ALIMENTARY SYSTEM
PHARYNX

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1 Overview

C. elegans feeds on bacteria in liquid suspension. Bacteria taken in by the mouth are concentrated, ground and transported to the intestine by a tube-like muscular pump called the pharynx. The pharynx is an epithelial organ that has its own muscles, nervous system, gland cells and structural cells. It contains 9 epithelial cells, 20 muscle cells, 9 marginal cells, 4 gland cells and 20 neurons (PhaFIG 1), and 6 valve cells at its posterior (see also PharynxAtlas). It is about 100 μm long and has a diameter of approximately 20 μm at its widest (at the posterior bulb). At the anterior, it is connected to the buccal cavity and at the posterior, to the intestine. The pharynx is isolated from the rest of the animal by a specialized basal lamina that lines the basal surface of the pharyngeal cells and isolates the pharynx from the pseudocoelom. There may be hormonal signaling between this organ and the rest of the body by way of the pseudocoelomic fluid; otherwise, the two systems appear to operate almost independently. The apical surface of the pharyngeal cells lies medially towards the lumen, which is lined with a cuticle secreted by the pharyngeal muscle and marginal cells. At several locations pharyngeal cuticle takes the form of specialized structures, such as the anterior “flaps”, the “sieve” and the “grinder” (PhaFIG 2; see Cuticle) (Avery and and Thomas, 1997).

PhaFIG 1 Cell nuclei positions in the pharynx
PhaFIG 1: Cell nuclei positions in the pharynx. (Based on drawing by Ron Ellis.) (Red) Neuron nuclei; (green) pharyngeal muscle nuclei; (lavender) gland nuclei; (fuchsia) marginal cell nuclei; (purple) epithelial nuclei. A. Graphic rendition; left lateral view of the ventral, left-side and dorsal nuclei. B. Graphic rendition; left lateral view of the right-side nuclei.
Note: More recent studies showed that the identification of g1AL and pm5VL on the left side and g1AR and pm5VR on the right side were switched. This is a corrected image (pers. comm. L. Avery).

PhaFIG 2 Pharynx anatomy
PhaFIG 2: Pharynx anatomy. A. Graphic rendition of the pharynx. The metacorpus is also called the anterior bulb or the first bulb. The posterior bulb is also called the terminal bulb or the second bulb. At the anterior end, the pharynx is connected to the buccal cavity. At the posterior end, it is connected to the intestine through the pharyngeal-intestinal valve (vpi). B-F. TEM sections through various parts of the pharyngeal lumen. Section levels are indicated in G. B. Buccal cavity at the level of the pharyngeal epithelial cells. (Image source: N2T [MRC] A60-23.) C. Procorpus. The channels (arrows) are seen at the three corners of the lumen. (Image source: N2W [MRC] A386-2.) D. Metacorpus at the level of the two ventral gland (Gl) openings and M3 cell bodies. Bacteria (arrows) are seen in channels while the rest of the lumen is structured as a sieve. (Image source: [MRC] JSA-71.) E. Posterior of the isthmus at the level of the excretory duct. (Image source: N2S [MRC] A1-4.) F. Grinder in the terminal bulb. (Image source: [MRC] JSA.) G. DIC micrograph of the pharynx.

The pharynx has intrinsic myogenic activity that is regulated by its nervous system. The nervous system, in turn, integrates internal signals such as the animal’s nutritional status and external signals such as the presence or absence of food (Avery and Horvitz, 1989; Franks et al., 2006). In the absence of food, the pharynx pumps approximately once every second, whereas in the presence of food the rate increases to about four pumps per second. Also, a well-fed worm suspended in liquid will pump only in the presence of bacteria, whereas a starved worm keeps pumping, albeit slowly and irregularly, in the absence of food and accelerates its pumping in the presence of lower amounts of bacteria compared to a well-fed worm (Avery et al., 1993). The pumping rate of the pharynx is also modulated by the somatic sensory system; for example, pumping is briefly inhibited upon sensing a light touch to the body (Chalfie et al., 1985; Avery and Thomas., 1997).

The pharynx has a distinctive shape; an extended anterior portion (procorpus) is connected to the buccal cavity via the pharyngeal epithelium (Albertson and Thomson, 1976; Franks et al., 2006). The metacorpus, also called the first bulb, lies posterior to the procorpus. The procorpus and metacorpus together make the corpus of the pharynx. Between the corpus and the second bulb (also called the terminal bulb) lies the isthmus (PhaFIG 2). The large somatic nerve ring surrounds the isthmus on the outside.



2 Embryonic Development of the Pharynx

Unlike the intestinal cells, all of which arise from a single founder cell E, the pharynx is composed of cells that arise from both AB and MS founder cells (AlimFIG 1). In these lineages, no strict clonal and lineal derivation can be recognized, and there is a heterogeneity of ancestry with respect to the final cell fate (PhaMOVIE 1&2). In the anterior divisions, no lineal boundaries exist between hypodermal, arcade and pharyngeal daughters. The pharyngeal components derived from MS and AB do not possess any functional boundaries either, such that in pm3, pm4 and pm5 muscle groups identical cells arise from these two lineages and some MS descendants fuse with those coming from the AB blast cell (Sulston et al., 1983; Horner et al., 1998).

During gastrulation, at approximately the 100-cell stage and after the movement of gut precursors to inside of the embryo, MS descendants start to move inward through the blastopore (AlimFIG 1 and PhaFIG 3) (Bucher and Seydoux, 1994; Mango, 2007). Slightly later, AB-derived precursors of the pharynx move inside of the embryo. When gastrulation is completed about 330 minutes after fertilization, pharyngeal precursors come to lie in the form of a compact ball-like primordium, surrounded by hypodermal and neuronal precursors on the outside. These cells are attached to each other and to the midgut by adherens junctions. However, they are not yet attached to the buccal cavity (see Epithelial System - Hypodermis) (Portereiko and Mango, 2001). At this time 78 of the 80 pharyngeal cells are already born. During the next hour, pharyngeal extension occurs such that the pharyngeal precursors reposition themselves to form a central cylinder and link to the buccal cavity, whereas the body myoblasts position themselves between this cylinder and the outer layer of cells. Pharyngeal extension is accomplished in roughly three steps; reorientation, epithelization and contraction (see Epithelial System - Hypodermis) (Portereiko and Mango, 2001). Later, the pharyngeal tube morphs into a bilobed structure and develops a lumen. Lumen formation is thought to be performed by retraction of the tips of the marginal cells from the midline of the pharyngeal primordium when the pharyngeal muscles differentiate and contract (PhaFIG 3) (Leung et al., 1999). Cell fusions in the pharynx occur either before or soon after hatching (Sulston et al., 1983). C. elegans initiates pharyngeal pumping right before hatching.

