The Postembryonic Cell Lineages of the Hermaphrodite and Male Gonads in Caenorhabditis elegans

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Table of contents  -  Abstract  -   Introduction  -   Materials & Methods  -   Results  -   Discussion  -   References

Introduction

How the developmental history of a cell influences its capacity to differentiate persists as one of the central questions in developmental biology. Cell lineages pose this fundamental question in a framework that permits an analysis of specific developmental events. Classically, cell lineage studies were used to explore the organization of the zygote and the basis of cell determination during embryogenesis. From these studies came the idea that many eggs are mosaics of cytoplasmic determinants that are distributed to specific cells by an invariant pattern of cell divisions (see Wilson, 1925).

The nematode Caenorhabditis elegans is an excellent organism for lineage studies because it has a limited number of cells and is genetically well defined (Brenner, 1974). Since C. elegans is transparent, individual cells can be distinguished microscopically and followed in living worms. The genetic control of lineage patterns can be studied using mutations that alter known lineages. Such mutations also provide a means of perturbing the normal pattern to investigate how changes in cell divisions or positions affect subsequent development. A similar method of approach to the genetic control of cell lineages was used by Lees and Waddington (1942) using the bristle lineage in Drosophila as a model system. However, they were required to infer developmental events from fixed specimens.

Considerable work has already been done on lineages in C. elegans. A description of the Postembryonic nongonadal lineages has been completed (Sulston and Horvitz, 1977), and work on the embryonic lineages is in progress (Deppe et al., 1978). Laser ablation experiments have demonstrated that cells are rigidly determined in at least some lineages (Sulston and Horvitz, 1977). Analysis of a lineage mutant in C. elegans has shown that nerve precursor cells blocked in division are still capable of exhibiting the differentiated phenotypes of their descendants (Albertson et al., 1978).

Previous studies in our laboratory have included a morphological description of the developing gonads in hermaphrodites and males (Hirsh et al, 1976; Klass et al, 1976), and the isolation of temperature-sensitive gonadogenesis-defective mutants (Hirsh and Vanderslice, 1976). This paper presents the postembryonic gonadal lineages of C. elegans. The lineages of the germ line progenitor cells are variable from worm to worm, and are discussed only briefly here. Although clonal information may be relevant to the generation of oocytes and sperm, other methods, such as laser ablation of precursor cells, will be necessary to elucidate the germ line lineages. By contrast, the lineages which generate the somatic structures of the gonad proceed according to an essentially invariant pattern.

The lineages that give rise to the somatic structures of the gonad are of particular interest because they display a complete program of development from only two cells, which are present when the worm hatches, to multiple cell types that are organized into discrete organs in the adult gonad. Although the embryonic ancestry of the two somatic progenitor cells is not known in C. elegans, Pai (1927) reported that the equivalent two cells of another nematode, Turbatrix aceti, arose from an embryonic stem cell, S5, as sisters. Since work on the embryonic lineage of C. elegans is in progress (Deppe et al., 1978), the complete lineage of these structures should be known. Another interesting aspect of this lineage is that the two cells follow one developmental pattern in the hermaphrodite and another in the male, so that a comparison of homologous programs is possible.


Adapted by Yusuf KARABEY for WORMATLAS, 2003