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The general form of the buccal capsule is well seen in living animals studied by interference microscopy (Fig. 1). The most obvious unit is a subtriangular cylindroid recessed slightly from the oral opening. The basal half of the cylindroid is surrounded by a thin collar-like extension of the esophagus, and its base is embedded directly in the anterior esophagus. In the base, three triangular flaps occur. The triradiate esophageal lumen continues from the base of the buccal capsule and the large tubular radii of the esophagus' procorpus lumen thus open to the base of the buccal capsule. The dorsal esophageal gland opens into the esophageal lumen just where the lumen begins to assume a triradiate form.
FIG. 1. Interference photomicrograph of the buccal capsule of a living adult Caenorhabditis elegans. The dorsal metastomal flap (a) is seen in edge view, and a subventral flap (b) is seen in face view. The cheilostom-prostom limit is noted by the short line. Asterisk notes prominent refractile cuticle of the telostom. X2000. FIG. 2. Longitudinal section through the buccal capsule of an adult. The classically identified regions of the buccal capsule are the cheilostom (C), prostom (P), mesostom (M), metastom (M'), and telostom (T). Prostom cuticle is underlain by anterior (a') and posterior (a") arcade tissue. Mesostom cuticle is underlain by the anterior epithelial cells of the esophagus (e), and muscle cells m1 and m2 underly cuticle of the metastom and telostom respectively. Muscle cell m3 comprises the procorpus of the esophagus. Asterisk identifies the telostom cuticle that is refractile in light microscopy. The anterior tip of a somatic muscle is noted on the right (arrow), x 11 000.
Electron micrographs clearly show that body wall cuticle lines the inner surface of the lips and makes a discrete contact with the cuticle that forms the prominent cylindroid (Figs. 2 and 3).
FIG. 3. Detail of the contact (large arrow) of body wall (cheilostom) cuticle and esophagus (prostom) cuticle. Note the contact of anterior arcade tissue with body wall hypodermis and the posterior arcade tissue (small arrows). Asterisk notes a posteriorly directed process of the anterior arcade tissue. Note also the infolded groove in the cheilostom cuticle, x 58 000. FIG. 4. Section through the dense "corner" of the buccal cuticular cylindroid. Arcade tissue appears to be more strongly attached to cuticle here, with many cytoplasmic filaments along the inner membrane. Asterisk notes a posteriorly directed process of the posterior arcade tissue lying outside the esophagus, x 26 500.
Cuticle of the lips is underlain by thin processes of hypodermal cytoplasm. At the contact with the cuticular cylindroid the hypodermis forms a continuous junctional complex (belt junction) with a ring of cytoplasm that encircles the buccal cuticle. This latter cytoplasm extends only 1.5 micrometer posteriorly, where continuous junctions join it to a second ring of cytoplasm that similarly encloses the buccal cuticle and about 2 micrometer posteriorly contacts the esophagus proper (Figs. 3, 4, and 5). The two units of cytoplasm with their associated cell processes will be referred to as the anterior and posterior arcade tissue. In the intermoult stage, arcade cytoplasm contains few mitochondria and scanty endoplasmic reticulum or other organelles, although there are numerous circularly oriented filaments in the cytoplasm. As these are prominent in worms fixed only in osmium it is likely that they are a class of tonofilaments (intermediate filaments) rather than actin. Many filaments appear to insert obliquely into the junctional complexes between cells.
FIG. 5. Cross section through the buccal cuticle just above the level of the prostom-mesostom change showing the shape of the cuticle with three dense "corners." At this level the posterior arcade cytoplasm (asterisks) entirely surrounds the cuticle while some of the anterior arcade cytoplasm (arrows) lies just outside it. x 15 000.