1A 1B
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PhaMOVIE 1A&B and PhaMOVIE 2: Development of a 3-D pharynx. 0 min is first cleavage, which is approximately at 40 min after fertilization. 1A&B (top row). Pharynx is derived from AB and MS lineages. (Blue spheres) Cells from AB lineage; (green spheres) cells from MS lineage; (pink spheres) cells from E lineage that form the intestine. A, ventral view; B, left side view. 2 (bottom row). After a bilayer of pharynx primordium forms, cells from both AB and MS lineages wedge themselves between this bilayer to create a 3-D pharynx. (Dark green spheres) Left sheet of the bilateral pharynx primordium; (light green spheres) right sheet of the bilateral pharynx primordium; (yellow spheres) cells that create the third layer of the pharynx primordium as the first step to create a 3-D pharynx. Colors do not follow the WormAtlas color code. Click arrows to play the movies and on the movies to go to the lineage key page with larger movies and precursor and lineage keys (Movie source: A. Santella and Z. Bao.)
PhaFIG 3A-D: Embryonic development of the digestive tract. (Based on Sulston et al., 1983 and Leung et al., 1999.) A. 200 minutes after first cell cleavage (99-cell stage), ventral aspect. (Dark green) Cells from MS lineage; (light green) cells from AB lineage. B. 260 min after first cell cleavage (late gastrulation), ventral aspect. (Green arrow) Blastopore in which cells migrate inside the embryo. C. End of gastrulation, dorsal aspect, midplane. Pharynx (Ph) and intestine (Int) after tubular extension. D. 430 min after first cell cleavage, lateral aspect. Pharynx and intestine are separated from the surrounding tissues by a basement membrane. Epithelization of the buccal cavity is complete. PhaFIG 3E-G: Embryonic development of the digestive tract. E. Development of the pharyngeal lumen by retraction of the marginal cells from the midline when pharyngeal muscles begin to contract. (Left panel) A 400-minute embryo; (middle panel) 430-minute embryo; (right panel) late embryogenesis. (aj) Adherens junctions. F. Adherens junctions between muscle and marginal cells (black arrows) and adherens junction remnants (white arrows) within the syncytial muscle cells. (Ch) Pharyngeal channels. TEM, transverse section. Bar, 1 μm. G. Adherens junction remnant (arrow) immunogold-stained with gold-coated MH-27 antibody. (Image source: Hall archive.)


3 Pharyngeal (Buccal) Epithelium

A series of interfacial cells join the lips to the buccal cavity and the buccal cavity to the pharynx (See Epithelial System - Interfacial Epithelial Cells; PhaFIG 4; PharynxAtlas) (Wright and Thomson, 1981). The buccal cavity is surrounded, from anterior to the posterior, by the anterior hypodermis and the arcade cells, which constitute the anterior limit of the pharyngeal lumen (PhaFIG 4; InterFIG 1; InterFIG 3). Due to steric hindrance, each of these cells contributes small territories along the buccal cavity and their cell bodies lie more posteriorly in the head. The arcade cells are contiguous with the pharyngeal epithelium, a thin tube made from nine cells, formed by two successive rings of nonsyncytial tissue with sixfold symmetry (PhaFIG 5) (Albertson and Thomson, 1976).  Similar to the anterior hypodermal cells and the arcade cells, the cell bodies of the epithelial cells lie far posterior to the buccal cavity and extend thin processes anteriorly within the pharyngeal nerve cords to reach their territories surrounding the lumen (Albertson and Thomson, 1976).  The most anterior epithelial cells, e1, are positioned as a single dorsal and two subventral cells, covering markedly thinner territories (as measured along the a/p axis) than the other six cells. The posteriormost cells, e3, are positioned in the same pattern, and their epithelial territories lie directly behind those of e1 cells. The intervening e2 cells lie at the three apices of the triangular lumen, and their epithelial territories span the width of both the e1 and e3 cells, yielding a sixfold symmetry. At their lateral borders, all of these epithelial cells are firmly connected to their immediate neighbors by large adherens junctions (running continuously at the apical border). Where the epithelial cells border the posterior arcade cells, there are again very prominent adherens junctions.

PhaFIG 4A_DThe anterior digestive track is formed by the alignment of a series of cells
PhaFIG 4A-D: The anterior digestive tract is formed by the alignment of a series of cells. A&B. Sarcomeres of pm1 lie near the posterior edge of the buccal cavity. A. Epifluorescent image of pm1 in an animal expressing a GFP-tagged transgene. (NR) Nerve ring. (Strain source: Z-W. Wang and B. Chen.) Magnification 400x. B. Same animal in merged DIC and epifluorescent images. C&D. Anterior to pm1, pharyngeal epithelium surrounds the posterior buccal cavity. C. Epifluorescent image of the pharyngeal epithelium and pm3 in an animal expressing a GFP-tagged transgene. (Strain source: Z-W. Wang and B. Chen.) Magnification, 600x. D. Same animal in merged DIC and epifluorescent images.
PhaFIG 4E-I: The anterior digestive tract is formed by the alignment of a series of cells. E&F. The thin ring of the syncytial hyp 1 cell surrounds the anterior buccal cavity in an adult (see Epithelial System - Hypodermis). E. Epifluorescent image of hyp 1 in an animal expressing a GFP-tagged transgene. Inset shows hyp1 in a larval animal from the same strain. (Strain source: Z-W. Wang and B. Chen.) Original magnification, 400x. F. Same animal in merged DIC and epifluorescent images. G. Two consecutive rings of arcade cells, anterior and posterior, lie just behind hyp1 and anterior to pharyngeal epithelium along the buccal cavity. Epifluorescent images taken from an animal expressing a GFP-tagged transgene. (Strain source: Z-W. Wang and B. Chen.) Magnification, 600x. H. Same image as in G, magnified. I. Graphic rendition of the structure of the anterior alimentary canal. The processes of hyp1 and arcade cells extend along the pharynx to reach the buccal region. Pharyngeal tissues (pharyngeal epithelium and pharyngeal muscles) begin posterior to the arcade rings.

