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

Takako Saito,Hitoshi Sawada

doi:10.3389/fcell.2021.827214

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.

Highlights

Fertilization of marine invertebrates has been extensively studied in classical research
After sperm binding to the vitelline coat (VC), gametes undergo a judgment of self- or nonself-gametes using three allelic protein pairs of s-Themis and v-Themis, and only self-recognized sperm are rejected because self-recognition triggers the SI response (Figure 2B). s/v-Themis homologous genes were identified in self-sterile species, such as H. roretzi and C. savignyi
The proteasome inhibitors MG115 and MG132 inhibited the fertilization of intact eggs but not VC-free eggs (Sawada et al, 1998). These inhibitors showed no appreciable inhibition of sperm binding to the VC of glycerinated eggs. These results suggest that the proteasome plays a key role in sperm penetration through the VC but not in sperm binding to the VC (Figure 2B)

Summary

INTRODUCTION

Fertilization of marine invertebrates has been extensively studied in classical research. The marine invertebrate Ciona intestinalis type A [another name: Ciona robusta (Brunetti et al, 2015)] is one of the model animals used to study many fields of biology, including reproductive biology (Sawada et al, 2001). Ascidian fertilization consists of five major steps: 1) sperm chemotaxis, 2) sperm binding to the VC, 3) self/nonself-recognition, 4) sperm penetration through the VC, 5) gamete fusion (Figure 1), similar to the fertilization processes as previously reviewed (Vacquier and Swanson, 2011; Gallo and Costantini, 2012). In C. intestinalis (type A), spermatozoa are attracted toward the eggs by sperm attractant SAAF, a sulfated steroid 3,4,7,26-tetrahydroxycholestane-3,26-disulfate (Yoshida et al, 2002). Transient intracellular Ca2+ increase is induced by SAAF gradient (Shiba et al, 2008), which is

Fertilization of Ascidians

GAMETE INTERACTION

Findings

CONCLUDING REMARKS