The anterior arcade cytoplasm gives rise initially to four posteriorly directed cell processes, three in the subdorsal fields and one in the ventral. The processes lie outside the esophagus (Fig. 4). One of the subdorsal processes soon ends and the remaining processes move laterally to lie, one in the dorsal aspect of each lateral hypodermal chord and one in the ventral chord. Cell bodies of these processes occur in the inner aspects of these chords (not in contact with cuticle) about 50 micrometer from the head where the tubular radii of the esophageal lumen end. Cell processes arising from the larger posterior arcade cytoplasm originate rather symmetrically as a dorsal and a ventral process, and as four processes one on either side of the lateral chords. As they progress posteriorly, the dorsal and right dorsolateral processes fuse, but again separate and connect ultimately to two cell bodies. The right ventrolateral process terminates at the level of the anterior procorpus. Considerably posterior to this the ventral process bifurcates. Thus, six cell processes were ultimately traced to cell bodies, one dorsally, one just above the right lateral hypodermal chord, one just above and one below the left lateral hypodermal chord, and two (from the bifurcated cell process) at either margin of the ventral hypodermal chord. These cell bodies lie just behind those of the anterior arcade tissue (see diagram, Fig. 6).
FIG. 6. Diagram of arrangement of syncytial arcade tissues, with connected cell bodies. Syncytia have been opened along the dorsal line. Cross hatched areas indicate lateral hypodermal chords.
The remainder of the cuticle of the buccal capsule is enclosed by cells of the esophagus. The entire esophagus is sheathed by a conspicuous basal lamina. The nine most anterior epithelial cells of the esophagus (described by Albertson and Thomson 1976) form the esophageal collar that surrounds the basal part of the cylindroid cuticle while the first two muscle cells (m1 and m2 of Albertson and Thomson (1976)) underly the buccal cuticle where it changes shape to the triradiate lumen of the procorpus (Fig. 2).
Although the cuticle of the buccal capsule is continuous from the point where it makes contact with body wall cuticle throughout the entire lining of the esophagus, it displays internal differentiations that can be readily equated with the regions of the buccal capsule recognised in taxonomic studies (Fig. 2). Thus, the cheilostom is that region enclosed by the lips and lined by body cuticle. The prostom and mesostom compose the subtriangular cylindroid cuticle. The presence of densities that traverse the cuticle in the region enclosed by the esophagus' epithelial cells allows distinction of the mesostom from prostom. However, throughout the prostom and mesostom the cuticle at the subdorsal and ventral apices of the "triangle" is also dense (Figs. 4 and 5). The anterior rim of the prostom cuticle projects inward as a slight flange into the anterior lumen of the buccal cavity. The metastome is that region from which the three triangular flaps arise. The cuticle is uniformly dense and is underlain by the m1 muscle cell. Just below this the cuticle has a less dense region in dorsal and subventral sectors that is responsible for the prominent retractile spots noted by light microscopy. This area and the remaining dense cuticle underlain by the m2 muscle cells can be recognised as the telostom.
Densities in the mesostomal cuticle are coincident with rows of small hemidesmosomes and tonofilament bundles that traverse the esophagus epithelial cells. These cells are apparently tightly adherent to the cuticle, whereas arcade cytoplasm may adhere mainly only along the dense apices of the "triangular" cuticle.
Myofilaments of the m1 muscle cell, which forms a complete ring around the front of the esophagus, converge from the outer membrane to the inner cell membrane at the anterior base of the metastomal flaps. Similarly, myofilaments of m2 muscle cells converge on the lumenal membrane just below the metastomal flaps. The dorsal esophageal gland duct opens into the buccal capsule by penetrating through the dorsal m2 cell. Cuticle of the esophagus lumen projects into the end of the gland cell forming a fluted cuticular end apparatus similar to that in tylenchid nematodes (Anderson and Byers 1975; Baldwin et al. 1977).
The anterior eight somatic muscle cells of the body wall extend to a level slightly above the prostom-mesostom transition (about 4 micrometer from the tip). The tip of each muscle is attached to the adjacent hypodermis by denser and more filamentous external laminas and the hypodermis has bundles of tonofilaments traversing its cytoplasm between densities on inner and outer cell membranes. This attachment occurs just at the outer posterior edge of the lips (Figs. 2 and 4).