PhaFIG 5A_C Pharyngeal epithelium
PhaFIG 5A-C: Pharyngeal epithelium. All except insets are transverse section TEM images. A. Ring of nine epithelial cells encircle the anterior of the pharynx. The dorsal and subventral sides of this circle are occupied by the e1 cells. Three e2 cells are localized at the corners of the lumen. Their thin processes make a short clockwise turn in front of pm1 to connect to the buccal cavity portion. Posterior to e1, three e3 cells occupy the dorsal and subventral regions of the posterior buccal cavity. The cell bodies of e1, e2 and e3 are located, respectively, about 30, 20 and 35 μm posteriorly within the corresponding nerve cords. (Based on Albertson and Thomson, 1976.) (Inset) DIC image indicating the levels of B and C. B. Transition between the posterior arcade cells and the pharyngeal epithelium. The cells are connected to each other by large adherens junctions (arrow), sealing the pharynx to the buccal tissues. Numbers seen in B and in C-E are from the original prints. Bar, 1 μm. (Image source: N2T [MRC] A60-8.) C. Relationship of e1 and e2 cells at the anterior of the pharyngeal epithelium. Cells within each set do not touch to each other, but e1 and e2 cells are connected to each other by adherens junctions (arrows). (Image source: N2T [MRC] A60-22.)
PhaFIG 5D&E: Pharyngeal epithelium. D. Level slightly posterior to C. e2 and e3 cells are connected to each other by adherens junctions (white arrowheads). (Top inset) Section level. Intermediate filaments (arrows), which extend from the lumenal cuticle to the pharyngeal basal lamina, are attached to the basal lamina by electron-dense half-desmosomes (arrowheads). Bar, 1 μm. (Image source: N2T [MRC] A61-11.) E. Posterior of the pharyngeal epithelium and the anterior of the pharyngeal musculature. Three cuticular flaps are also seen. (Image source: N2T [MRC] A63-4.)

The pharyngeal epithelium is a rather rigid narrow cylinder that restricts entry of food into the pharynx. Its cylindrical shape is heavily reinforced by short radial bundles of intermediate filaments anchored to the apical and basal membranes of the epithelial cells by large hemidesmosomes. These well-anchored filaments seem to limit the epithelial cylinder from stretching or collapsing, despite the vigorous movements of the nearby pharyngeal musculature. The pharyngeal epithelial cells also secrete the cuticle that lines the buccal cavity along the former mesostom portion.

The inside caliber of the buccal epithelial lumen increases markedly at each larval molt, and this increase in size of the buccal cavity is suggested to permit increased growth rate after each molt (Knight et al., 2002). The buccal cavity is much narrower in the dauer larva, which stops actively feeding.



4 Muscle Cells of the Pharynx

The pharyngeal muscles are grouped into eight separate segments (pm1-pm8), which are arranged as eight consecutive rings encircling the pharynx (PhaFIG 6;PharynxAtlas) (Albertson and Thomson 1976; Avery and Thomas, 1997; Franks et al., 2006). Unlike the body wall muscles, no hypodermal layer separates the muscle anchorage from the cuticle lining the lumen of the pharynx. Indeed, most of the pharyngeal muscles appear to participate directly in secreting cuticle (e.g., the two anteriormost pharyngeal muscle cells, pm1 and pm2, secrete the cuticle that lines the metostom and telostom portions of the buccal cavity) and thus qualify as having myoepithelial properties (Albertson and Thomson 1976, D.H. Hall, unpublished). Most of the pharyngeal muscle segments are made up of three syncytial cells positioned in a three-fold symmetrical manner in any cross section. Each of these cells contains two nuclei as a result of fusion of two cells around the time of hatching (See Table 1 in Albertson and Thomson 1976; see also PhaTABLE 1). The exceptions are pm1 and pm6-pm8; pm1 is a syncytial cell that contains six nuclei, pm6 and pm7 are made of three nonsyncytial cells each, and pm8 is a single, nonsyncytial cell. In pm2-pm5 of adult pharynx, there are still small remnant adherens junctions at the sites of former cell fusions between pairs of muscle cells, marking the exact apical border where the fusion has occurred (PhaFIG 3) (Hedgecock and Thomson, 1982). These remnant junctions express the AJM-1 protein and can be stained by immunocytochemistry (Koppen et al., 2001; D.H. Hall, unpublished). The three muscle cells of each segment are separated from each other by three marginal cells, whereas the muscle cells of the neighboring rings are linked by gap junctions and also connected via interlocking short fingers on the anterior and posterior margins. Each syncytial muscle cell contains a deep groove on the basal side where a longitudinal pharyngeal "nerve cord" is situated (PhaFIG 6 and PhaFIG 7A). These nerve cords enclose the cell bodies and processes of neurons, gland cells, and anterior epithelial cells. Many synapses, including neuromuscular junctions onto the pharyngeal muscles, occur along these cords.

PhaTABLE 1 Characteristics of pharyngeal muscle cells and marginal cells
PhaTABLE 1: Characteristics of pharyngeal muscle cells and marginal cells. As a general rule, cells also have gap junctions with their nearest neighbors (marginal cell to muscle cell within a segment, marginal cell to marginal cell, and muscle cell to muscle cell between segments). aL. Avery, pers. comm. bMakes gap junctions to mc3 that are innervated by M5.
PhaFIG 6: Muscle cells of the pharynx. A. There are eight muscle segments (pm1-pm8) in the pharynx. All but pm6, pm7 and pm8 form syncytia. The most anterior segment, pm1, is a single cell with six nuclei. Its processes extend anteriorly adjacent to the outer edges of the marginal cells and terminate in a ring structure. Each pm2 soma has two nuclei and projects into a nerve ring to extend anteriorly. pm3 cells are located in procorpus, pm4 cells in the anterior bulb, and pm5 cells in isthmus. The terminal bulb contains pm6-pm8. The last muscle segment contains a single cell, pm8, that has a single nucleus located on the left side. (Top insets) Epifluorescent images of pm1 (left), pm6 (middle), and pm8 (right) in animals expressing GFP-tagged transgenes. (Strain source: Z-W. Wang and B. Chen.) Each magnification, 400x. B. Pharyngeal muscle cells contain radially oriented filaments. Here, myofilaments in pm3-pm7 can be seen in an epifluorescent image taken from a transgenic animal expressing the reporter gene, C32F10.8::GFP. (Asterisk) Position of g1 gland cells. (Image source: R. Newbury.) C. Muscles of the terminal bulb. Epifluorescent image from a transgenic animal expressing the reporter gene, K02A4.1::GFP. (Image source: R. Newbury.)

