Fertilization of Ascidians: Gamete Interaction, Self/Nonself Recognition and Sperm Penetration of Egg Coat

Abstract

Fertilization is one of the most important events in living organisms to generate a new life with a mixed genetic background. To achieve successful fertilization, sperm and eggs must undergo complex processes in a sequential order. Fertilization of marine invertebrate Ciona intestinalis type A (Ciona robusta) has been studied for more than a hundred years. Ascidian sperm are attracted by chemoattractants from eggs and bind to the vitelline coat. Subsequently, sperm penetrate through the vitelline coat proteolytically and finally fuse with the egg plasma membrane. Here, we summarize the fertilization mechanisms of ascidians, particularly from sperm-egg interactions to sperm penetration of the egg coat. Since ascidians are hermaphrodites, inbreeding depression is a serious problem. To avoid self-fertilization, ascidians possess a self-incompatibility system. In this review, we also describe the molecular mechanisms of the self-incompatibility system in C. intestinalis type A governed by three allelic gene pairs of s-Themis and v-Themis.

Mechanisms of Sperm–Egg Interactions: What Ascidian Fertilization Research Has Taught Us

“…As expected, CiVC57 was found to bind to CiUrabin [41]. Therefore, primary binding between sperm and the VC must be mediated by the interaction between CiUrabin and CiVC57 [6,41] (Table 1).…”

“…Many ascidian species show strict self-sterility or preference for nonself fertilization [6,10,[57][58][59][60][61][62]. Upon sperm binding to the VC, the sperm undergo a self/nonself recognition process [6,12].…”

“…Many ascidian species show strict self-sterility or preference for nonself fertilization [6,10,[57][58][59][60][61][62]. Upon sperm binding to the VC, the sperm undergo a self/nonself recognition process [6,12]. Regardless of the lack of adaptive immunity in ascidians (Urochordate), how can ascidian sperm distinguish between self and nonself eggs?…”

“…His findings implied that sperm glycosidase (hyaluronidase) and protease (acrosin) may be lysins in mammalian spermatozoa. Since then, it has long been believed that the acrosomal trypsin-like protease acrosin [5,6,12,23] is a lytic agent lysin that is released by acrosomal exocytosis and digests the ZP, creating a small hole for the sperm passage of the ZP [101,102]. However, such a function of sperm acrosin has been debated, as sperm binding to the ZP but not sperm penetration of the ZP was strongly inhibited by several trypsin inhibitors [103].…”

“…Generally, animal fertilization consists of five steps: (1) sperm activation and chemoattraction to the eggs; (2) sperm binding to the proteinaceous egg coat, together with xenogeneic recognition (species-specificity) and allogeneic recognition (self/nonself recognition) processes between gametes; (3) sperm activation and/or acrosome reaction (AR), an exocytosis of the acrosomal vesicle (occasionally, step (3) precedes step (2)); (4) sperm penetration of the egg coat; and (5) gamete fusion [1][2][3][4][5][6][7][8][9] (Figure 1). In the present review, we summarize the historical view and our current understanding of the mechanisms of fertilization.…”