Ascidian Sexual Reproductive Strategies: Mechanisms of Sperm-Egg Interaction and Self-Sterility
Ascidians (protochordate) are hermaphrodites that release sperm and eggs nearly simultaneously. However, self-fertilization is prohibited by self-sterility mechanisms during interaction between sperm and the vitelline coat (VC) of the eggs in many ascidian species, including Ciona robusta(former name: Ciona intetsinalis type A) and Halocynthia roretzi. A recent genetic study in C. robusta revealed that two tightly linked gene pairs in loci A and B, i.e., the sperm PKDREJ-like receptor s-Themis-A and the VC fibrinogen-like ligand v-Themis-A, and s-Themis-B and v-Themis-B, which include highly variable regions among individuals, are responsible for self-recognition. Sperm recognizes an egg as a self-egg when both alleles of s/v-Themis-A and s/v-Themis-B possess the same haplotypes. When attached to the VC of self-eggs, acute and drastic Ca2+ influx takes place in the sperm head and flagella probably via the Ca2+-conducting cation channel in the C-terminal region of s-Themis-B, which results in sperm detachment from the VC or decrease in sperm motility. We recently identified v-Themis-like, an acid-extractable VC protein with no allelic polymorphism, as a new candidate that participates in self-sterility. This self-sterility mechanism is closely related to the self-incompatibility systems in angiosperms. A different ascidian, Halocynthia roretzi, utilizes a different self/nonself-recognition system during fertilization, using an EGF-like repeat-containing VC protein, HrVC70. Moreover, the genome database of H. roretzi contains four pairs of s/v-Themis homologs. These gene products may also play a role in self-sterility in this species. This chapter describes the historic and current understandings of the mechanisms of gamete interaction and self/nonself-recognition in ascidian fertilization.
KeywordsSperm Sperm-egg interaction Self/nonself-recognition Self-sterility Self-incompatibility Ascidian
This study was supported in part by Grant-in-Aids for Scientific Research on Innovative Areas from MEXT, Japan to HS (21112001, 21112002).
- 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 EK, Piette J, Racioppi C, Ristoratore F, Sasakura Y, Takatori N, Brown TC, Delsuc F, Douzery E, Gissi C, McDougall A, Nishida H, Sawada H, Swalla BJ, Yasuo H, Lemaire P (2015) Aniseed 2015: a digital framework for the comparative developmental biology of ascidians. Nucleic Acid Res 44(D1):D808–D818CrossRefGoogle Scholar
- Fuke TM (1983) Self and nonself recognition between gametes of the ascidian, Halocynthia roretzi. Roux’s Arch. Dev Biol 192:347–352Google Scholar
- Fukumoto M (1988) Fertilization in ascidians: apical processes and gamete fusion in Ciona intestinalis. J Cell Sci 89:1890196Google Scholar
- Fukumoto M (1990c) Morphological aspects of ascidian fertiizattion. Zool Sci 7:989–998Google Scholar
- Sawada H, Akasaka M, Yokota N, Sakai N (2005) Modification of ascidian fertilization related gamete proteins by ubiquitination, proteolysis, and glycosylation. In: Tokumoto T (ed) New impact on protein modifications in the regulation of reproductive system. Research Signpost, Trivandrum, pp 61–81Google Scholar
- Sawada H, Mino M, Akasaka M (2014a) Sperm proteases and extracellular ubiquitin-proteasome system involved in fertilization of ascidians and sea urchins. In: Sutovsky P (ed) Posttranslational protein modifications in the reproductive system, Advances in Experimental Medicince and Biology, vol 759. Springer, New York/Heidelberg/Dordrecht/London, pp 1–11Google Scholar
- Vacquier VD, Sawanson WJ (2011) Selection in the rapid evolusion of gamete recognition proteins in marine invertebrates. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a002931
- Voskoboynik A, Newman AM, Corey DM, Sahoo D, Pushkarev D, Neff NF, Passarelli B, Koh W, Ishizuka KJ, Palmeri KJ, Dimov IK, Keasar C, Fan HC, Mantalas GL, Sinha R, Penland L, Quake SR, Weissman IL (2013) Identification of a colonial chordate histocompatibility gene. Science 341:384–387CrossRefGoogle Scholar