PhaFIG 7A Marginal cells of the pharynx
PhaFIG 7A: Marginal cells of the pharynx. A. Marginal cells lie along the three corners of the pharyngeal lumen. Syncytial pharyngeal muscle cells lie between the marginal cells in the dorsal and subventral positions. Pharyngeal nerve cords, which contain the cell bodies of the epithelial cells, the gland cell processes and the neurons, are situated in grooves within the muscle cells. Cells are pseudocolored on a transverse TEM image. (Inset) Raw TEM image. (Top) Graphic rendition of the section level along the pharynx. PhaFIG 7B&C: Marginal cells of the pharynx. B. Epifluorescent image of marginal cells expressing the reporter gene C07H6.3::GFP. (Image source: R. Newbury.) C. Pharyngeal muscle cells and marginal cells (mc) are connected to one another by adherens junctions (aj) and gap junctions (gj). TEM image. (Image source: Hall archive.)

Specialized zones mark the apical regions of several of the pharyngeal muscles where they secrete cuticle. Here, the cytoplasm contains electron dense tubules, and sometimes, dense core vesicles just under the plasma membrane. The cytoplasm of pm6 is particularly specialized in the region underlying the grinder, which is a very elaborate cuticular structure secreted by the pm6 muscle cells (PhaFIG 2). Prominent networks of sarcoplasmic reticulum along the borders of each muscle sarcomere presumably sequester calcium needed for muscle contractility. Pharyngeal muscle cells also contain many mitochondria.

In most pharyngeal muscle segments, contractile filaments are oriented radially, and when the muscles contract, the pharyngeal lumen opens. However, in the terminal bulb, the pm7 muscle filaments are oriented obliquely with regard to the anterior-posterior axis and pull on the grinder region when the muscle contracts. pm1-pm4 function in sucking up and trapping bacteria. pm5 regulates flow of food from corpus to the terminal bulb, and pm6-pm8 operate the grinder.



5 Marginal Cells

The pharynx is a mosaic of several non-equivalent cell types, each with threefold symmetry that assemble into a nonstratified, one-cell-deep epithelium along the lumen (PhaFIG 7; PharynxAtlas). As described above, muscle cells are a major part of this epithelium. Cells of another type, the marginal cells (mc), are placed at the three corners of the pharyngeal lumen and separate the muscle cells from one another. There are three mc segments along the pharynx and a total of seven marginal cells; three mc1 cells comprise the anterior segment, three mc2 cells comprise the second segment, and a syncytial mc3 cell with three nuclei comprises the terminal bulb segment (PhaFIG 1 and PhaFIG 6). From segment to segment, the marginal cells lie in rows at the corners of the lumen. They vary markedly in size between segments, but the three cells within one segment are essentially equivalent.

Marginal cells supply reinforcing strength to this muscular organ. Their large size and block-like shape is fortified by the placement of large radial bundles of intermediate filaments running from apical to basal borders of each cell. These filaments are anchored to the plasma membrane by large hemidesmosomes. Within each segment, the marginal cells are linked to neighboring muscle cells on their lateral borders by large gap junctions as well as apical adherens junctions separating the membrane to apical and basal surfaces (PhaFIG 7B&C) (Avery and Thomas, 1997). Large interlocking finger-like extensions also connect marginal cells to muscles within each segment and may also add to the structural integrity of the whole organ. Because of this arrangement, marginal cells within a segment communicate with muscle cells of the same segment and not with other marginal cells. In contrast, between segments, these cells form interlocking fingers and gap junctions to neighboring marginal cells.

The marginal cells contain many mitochondria, which suggests that these cells may perform some active role beyond merely providing continuity and strength to the epithelium. Because marginal cells are coupled to pharyngeal muscles via gap junctions, they may have some motor function, i.e., they may be myoepithelial in nature. Alternatively, they may act as relay stations to synchronously transmit signals from motor neurons to surrounding pharyngeal muscles so that all pharyngeal muscles within a segment can contract and relax at the same time. It is noteworthy that when the pharyngeal muscles contract, the muscle cells become thinner to open the lumen. Because the marginal cells are already relatively thin, this suggests that at full contraction, the pharyngeal lumen may open practically as wide as the inside corners of the marginal cells and form an open triangular lumen, whereas when the muscles relax, the lumen is practically closed except for the three channels at the apices of the anterior lumen.



6 Gland Cells of the Pharynx

Two classes of gland cells, g1 (three cells) and g2 (two cells), are found in the second bulb of the pharynx (PhaFIG 8; PhaMOVIE 3; PharynxAtlas). Although previously dorsal g1 and right ventral g1 cells were reported to fuse, recent results with fluorescent marker expression studies suggest that these cells remain separate (Smit et al, 2008; J. Gaudet, pers. comm). The g1 cells extend three cuticle-lined ducts anteriorly within the narrow pharyngeal nerve cords. Two of these ducts pass through the isthmus before emptying into the pharyngeal lumen near the first bulb. The dorsal g1 duct travels much farther and empties near the anterior limit of the pharynx. The g2 cells also extend ducts, which are much shorter and empty into the lumen of the second bulb. The g1 cells contain a lamellar cytoplasm and few vesicles, whereas the g2 cells have a rather clear cytoplasm and more vesicles. These contents may vary from animal to animal, and vesicle sizes are quite large and variable. Gland cells receive motor innervation from M4 and M5 motor neurons, which suggests that they may be stimulated to secrete digestive enzymes synchronously with pharyngeal pumping activity. Periodic episodes of secretion (vesicle motion) have been seen in g1 ducts by light microscopy and are apparently associated with molting (Hall and Hedgecock, 1991; unpublished observations of J. Sulston as reported by Albertson and Thomson, 1976). This suggests that gland secretion may participate in the digestion of the pharyngeal cuticle during molting.

