Oogenesis in Caenorhabditis elegans

Abstract

Background: The nematode, Caenorhabditis elegans has proven itself as a valuable model for investigating metazoan biology. C. elegans have a transparent body, an invariant cell lineage, and a high level of genetic conservation which makes it a desirable model organism. Although used to elucidate many aspects of somatic biology, a distinct advantage of C. elegans is its well annotated germline which allows all aspects of oogenesis to be observed in real time within a single animal. C. elegans hermaphrodites have two U-shaped gonad arms which produce their own sperm that is later stored to fertilise their own oocytes. These two germlines take up much of the internal space of each animal and germ cells are therefore the most abundant cell present within each animal. This feature and the genetic phenotypes observed for mutant worm gonads have allowed many novel findings that established our early understanding of germ cell dynamics. The mutant phenotypes also allowed key features of meiosis and germ cell maturation to be unveiled.

Summary: This review will focus on the key aspects that make C. elegans an outstanding model for exploring each feature of oogenesis. This will include the fundamental steps associated with germline function and germ cell maturation and will be of use for those interested in exploring reproductive metazoan biology.

Key messages: Since germ cell biology is highly conserved in animals, much can be gained from study of a simple metazoan like C. elegans. Past findings have enhanced understanding on topics that would be more laborious or challenging in more complex animal models.

Keywords: Caenorhabditis elegans; Development; Oocyte meiotic maturation; Oogenesis.

Fig. 1.

Overview of C. elegans development. a Differential interference contrast (DIC) microscopy of a live adult hermaphrodite, highlighting one gonad arm. The gonad arm is outlined by a dotted black line. The top left-hand side of the image shows a one-cell embryo in the uterus, followed to the right by the spermatheca, where sperm is stored and through which oocytes are ovulated. The proximal end of the gonad contains oocytes awaiting fertilisation. The gonad bends itself in the “loop” region where germ cells are in the pachytene stage of meiotic prophase I. Germ cells are only partially enclosed in a plasma membrane and share a common cytoplasm called the rachis. Individual germ cells are located on the edge of the gonad tube. The dotted white line in the meiotic syncytium indicates the location of the gonad cross-section shown in the box (the black dotted line indicates the focal plane of the DIC image). The distal end of the gonad arm is out of view to the left of the image. b Cartoon outline of embryonic germline development. The light pink corresponds to germ plasm, and dark pink dots denote germ granules. The germ plasm/granules are segregated into the germline precursor cells. The Z2 and Z3 germ cells will each develop into adult gonads. c Cartoon graphic of larval and adult hermaphrodite gonadal development. Germ cell proliferation begins during the mid-first larval stage (L1) and significantly increases during the later larval stages. During the fourth larval stage (L4), sperm is produced. In adulthood, sperm production ceases, and germ cells exclusively develop into oocytes. The distal tip cells (DTC) are shown in red, regions of germ cell mitotic proliferation in yellow, the meiotic region in green, sperm in blue, oocytes in pink, and embryos in the uterus in purple. Adapted from Hubbard and Greenstein [2005].