Genes required for the common miracle of fertilization in Caenorhabditis elegans

Abstract

Fertilization involves multiple layers of sperm-egg interactions that lead to gamete fusion and egg activation. There must be specific molecules required for these interactions. The challenge is to determine the identity of the genes encoding these molecules and how their protein products function. The nematode worm Caenorhabditis elegans has emerged as an efficient model system for gene discovery and understanding the molecular mechanisms of fertilization. The primary advantage of the C. elegans system is the ability to isolate and maintain mutants that affect sperm or eggs and no other cells. In this review we describe progress and challenges in the analysis of genes required for gamete interactions and egg activation in the worm.

Fertilization and the oocyte-to-embryo transition in C. elegans

“…Egg activation results in the completion of meiosis, polar body formation, cytoskeletal reorganization, and the secretion of chitinous eggshell (27). The egg then begins embryogenesis while passing through the uterus and is eventually laid and hatched (8).…”

“…Additionally, reverse genetic approaches, including RNAi treatment or gene knockout, are also viable options to study gene function. Unfortunately, many genes are refractory to RNAi and sperm genes are particularly insensitive to RNAi mediated knockdown (8,31). A large number of "sterile" mutants have been isolated in C. elegans with the potential defects in gametogenesis, germline development and proliferation, or embryonic development (8,31,32).…”

“…Sperm-sterile mutants are referred to as spe for spermatogenesis defective or fer for fertilization defective, and egg-sterile mutants are referred to as egg (8,(31)(32)(33). spe and fer mutants are equivalent to paternal infertility and these mutants produce spermatocytes, spermatids, and/or sperm whose functions are aberrant during spermatogenesis, spermiogenesis, and/or fertilization.…”

“…The mouse model system has been particularly important for understanding the genetics and molecular basis of fertilization because of the ability to create gene-specific knockout mice and to study gamete function and development in a defined in vitro system (7). More recently, the nematode Caenorhabditis elegans has emerged as a valuable model system to understand fertilization and early development (8). C. elegans is an ideal model organism for studying fertilization and the oocyte-toembryo transition because it has a short reproductive cycle (~3.5 days), produces a large number of progeny, and is transparent, which allows for the direct observation of oocyte development, ovulation, fertilization, and early embryogenesis in intact animals (9).…”

“…Fertilization in C. elegans shares many characteristics with mammalian fertilization, including the need for sperm activation in the female reproductive tract, internal fertilization and multiple egg activation events including a membrane block to polyspermy, cortical granule (CG) exocytosis, meiotic resumption, and activation and degradation of selected maternal mRNAs and proteins (Table 1) (1,8,13). In this review, we will discuss C. elegans as a model system for fertilization and the oocyte-to-embryo transition.…”