PhaFIG 8A_F Gland cells of the pharynx
PhaFIG 8A-G: Gland cells of the pharynx. There are five gland cells: two posterior subventral g2 cells, one right and one left subventral g1 cells and a dorsal g1 cell. A. Epifluorescent image of gland cells taken expressing the reporter gene B0280.7::GFP, left lateral oblique view. (Image source: R. Newbury.) B. Graphic rendition of gland cells. (Although previously the dorsal and right side g1 cells were reported to fuse at the anterior of the terminal bulb and hence make a syncytium, more recent results suggest they stay separate [J. Gaudet, pers. comm]). The pair of subventral g1 cells open to the pharyngeal lumen at the posterior of the first bulb, whereas g2 gland cells open into the lumen anterior to the grinder. (Black ovals) Gland cell nuclei; (short arrows) gland openings to lumen. C. The dorsal g1 gland duct lies within the dorsal nerve cord and opens to the lumen through a short cuticular duct (arrow) close to the buccal cavity. Nearby muscles attach to the duct with adherens junctions (white arrowhead). D&E. Epifluorescent images of gland cells expressing the reporter gene F20B10.1::GFP or phat-1::GFP (E, bottom panel). D. Ventral oblique view. (Arrow) Dorsal g1 process. E. Ventral view (both panels). (Arrows) Ventral g1 processes. (Strain source [top panel]: L. Haklai-Topper and E. Peles.) (Image source [bottom panel]: R. Smit and J. Gaudet.) Magnification, 400x. F. The g1cells have lamellar cytoplasm, whereas the g2 cells have lighter cytoplasm with vesicles. TEM, transverse section through the posterior terminal bulb. (Image source: [MRC] N2T.) G. Epifluorescent images of dorsal gland cells expressing the reporter gene Y8A9A.2::GFP. (Arrow) dorsal g1 process. (Image source: R. Smit, V. Ghai and J. Gaudet.) PhaFIG 8H: Gland cells of the pharynx. H. Same TEM section as in F, pseudocolored. Top graphic shows the section level along the pharynx. (Inset) Raw TEM image.
PhaMOVIE 3: 3-D reconstruction of pharyngeal gland cells. 3-D movie was created from confocal images of a strain expressing the GFP marker linked to the promoter for B0280.7 using Zeiss LSM 5 Pascal software v. 3.2. (Image source: R. Newbury and D. Moerman.) Click on image to play movie.

7 Pharyngeal Neurons

The pharynx has 20 intrinsic neurons of 14 types, all of which have cell bodies located in the anterior or posterior bulb (see also PharynxAtlas). Six types are bilaterally paired and eight are single neurons. These neurons extend processes anteriorly and/or posteriorly along the three longitudinal pharyngeal nerve cords (the dorsal and the right and left subventral) and form a small plexus (the pharyngeal nerve ring) within the anterior bulb where they decussate to the other side. A half-ring (the terminal bulb commissure) is made by neuronal processes more posteriorly within the anterior portion of the terminal bulb (PhaFIG 9 and PhaFIG 10). A few neurons (M1, M2 and M3) send out processes along unique routes. The M1 process runs anteriorly between the muscle and the right marginal cell until it reaches the pharyngeal nerve ring where it relocates to the dorsal nerve cord and continues traveling anteriorly in this location. Unlike other neuron processes, M2 and M3 processes do not make their dorsal turn within the pharyngeal nerve ring, but more anteriorly within the pm4 where they pierce through the pm4 as they travel towards the dorsal side to enter the dorsal nerve cord (PhaFIG 10E-J). M2 neurons make synapses to pm4 along the way.

PhaFIG 9A_E Pharyngeal neurons
PhaFIG 9A-E: Pharyngeal neurons. A. Schematic of pharyngeal neurons I1L, NSML and M2L. (Arrowhead) Position of the pharyngeal nerve ring where processes from these and other neurons make dorsal-ventral turns. (Boxes) Section levels of D and E. B. Epifluorescent image of I1L expressing the reporter gene, zag-1::GFP, lateral view. (NR) nerve ring. (Strain source: S. Clark.) Magnifications, 400x. C. Epifluorescent image of NSML expressing the reporter gene tph-1::GFP, lateral view. (NR) nerve ring. Box indicates level of E. (Strain source: S. Clark.) Magnifications, 400x. D. Transverse TEM section where the somatic neuron RIP enters the pharynx to make gap junctions (inset, white arrow) to the pharyngeal neuron I1. The subcuticular ending of I1 is also seen close to the lumen. Bar, 1 μm. (Image source: [MRC] Q series 1730-8a.) E. Subcuticular ending of one NSM cell near the pharyngeal nerve ring. NSM attaches to the muscle cell by adherens junctions (arrowheads). Muscle cells contain dark-staining tubules and make adherens junctions to marginal cells (mc) as well (arrowheads). (Inset) NSM, enlarged, with multiple small clear vesicles inside. (Numbers on the image are from the original print.) (Image source: N2T [MRC] A348-8.) PhaFIG 9F-H: Pharyngeal neurons. F & G. Subventral F and dorsal G NSM processes reach the basal side via short branches containing many vesicles (arrow) and presynaptic densities towards the pseudocoelom. (Numbers on the images are from the original prints.) (Bl) basal lamina. (Image source [MRC] N2W.) H. Schematic of the I5 and M5 neurons. (Arrowhead) Terminal bulb commissure.

PhaFIG 10AB The processes of three of the pharyngeal neurons M1, M2 and M3
PhaFIG 10A&B: The processes of three of the pharyngeal neurons M1, M2 and M3. These neurons have unusual trajectories. All panels except A are transverse TEMs. Bars in B-J, 1 μm. (Image source: N2W [MRC] A382-A409. A. Schematic illustration of section levels in panels B-J. B. Cell bodies of I4 and M2 neurons in the terminal bulb. PhaFIG 10C-J: The processes of three of the pharyngeal neurons M1, M2 and M3. C. M3 cell bodies are near the ventral g1 duct openings into the lumen. D. Pharyngeal nerve ring is composed of the circumferential neuron processes. E-J. Consecutive sections through the first bulb show the trajectories of M2 and M3 processes piercing pm4 to reach the dorsal cord.

Most of these processes interact synaptically with others within the pharyngeal nerve ring, formed between the narrow region where pm4 and pm5 appose each other (PhaFIG 9). These synapses are of the en passant type, similar to those seen in the somatic neurons. The pharyngeal motor neurons also form neuromuscular junctions (NMJs) onto pharyngeal muscles. Unlike NMJs between somatic neurons and body wall muscles, no basal lamina has been found separating the neurons from muscles in the pharynx. There are no direct contacts between pharyngeal neurons and the larger somatic nervous system except the gap junctions made between RIPL/R neurons and the pharyngeal I1s, and gap junctions between RIPL/R and the pharyngeal motor neuron, M1 (Albertson and Thomson, 1976; Avery and Thomas, 1997). Ablation of RIP cells results in only a minor effect on pharyngeal function such that the brief inhibition of pumping in response to light touch to body disappears (Avery and Thomas, 1997). It is possible that one or more pharyngeal neurons, such as NSM cells, could secrete hormonal factors into the pseudocoelom to influence the rest of the animal. Otherwise, pharyngeal and somatic nervous systems function more or less independently of each other. A dissected and isolated pharynx continues its normal pumping behavior.