Observations on moulting
The present report does not consider in detail all of the aspects of formation of the buccal capsule but aims at determining the manner in which various cells participate in this process. Early stages in the moulting process (as identified by Singh and Sulston (1978)) in which secretory activity is detectable in hypodermal seam cells show that the original cuticle separates from the body wall (apolysis), and new cuticle is laid down, closely following the contours of the hypodermal cell membrane. At the same time the hypodermal cytoplasm in the tip of the head retracts so that no cell processes extend beyond the anterior lip-like rim of the prostom (Fig. 7). Retraction of this cytoplasm results in deepening of the groove in the inner surface of cheilostom cuticle just before its contact with prostom cuticle. New body wall cuticle forms along the outer surface of the retracted hypodermal cytoplasm, which appears to be rolled inwards, with a deep groove formed between hypodermal cytoplasm and arcade cytoplasm (Fig. 7). At this stage, cuticle of the buccal capsule has not undergone apolysis and both arcade cytoplasm and cells of the esophagus proper are in close contact with the original cuticle. The nematodes continue to feed. Both arcade cytoplasm and esophageal cells contain dense granules in their cytoplasm. As new body cuticle is deposited, the number of granules increases in arcade and esophageal tissues. Neither anterior nor posterior rings of arcade cytoplasm contain identifiable ribosomes or endoplasmic reticulum. However, granules occur in the posteriorly directed cell processes, and arcade cell bodies are enlarged, contain granular endoplasmic reticulum, and their Golgi apparati have associated dense granules. Similarly, there appear to be more cytoplasmic ribosomes in the epithelial cells of the esophagus. Small clusters of vesicles (perhaps Golgi apparati), but lacking dense granules, do occur in the epithelial cells. However, granules are more prominent in their cell processes that project backward to cell bodies lying within the limit of the esophagus (Albertson and Thomson 1976), These may be the major site of granule synthesis in epithelial cells and arcade tissue. Granular endoplasmic reticulum and cytoplasmic ribosomes become prominent in both muscle cells and marginal cells of the remainder of the esophagus but myofilaments remain throughout the moulting period.
FIG. 7. An early stage in the L4 to adult moult. Hypodermis from the head has retracted from its cuticle (open arrow). Note position of dense material (asterisk) in cheilostom cuticle and deepened cheilostom groove. Small arrows indicate the deep groove formed between arcade cytoplasm and hypodermis. Granules (g) are evident in arcade tissue, epithelial cells and muscle cells of the esophagus, x 12000.
The membrane of arcade tissues finally separates from the cuticle leaving a clear space. Similarly, the membrane of epithelial cells, marginal cells, and muscle cells of the esophagus separates at small areas as hemidesmosome connections along the membrane disappear.
Later stages of moulting are characterised by a general lethargy in the animal and a lack of esophageal activity as seen in contractions of the posterior bulb. At the same time the mouth opening seems to be "closed". New body cuticle formed around the retracted anterior hypodermal cytoplasm is thicker while the old lip cuticle appears to have been inflated (Fig. 8). The previously deepened fold of the cheilostom cuticle has opened out so that this cuticle now bulges inwards leaving only a very narrow channel into the buccal cavity.
FIG. 8. A later stage of moulting when much of the body cuticle has been formed. The mouth is occluded by inflation of old cuticle with loss of the cheilostomal groove and forward movement of densities in cheilostom cuticle (asterisk). Granules are evident in arcade cytoplasm and epithelial cells of esophagus. On the right, anterior arcade tissue has retracted from old prostom cuticle. Arrow notes the anterior limit of arcade tissue which is also the level of the new prostom rim when it is formed later. Dense granular material occurs between old buccal cuticle and cell surfaces x 19 800.
In a later stage, when body cuticle is more completely formed, apolysis of the entire buccal capsule and esophagus cuticle has taken place and the space between the old buccal cuticle and underlying cells is occupied by dense granular material (Fig. 8). Dense granules still occur in both arcade and esophageal cytoplasm. As new buccal and esophageal cuticle forms, the dense granules disappear and the old cuticle becomes progressively thinner. Multivesicular bodies, characteristic of the hypodermis during body wall cuticle formation, do not occur in arcade or esophageal tissue during buccal cuticle formation. After apolysis the contour of the anterior epithelial collar of the esophagus changes so that it tapers more gradually into the esophagus. This appears to be related to the disappearance of tonofilament insertions along the inner epithelial membrane.
Apparently when the mouth closes, the anterior arcade cytoplasm begins to retract from the anterior margin of the prostom cuticle. Thus the newly formed rim of the prostom cuticle occurs posterior to the old, but at a level "appropriate" to the newly forming cheilostom and lip cuticle, being made over the retracted anterior hypodermis (Fig. 8).
Adapted by Yusuf KARABEY for WORMATLAS, 2003