The buccal capsule of Caenorhabditis elegans (Nematoda: Rhabditoidea): an ultrastructural study

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

Discussion

Although the classical divisions of the rhabditid buccal capsule (i.e. cheilostom, prostom, mesostom, metastom, and telostom) can be recognised at the ultrastructural level in Caenorhabditis elegans, only the distinction between the cheilostom and prostom is marked by a discontinuity of cuticles of different types (i.e. contact of the body wall and esophageal cuticles). Since the cuticle of the rest of the buccal capsule is continuous, showing only internal differences in density, the identification of discrete rhabdions (implying separately formed plates) as composing the walls of the buccal capsule seems untenable. Denser differentiations of the cuticle seem to be related to the degree of attachment of cuticle to underlying cells.

The prostom region is underlain by two rings of syncytial cytoplasm whose cell bodies lie considerably further back, outside the limits of the esophagus as defined by its prominent basal lamina. These can probably be equated with arcade tissue or arcade cells identified earlier in Ascaris (as reviewed in De Coninck 1965). However, similar arcade tissues were not identified in some other nematodes studied recently, notably Nippostrongylus brasiliensis (see Wright 1976). Perhaps the development of this tissue varies in different nematode groups. For example, is it possible that arcade "cells" have given rise to intrinsic musculature of the buccal capsule in the nematodes with "stomatous buccal capsules" (Wright 1976)?

Although contemporary nematologists often refer to the esophagus as being a stomodeum, and hence presumably derived as a rather late embryological process of ectodermal invagination into the developing embryo, it has also been suggested that a true stomodeal invagination may occur only in certain groups (Wright 1976). This may appear in adult forms as an infolding of hypodermis and its attendant body type of cuticle into the functional buccal capsule of the nematode. On this basis, the cheilostom of C. elegans, the only component of the buccal capsule lined by body cuticle, seems to be the only candidate to be considered as a stomodeal invagination. In comparison with other groups (Wright 1976), the cheilostom seems too superficial to be considered a true stomodeum. Recent studies of early embryogenesis in C. elegans (J. E. Sulston, E. Schierenberg, and G. Von Ehrenstein, unpublished data) have found that precursor cells for both esophagus and buccal cavity move inwards from the ventral position with no invagination process. Furthermore, arcade tissues have been found to be lineage related primarily to the esophagus.

Observations on the moulting of the buccal capsule, given here, may also indicate that arcade tissue is more related to esophagus than to hypodermis. The production of body cuticle (apolysis and new cuticle formation) precedes that of the esophagus. Whereas the process of apolysis of body cuticle results simply in the release of the intact body cuticle, apolysis of buccal capsule and esophagus cuticle (prostom as well as the remainder of the buccal cuticle) is followed by extensive breakdown of the cuticle followed by formation of new cuticle. Furthermore, formation of esophageal and buccal cuticle (exclusive of the cheilostom) is characterized by the build up of dense granules in the cuticle forming cells. This characterizes arcade cytoplasm as well as epithelial, muscle, and marginal cells of the esophagus proper, but not body wall hypodermis. Anterior hypodermal cytoplasm retracts from the old cuticle to form the new lip and cheilostom cuticle. Although the anterior arcade cytoplasm also retracts, it does so later, coordinated with apolysis of the esophageal cuticle. It seems that arcade cells do not originate as an ectodermal stomodeum. In the terminology suggested by Wright (1976) C. elegans buccal capsule would be "astomatous."

Although functional aspects of the buccal capsule will be considered separately, it may be noted here that somatic muscles are not modified to operate the buccal capsule as shown in some other nematodes with astomatous buccal capsules (Wright 1976). The attachment of somatic muscles to the body wall at the base of the lips presumably allows these muscles to manipulate the tip of the nematode's head giving delicate, seemingly probing activities resulting in passive bending of the buccal capsule. The flexibility of the buccal cuticle is more apparent in larvae where the length-width ratio of the buccal capsule is greater.


Adapted by Yusuf KARABEY for WORMATLAS, 2003