In fact, generation of electrical potential changes required for pharyngeal pumping is probably intrinsic to the pharyngeal muscle cells themselves since pumping behavior continues even when all the pharyngeal neurons are ablated (Avery and Horvitz, 1989). Although pumping can still occur after complete ablation of the pharyngeal nervous system, four of the pharyngeal neurons, MC and M3 motor neuron pairs, are important for the regulation of the pump motion.

Pharyngeal neurons fall into three categories: motorneurons, interneurons and other neurons. However, this distinction is somewhat arbitrary because most of these neurons have structures that suggest mixed functions.


7.1 Pharyngeal Motor Neurons

Among motor neurons, M2 and M3 are paired neurons, whereas M1, M4 and M5 are single (PhaFIG 10; PharynxAtlas). M2 and M3 neurons are subventrally located and each innervates one side of the subventral and dorsal muscle sectors. M3s are also suggested to have proprioceptive sensory function. M4 and M5 neurons send out two branches, each of which first innervates the subventral sectors and then turns and innervates the dorsal sectors.


7.2 Interneurons

I1, I2, I3 and I6 are unbranched bipolar cells. I1 cells make electrical synapses with the somatic neurons RIPL/R and synapse onto MC neurons. I4 has two processes that grow anteriorly. I5 is a fairly complex cell, the processes of which make a circle within the pharyngeal nerve ring. All of these neurons except for I4 have free subcuticular endings that may have proprioceptive function. See PharynxAtlas for more details.


7.3 Other Neurons

MC neurons are a pair of bipolar cells situated within the anterior bulb that innervate pm4 (L. Avery pers. comm.). The motor-interneuron, MI, is a single unipolar cell situated in the dorsal side of the anterior bulb and synapses onto both muscle and other neurons. The neurosecretory-motor neurons NSML and NSMR send out branches that form varicosities and contain mixed-sized vesicles (PhaFIG 9). The two main processes of the NSMs run in close apposition to the pseudocoelom over most of their length and form some release sites towards this space. NSMs are serotonergic. These cells may have both neurosecretory and motor functions and may communicate the presence of food to the rest of the animal's body. Exogenous application of serotonin stimulates pumping, decreases locomotion and stimulates egg-laying. The same responses are seen in the presence of bacteria in the environment. NSMs were thought to be potential candidates for mediating the effects of endogenous serotonin. However, ablation of NSMss has only subtle effects on pumping, suggesting that they may be redundant for this function (Avery et al., 1993, Avery and Thomas, 1997). The slowing of locomotion in the presence of bacteria becomes more enhanced in animals that were previously food-deprived, compared to well-fed animals. This phenomenon is described as "the enhanced slowing response." When NSMs are ablated there is a small but significant decrease in this enhanced slowing of locomotion, which suggests NSMs contribute to this behavior (Sawin et al., 2000).


7.4 List of Pharyngeal Neurons

1. Motor neurons
M1
M2L/R
M3L/R
M4
M5
2. Interneurons
I1L/R
I2L/R
I3
I4
I5
I6
2. Other neurons
MI
NSML/R
MCL/R

See also PharynxAtlas



8 Pharyngeal-Intestinal Valve (VPI)


A group of six equivalent cells forms a tightly constructed “valve” that links the posterior bulb of the pharynx to the anterior four cells of the intestine (PhaFIG 11, PhaFIG 12 and PhaMOVIE 4.) These six cells comprise a small epithelial channel with a cuticular lining in continuity with the pharyngeal cuticle. The channel links the lumen of the pharynx to the large lumen of the anterior intestine. Three sets of cells form consecutive rings containing one, three and two cells from anterior to posterior (PhaFIG 12). The inside cuticle is reinforced by a series of closely spaced circumferential ridges, rather like the cuticle of the anterior buccal cavity. The valve cells are not syncytial, but are firmly linked to their neighbors and to the pharynx and/or intestine by robust adherens junctions at their apical borders and by gap junctions (valve-to-valve cell and valve to intestine) (PhaFIG 11).

PhaFIG 11 Pharyngeal-intestinal valve (vpi) is composed of sex cell: one vpi1, three vpi2 and two vpi3
PhaFIG 11: Pharyngeal-intestinal valve (vpi) is composed of six cells: one vpi1, three vpi2 and two vpi3. A. Horizontal TEM section through the pharynx-intestine junction. Each valve cell occupies a thin wedge-shaped domain surrounding some of the lumen of the valve. Bar, 1 μm. (Image source: Hall archive.) B. Adjacent thin section showing the valve cells in higher resolution. (Arrowhead) vpi1 projection into pm8, which is sealed to pm8 by adherens junctions. Bar, 1 μm.( Image source: Hall archive.) C. Epifluorescent image of the valve expressing the reporter gene hum-1::GFP, lateral view. (Strain source: M. Titus.) Magnification, 400x. PhaFIG 12: Structure of the pharyngeal valve. Shown is stacking of the six vpi cells from the anterior end (top left) toward the posterior. Three-dimensional rendition of the cells based on tracings from serial TEMs. (Image source: B. Henick and A Hartley, based on MRC series.) Each cell is given a unique color. Colors do not follow the WormAtlas color code.
PhaMOVIE4 3-D reconstruction of how VPI cells stack
PhaMOVIE 4: 3-D reconstruction of how VPI cells stack. Stacking of the six vpi cells from the anterior end (top left) toward the posterior is shown. Three-dimensional rendition of the cells based on tracings from serial TEMs. (Image source: B. Henick and A Hartley, based on MRC series.) Each cell is given a unique color. Colors do not follow the WormAtlas color code. Click on image to play movie.

