Post-embryonic Cell Lineages of the Nematode, Caenorhabditis elegans

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

Introduction

The development of a multicellular organism from a unicellular egg involves a complex pattern of repeated cell divisions. Classical observations of nematode embry-ogenesis (reviewed by Chitwood and Chitwood, 1974) revealed that in these organisms early development follows a rigidly fixed program, i.e., an invariant pattern of cell divisions produces specific progeny cells which, in turn, give rise to particular parts of the organism. These and similar studies led to the concept of "cell lineages," in which the ancestry of different organs can be traced back to specific progenitor cells and, ultimately, to the egg (e.g., Wilson, 1925).

In this paper, we extend these observations from the embryonic to the postembryonic period. Many cell divisions occur in the nematode Caenorhabditis elegans after hatching. As in embryogenesis, the pattern of these divisions is rigidly determined; essentially invariant postembryonic cell lineages generate fixed numbers of neurons, glial cells, muscles, and hypo-dermal cells of rigidly specified fates. These lineages reveal the ancestral relationships among specific cells of known structure and function; they thus complement the classical embryology, which defined the ancestral relationships among different organs. We have determined the postembryonic cell lineages by direct observation of living nematodes.

C. elegans is an excellent organism for the study of cell lineages. It is small, easily cultured, and readily amenable to genetic manipulations (Brenner, 1973, 1974). Like other nematodes (e.g., Chitwood and Chitwood, 1974), C. elegans is anatomically simple (Fig. 1). Its tubular body, consisting of a hypodermal wall and an underlying musculature, encloses its digestive and reproductive systems. Although it has most major differentiated tissue types (nerve, muscle, hypodermis, intestine, and gonad), C. elegans consists of relatively few cells; as we show below, the adult contains fewer than 1000 nongonadal nuclei.

Figure 1

Fig. 1  Adult hermaphrodite (above) and male (below), lateral views; bright field illumination. 137 x. Bar= 20 micrometer

The life cycle of C. elegans is rapid; in 3.5 days (at 20oC) it develops from a fertilized egg through four larval stages to a mature adult. Superficially, the newly hatched larva appears to be quite similar to the adult. The most obvious developmental change is in the size and complexity of the gonad, which contains 4 nuclei in the young larva and increases to about 2500 in the mature adult (Hirsh et al., 1976). Gross morphological differences are also apparent in the nongonadal sexual structures of the hermaphrodite and male; these structures are not present in young larvae (Figs. 1 and 2).

Recently, one of us (Sulston, 1976) described a technique with which it is possible to determine cell lineages by observing living nematodes. When appropriately mounted on a thin block of agar on a microscope slide, a nematode proceeds through its normal life cycle. Observation of such animals under Nomarski differential interference contrast optics in the light microscope allows one to directly follow the migrations, divisions, and deaths of individual cells.

Using this technique, we have extended the earlier study (Sulston, 1976) of development in the ventral nervous system of C. elegans. In this paper, we report the complete postembryonic nongonadal cell lineages of C. elegans. These lineages produce the accessory sexual structures of the hermaphrodite and male and lead to other significant developmental changes in the neuronal, muscular, hypodermal, and digestive systems.
To provide a framework for describing the anatomical changes which occur during larval development, we begin with a detailed account of the cellular anatomy of the young nematode. This anatomy has been determined by a combination of Nomarski and electron microscopy.

Figure 2

Fig. 2. Young L1 hermaphrodite, lateral view; Nomarski optics. Montage of photographs of a single living animal. exc, excretory cell; i, intestinal nuclei; vcn, ventral cord neurons. Bar = 20 micrometer.

Readers who do not wish to become submerged in the detailed descriptions under Materials and Methods and Results will find a summary of our observations and conclusions under Discussion.


Adapted by Yusuf KARABEY for WORMATLAS, 2003