasing the fertilization rate. Such an effect was not observed with Mg2+ or K+. These results led us to conclude that a low-Ca2+ environment is sufficient to block the self-recognition signal upon fertilization. As low-Ca2+ seawater showed no effect on H. roretzi self-sterility, we propose that the mechanism of self-sterility in Ciona must be distinctive from that in Halocynthia.

Keywords

AscidianCalciumFertilizationSelf-incompatibilitySelf-sterility
Type
Short Communication
Information
Zygote , Volume 30 , Issue 5 , October 2022 , pp. 738 - 742
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

†

Present address: Research Center for Marine Biology, Graduate School of Life Sciences, Tohoku University, Asamushi, Aomori 039–3501, Japan.

References

Brozovic, M., Martin, C., Dantec, C., Dauga, D., Mendez, M., Simion, P., Percher, M., Laporte, B., Scornavacca, C., Di Gregorio, A., Fujiwara, S., Gineste, M., Lowe, E. K., Piette, J., Racioppi, C., Ristoratore, F., Sasakura, Y., Takatori, N., Brown, T. C., et al. (2016). Aniseed 2015: A digital framework for the comparative developmental biology of ascidians. Nucleic Acids Research, 44(D1), D808–D818. doi: 10.1093/nar/gkv966 CrossRefGoogle ScholarPubMed
Brunetti, R., Gissi, C., Pennati, R., Caicci, F., Gasparini, F. and Manni, L. (2015). Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis . Journal of Zoological Systematics and Evolutionary Research, 53(3), 186–193. doi: 10.1111/jzs.12101 CrossRefGoogle Scholar
Casazza, G., De Santis, R. and Pinto, M. R. (1984). Sperm binding to eggs of Ciona intestinalis. Role of Ca2+ . Experimental Cell Research, 155(1), 261–266. doi: 10.1016/0014-4827(84)90787-0 CrossRefGoogle ScholarPubMed
Harada, Y. and Sawada, H. (2008). Allorecognition mechanisms during ascidian fertilization. International Journal of Developmental Biology, 52(5–6), 637–645. doi: 10.1387/ijdb.072544yh CrossRefGoogle ScholarPubMed
Harada, Y., Takagaki, Y., Sunagawa, M., Saito, T., Yamada, L., Taniguchi, H., Shoguchi, E. and Sawada, H. (2008). Mechanism of self-sterility in a hermaphroditic chordate. Science, 320(5875), 548–550. doi: 10.1126/science.1152488 CrossRefGoogle Scholar
Iwano, M. and Takayama, S. (2012). Self/non-self discrimination in angiosperm self- incompatibility. Current Opinion in Plant Biology, 15(1), 78–83. doi: 10.1016/j.pbi.2011.09.003 CrossRefGoogle ScholarPubMed
Izumi, H., Márián, T., Inaba, K., Oka, Y. and Morisawa, M. (1999). Membrane hyperpolarization by sperm-activating and -attracting factor increases cAMP level and activates sperm motility in the ascidian Ciona intestinalis . Developmental Biology, 213(2), 246–256. doi: 10.1006/dbio.1999.9367 CrossRefGoogle ScholarPubMed
Morgan, T. H. (1910). Cross- and self-fertilization in Ciona intestinalis . Archiv für Entwicklungsmechanik der Organismen, 30(2), 206–235. doi: 10.1007/BF02263809 CrossRefGoogle Scholar
Morgan, T. H. (1923). Removal of the block to self-fertilization in the ascidian Ciona . Proceedings of the National Academy of Sciences of the United States of America, 9(5), 170–171. doi: 10.1073/pnas.9.5.170 CrossRefGoogle ScholarPubMed
Morgan, T. H. (1939). The genetic and the physiological problems of self-sterility in Ciona. III. Induced self-fertilization. Journal of Experimental Zoology, 80(1), 19–54. doi: 10.1002/jez.1400800103 CrossRefGoogle Scholar
Nakazawa, S., Shirae-Kurabayashi, M. and Sawada, H. (2019). The role of metalloproteases in fertilization in the ascidian Ciona robusta . Scientific Reports, 9(1), 1009. doi: 10.1038/s41598-018-37721-1 CrossRefGoogle ScholarPubMed
Rosati, F. and De Santis, R. (1978). Studies on fertilization in the ascidains I. Self-sterility and specific recognition between gametes of Ciona intestinalis . Experimental Cell Research, 112(1), 111–119. doi: 10.1016/0014-4827(78)90531-1 CrossRefGoogle ScholarPubMed
Saito, T., Shiba, K., Inaba, K., Yamada, L. and Sawada, H. (2012). Self-incompatiblity response induced by calcium increase in seprm of the ascidian Ciona intestinalis . Proceedings of the National Academy of Sciences of the United States of America, 109(11), 4158–4162. doi: 10.1073/pnas.1115086109 CrossRefGoogle Scholar
Sawada, H., Yokosawa, H., Ishii, S. and Hoshi, M. (1982). Evidence for acrosin-like enzyme in sperm extract and its involvement in fertilization of the ascidian, Halocynthia roretzi . Gamete Research, 5(3), 291–301. doi: 10.1002/mrd.1120050309 CrossRefGoogle Scholar
Sawada, H., Morita, M. and Iwano, M. (2014). Self/non-self recognition mechanisms in sexual reproduction: New insight into the self-incompatibility system shared by flowering plants and hermaphroditic animals. Biochemical and Biophysical Research Communications, 450(3), 1142–1148. doi: 10.1016/j.bbrc.2014.05.099 CrossRefGoogle ScholarPubMed
Sawada, H., Yamamoto, K., Yamaguchi, A., Yamada, L., Higuchi, A., Nukaya, H., Fukuoka, M., Sakuma, T., Yamamoto, T., Sasakura, Y. and Shirae-Kurabayashi, M. (2020). Three multi-allelic gene pairs are responsible for self-sterility in the ascidian Ciona intestinalis . Scientific Reports, 10(1), 2514. doi: 10.1038/s41598-020-59147-4 CrossRefGoogle ScholarPubMed
Schultz, J. E., Klumpp, S., Benz, R., Schürhoff-Goeters, W. J. C. and Schmid, A. (1992). Regulation of adenylyl cyclase from Paramecium by an intrinsic potassium conductance. Science, 255(5044), 600–603. doi: 10.1126/science.1371017 CrossRefGoogle ScholarPubMed
Takayama, S. and Isogai, A. (2005). Self-incompatibility in plants. Annual Review of Plant Biology, 56(1), 467–489. doi: 10.1146/annurev.arplant.56.032604.144249 CrossRefGoogle ScholarPubMed
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