No apparent muscular elements operate within the valve cells, nor are there any muscles attaching to this valve from the outside. Thus, the valve is probably a passively open and patent channel at all times, but rather narrow in caliber. The pm8 muscle of the pharynx is in appropriate position to act alone as a sphincter just rostral to the valve cells, but pm8 shows no direct innervation. Contraction of the pm8 has been suggested to open the valve wider when the grinder is active (Avery and Thomas, 1997). Hence, restrictions to regurgitation of ingested material may be due to operation of the pharyngeal grinder within the second bulb of the pharynx, immediately anterior to this valve. Squeezing motions of the terminal bulb would force food through the grinder and into the intestine via the pharyngeal-intestinal valve during the pumps when the pressure in terminal bulb is high. The intestinal lumen widens considerably just behind this region, which would result in a drop in internal pressure, which may limit any reflux from the intestine back through the valve.

Each valve cell has an electron-dense cytoplasm and occupies a thin wedge-shaped domain surrounding about one half of the lumen of the valve (PhaFIG 11). The nuclei of valve cells are flattened in shape, and the cytoplasm contains radial bands of intermediate filaments anchoring the apical cuticle to the basal lamina of the epithelium via hemidesmosomes, again in a very similar fashion to those seen in the buccal epithelium (D.H. Hall, unpublished).



9 Specific Structures Within the Pharynx


9.1 Channels of the Pharyngeal Lumen

These channels, three narrow grooves in outer corners of the pharyngeal cuticle, seem to allow an escape route for liquid to be regurgitated out of the pharynx via the buccal cavity. This results in food particles being trapped in the sieve while fluid is expelled. These channels extend under the mc1 marginal cells and connect into the buccal cavity (PhaFIG 2) (Albertson and Thomson, 1976).


9.2 Cuticle of the Pharynx

A thin cuticle lining extends to cover the interior surface of the pharyngeal passageway from the lips to the back of the pharynx, ending at the rear of the pharyngeal-intestinal valve. The pharyngeal cuticle is formed by the pharyngeal epithelium and the muscle cells to cover the apical surfaces of many cells acting in concert, much as the thickened pharyngeal basal lamina is formed jointly on basal surfaces of the pharyngeal cells. Unlike the body cuticle, this cuticle shows no layers; however, it shows some reinforcement at points of stress. For instance, it becomes keratinized to stain more densely by TEM at certain regions (PhaFIG 2). Other specialized portions of the pharyngeal cuticle include the following.


9.2.1 Bridging Cuticle

A small discrete region of cuticle connects the body wall cuticle covering the lips to the cuticle lining the buccal cavity. This bridging cuticle lies on the outer face of the anterior arcade and may also be touched briefly by the posterior arcade (see Epithelial System - Interfacial Cells; InterFIG 1).


9.2.2 Flaps

These structures close the opening of the buccal cavity to the pharyngeal lumen and may correspond to the onchia or buccal teeth described in larger nematodes (see Chitwood and Chitwood, 1950; see also PhaFIG 2; PhaFIG 5; InterFIG 1). Three flaps extend inward from the level of from the pharyngeal muscle cells pm1 and pm2 to restrict flow at the rear of the buccal cavity. The flap cuticle is very electron dense, suggesting a sclerotic hardening to stiffen the flaps and the entryway to the true pharynx.


9.2.3 Grinder

The grinder is a cuticle specialization made primarily by pm6 and pm7 muscles. Its three contact zones, made by the three pairs of muscle cells, rotate when the muscles contract (Avery and Thomas, 1997). These interlocking "teeth" macerate the food and may function as a valve to regulate one-way traffic of food into the intestine (PhaFIG 2). Although the pm6 muscle filaments are oriented in radial fashion to the grinder, some portions of the pm7 muscles are oriented obliquely to the anterior-posterior axis and are anchored on the basal pole to the rear of the terminal bulb. These pull from the posterior side of the teeth, and coordinated action of these muscles may then rotate the grinder segments and force the teeth to scrape past and engage one another. The food caught and ground up between the teeth is passed back to the intestine through the pharyngeal-intestinal valve. Relaxation of the terminal bulb returns the grinder to its resting state.


9.2.4 Pharyngeal Sieve

These finger-like extensions from the pharyngeal cuticle probably act to trap bacteria (PhaFIG 2). They extend from the cell borders where pm4 muscles meet the neighboring mc1 cells. They project over a region of about 20 μm in length within the narrow lumen, ending near the transition of the metacorpus to the isthmus.


9.3 Gap Junctions

The muscle cells and the marginal cells of the pharynx are linked to and communicate with each other via elaborate gap junctions (Phelan, 2005; see also PhaFIG 7; PhaTABLE 1). Gap junctions also exist between the pharyngeal neurons and also between the pharyngeal neuron I1 and the extrapharyngeal neuron RIP. Gap junctions within the pharynx are composed of innexins, invertebrate gap junction proteins. Innexins heteromerically assemble into hexameric hemichannels and form pores between cells. This gap junction network confers a high level of connectivity within the pharynx, which is essential in coordinating waves of muscle contractions and spreading the neuronal input.



10 Feeding Behavior

C. elegans is a filter-feeder. Particles (bacteria) are taken in as suspended in liquid and then trapped in the pharynx while the liquid is expelled outside by the function of the corpus and anterior isthmus (Avery and Thomas, 1997; Avery and Shtonda, 2003). The particles are then transported to the terminal bulb, ground and passed into the lumen of the intestine. The feeding behavior consists of two motions; pumping, a contraction-relaxation cycle involving the corpus, anterior half of the isthmus and terminal bulb; and posterior isthmus peristalsis. Pumping involves near-simultaneous contraction of the muscles of the corpus, anterior isthmus and terminal bulb followed by near-simultaneous relaxation. When a feeding motion begins, contraction of the corpus and anterior isthmus opens their lumens, sucking particles and liquid in, whereas contraction of the terminal bulb muscles breaks up already-trapped bacteria and passes the debris posteriorly towards the intestine (Avery and Shtonda, 2003). At this stage corpus and anterior isthmus are separated hydrodynamically from the terminal bulb by a closed isthmus. During the relaxation period that follows, the lumens of the corpus and the anterior isthmus close, allowing for the liquid to be expelled through the radial channels while bacteria are retained and the grinder returns to its resting position. Unlike the corpus, which contracts and relaxes as a unit, the anterior isthmus contracts in a wave that proceeds rapidly from anterior to posterior. Also, the motions of the anterior isthmus are slightly delayed relative to the corpus, resulting in a net posterior transport of food particles during a pump (Avery and Shtonda, 2003). When the muscles again contract, the bacteria are carried further posteriorly by the inflow of liquid. Roughly one out of four pumps is followed by a posterior isthmus peristalsis where the trapped bacteria are carried from the anterior isthmus backwards to the grinder. Although each pm5 muscle cell runs the entire length of the isthmus, peristalsis occurs as a wave that propagates from anterior to posterior instead of simultaneously along its length. This capacity of isthmus for asynchronous contraction is suggested to permit the terminal bulb and corpus lumen to be at different pressures (Avery and Thomas, 1997).

Pumping is suppressed during the dauer larval stage and in response to a touch stimulus in adults. As described above, the latter response depends on an RIP/I1 connection. This circuit may also be important for suppression of pumping in the dauer larva (Keane and Avery, 2003). Inhibition of pumping during the dauer stage may save energy and prevent ingestion of environmental toxins when no appropriate food is available.

Under laboratory conditions, neural control of feeding can be managed completely by the pharyngeal nervous system. Three pharyngeal motor neuron types, M3, MC and M4, seem necessary and sufficient for normal feeding of the animal under these conditions. M3 neurons control the timing of the end of a pump, that is, initiation of pharyngeal relaxation. They are inhibitory-type motor neurons, and because of their free endings in the metacorpus, they are also suggested to be proprioceptive sensory neurons (Albertson and Thomson, 1976). Through a self-acting proprioceptive loop, M3 neurons are postulated to fire in response to corpus muscle contraction and cause muscle relaxation. M3 neurons are glutamatergic, and the fast inhibitory glutamatergic transmission from M3 neurons to the pharyngeal muscle is thought to be mediated through a glutamate-gated (ionotropic) chloride channel (Dent et al., 1997, 2000).

MC motor neurons control the rate of excitation of pharyngeal muscle. They mediate rapid pharyngeal pumping and are necessary for increased pumping in response to food (Avery and Horvitz, 1989). MC neurons are cholinergic excitatory motor neurons (Raizen et al., 1995; Keane and Avery, 2003). Mutants in which acetylcholine synthesis (cha-1) or packaging (unc-17) is disrupted show a pumping defect similar to that seen after MC ablation. Functional studies suggest that MC neurons synapse onto pm4 and that synaptic transmission from MC neurons to pm4 requires the nicotinic acetyl-choline receptor (nAChR) subunit, EAT-2 to be expressed on pm4.  Mutations in eat-2 mimic MC cell loss (Keane and Avery, 2003; L. Avery, pers. comm.). MC neurons may also be mechanosensory, because they have free endings at the boundary between the procorpus and metacorpus and may sense the presence of bacteria in the pharynx.

The M4 neuron is required for posterior isthmus peristalsis. It synapses onto the posterior half of the isthmus muscles. M4 ablation leads to growth failure since the animals can not ingest any food (Avery and Horvitz, 1989). However, these animals continue to pump, and as a result the anterior isthmus and corpus become stuffed with bacteria. M4 is cholinergic but may also be utilizing another neurotransmitter since cholinergic antagonists and mutations that affect nicotinic ACh receptors only partially block M4 function (L. Avery, pers. comm.).



11 List of Pharyngeal Cells

i. Buccal epithelium of the pharynx (e)

1. First epithelial ring
e1D
e1VL
e1VR
2. Second epithelial ring
e2DL
e2DR
e2V
3. Third epithelial ring
e3D
e3VL
e3VR

ii. Pharyngeal muscles (pm). Note that in earlier publications these cells are labeled as "m"; m1, m2, m3 etc., but here they are labeled "pm" for "pharyngeal muscle" (Avery and Thomas, 1997).

1. First pharyngeal muscle ring; all fuse into one syncytium around hatching
pm1DL
pm1DR
pm1L
pm1R
pm1VL
pm1VR
2. Second pharyngeal muscle ring
pm2DL; fuses with DR around hatching
pm2DR; fuses with DL around hatching
pm2L; fuses with VL around hatching
pm2R; fuses with VR around hatching
pm2VL; fuses with L around hatching
pm2VR; fuses with R around hatching
3. Third pharyngeal muscle ring
pm3DL; fuses with DR around hatching
pm3DR; fuses with DL around hatching
pm3L; fuses with VL around hatching
pm3R; fuses with VR around hatching
pm3VL; fuses with L around hatching
pm3VR; fuses with R around hatching
4. Fourth pharyngeal muscle ring
pm4DL; fuses with DR around hatching
pm4DR; fuses with DL around hatching
pm4L; fuses with VL around hatching
pm4R; fuses with VR around hatching
pm4VL; fuses with L around hatching
pm4VR; fuses with R around hatching
5.Fifth pharyngeal muscle ring
pm5DL; fuses with DR around hatching
pm5DR; fuses with DL around hatching
pm5L; fuses with VL around hatching
pm5R; fuses with VR around hatching
pm5VL; fuses with L around hatching
pm5VR; fuses with R around hatching
6. Sixth pharyngeal muscle ring
pm6D
pm6VL
pm6VR
7. Seventh pharyngeal muscle ring
pm7D
pm7VL
pm7VR
8. Eighth pharyngeal muscle ring
pm8

iii. Marginal cells (mc)

1. First marginal cell ring
mc1DL
mc1DR
mc1V
2. Second marginal cell ring
mc2DL
mc2DR
mc2V
3. Third marginal cell ring (syncytial, cells fuse around hatching)
mc3DL
mc3DR
mc3V

iv. Pharyngeal-intestinal valve (vpi)

1. First pharyngeal valve ring
vpi1
2. Second pharyngeal valve ring
vpi2DL
vpi2DR
vpi2V
3. Third pharyngeal valve ring
vpi3D
vpi3V

v. Pharyngeal neurons

1. Motor neurons
M1
M2L/R
M3L/R
M4
M5
2. Interneurons
I1L/R
I2L/R
I3
I4
I5
I6
2. Other neurons
MI
NSML/R
MCL/R

vi. Pharyngeal glands (g)

1. First pharyngeal gland ring
g1AL; ventral left g1 gland cell
g1AR; ventral right g1 gland cell
g1P; dorsal gland cell
2. Second pharyngeal gland ring
g2L
g2R

See also PharynxAtlas



12 References

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This chapter should be cited as: Altun, Z.F. and Hall, D.H. 2009. Alimentary System, Pharynx. In WormAtlas.  doi:10.3908/wormatlas.1.3
Edited for the web by Laura A. Herndon. Last revision: July 21, 2012.
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