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Chapter 4—Ultrastructure of Esophagus of Juveniles of the Soybean Cyst Nematode, Heterodera glycines

Figure Captions

Figure 68.Longitudinal diagram of esophageal region of a second-stage juvenile of Heterodera glycines.


Figure 69. Terminology of body regions of nematodes citing the triradate symmetry of esophagus. Reprinted with permission of Dr. A. Coomans and The Société Royale Zoologique de Belgique from Annales de la Société Royale Zoologique de Belgique 108:115–117, 1979.


Figure 70. Diagram of dorsal gland ampulla valve or end apparatus in closed position. Note that the infolded valve membrane curves into the valve duct lumen.


Figure 71. Diagram of one of two subventral gland ampullae with valve or end apparatus in an open position.


Figure 72. Longitudinal section of anterior procorpus region of esophagus of Heterodera glycines, showing stylet protractor muscles (Pm) and portions of their cell bodies (PmC). Tonofilamentous (tf) regions of protractor muscle cell bodies are separated by a delta-shaped, mitochondria-filled (Mc) part of a stylet shaft supporting cell (ShC). N, nucleus; Sk, stylet knob. Bar=0.5 µm.


Figure 73. In longitudinal section, stylet shaft cell (ShC) extending anteriorly and beyond stylet knob (Sk). Pm, protractor muscle; PmC, cell body of protractor muscle. Bar=0.5 µm.


Figure 74. In longitudinal section of two of four secondary muscle (sm) elements, their cell bodies (smC) are located on either side of stylet shaft cell body (ShC). EL, esophageal lumen; Pm, protractor muscle; Sk, stylet knob. Bar=0.5 µm.


Figure 75. Transverse section of anterior procorpus just posterior to stylet knobs, showing cell bodies of stylet protractor muscles (PmC), stylet shaft tissues (ShT), and secondary muscle elements (sm). cu, cuticle; EL, esophageal lumen; N, nucleus; Sm, somatic muscle. Bar=0.5 µm.


Figure 76. Longitudinal section showing esophageal lumen (EL), dorsal esophageal gland ampulla valve (DAv), stylet knobs (Sk), and part of lumen wall (ELW) with its supporting membranes (arrows). Lumen wall forms a short branch that ends in a membranous valve with cuticularized arms (see fig. 80). Valve membrane is continuous with anterior supporting membrane of dorsal gland ampulla (DA). Mt, microtubules. Bar=0.5 µm.


Figure 77. Medial longitudinal section of base (VB) of dorsal gland ampulla valve. Note that microtubules (Mt) of ampulla cytoplasm end at or near the base of dorsal gland ampulla valve (see fig. 76). Bar=0.5 µm.


Figure 78. Transverse section of a distal section of dorsal gland ampulla valve. Bar=0.5 µm.


Figure 79. Transverse section through base of valve (VB) of dorsal gland ampulla (DA). Procorpus cells are densely packed with mitochondria (Mc) and other organelles. EL, esophageal lumen. Bar=0.5 µm.


Figure 80. Transverse section of dorsal gland ampulla (DA) showing nearby esophageal lumen wall (ELW) and complex of cells and support membranes that are continuous with anterior ampulla membranes. Dorsal surface of ampulla is apposed to an enlarged neural process (NP) that contains numerous neurosecretory granules. Cuticularized support arms (ca) of tetraradiate dorsal gland ampulla valve (DAv) are shown in closed position. EL, esophageal lumen. Bar=0.5 µm.


Figure 81. Longitudinal section of posterior procorpus and anterior metacorpus, showing dorsal gland extension (Dx) within procorpus (prc) and anterior metacorpus (m). Gland extension contains irregularly distributed groups of secretion granules (SG) and dilated, circular-to-elongate, vesicular rough endoplasmic reticulum (RER). Narrow anterior region of metacorpus consists of collar of multidirectional sphincter-muscle (Spm) elements. Bar=1.0 µm.


Figure 82. Submedian longitudinal section of junction between procorpus and metacorpus, showing tangential view of a sphincter-muscle (Spm) complex with some forward-directed muscle elements (arrows). Bar=1.0 µm.


Figure 83. Transverse section of sphincter muscles (Spm) showing lack of direct contact with esophageal lumen wall (ELW). Bar=1.0 µm.


Figure 84. Transverse section of anterior region of metacorpus showing a membrane complex (mc) attached to lumen wall (ELW). Sections of five of eight nuclei (N) in this plane of metacorpus are shown among muscle elements (mm) that extend forward from metacorpus pump wall. Dorsal region of metacorpus is occupied by dorsal gland extension (Dx) and three neural processes (NP), one of which is a large neurosecretory cell (NSC). Bar=1.0 µm.

Figure 85. Cross section through anterior region of metacorpus, showing esophageal lumen wall (ELW) surrounded by muscle elements (mm) of metacorpus pump located slightly posteriad. Dorsal gland extension (Dx) lies between two metacorpus muscle elements. N, nucleus; SG, secretion granules. Bar=1.0 µm.

Figure 86. Longitudinal section through metacorpus showing metacorpus pump with associated muscles, nuclei, and subventral esophageal gland ampullae (SvA) with valves (SAv). Ventrosublateral longitudinal section of metacorpus shows outline of a ventrally directed flange of pump wall (mP) with associated muscles (mm) attached to pump chamber wall. Muscles extend outward to various sectors of basal lamina of metacorpus. Paired ampullae of subventral esophageal gland extensions are supported by cellular and membranous complexes (CMC) just posterior to pump. NP, neural process; Spm, sphincter muscle. Bar=1.0 µm.


Figure 87. Longitudinal section through pump valve, showing row of five of ten nerve nuclei that occur in ventrosublateral sectors of metacorpus. Two arms of triradiate pump chamber (mP) are shown in longitudinal sections. N, nucleus; Spm, sphincter muscle. Bar=1.0 µm.


Figure 88. Enlargement of fig. 87 metacorpus pump chamber, showing electron-translucent cuticular walls of esophageal lumen branch (ELB) and pump arms (PA), which are supported by pair of electron-translucent cuticular ridges (cuR). Lumen wall extends into subventral gland ampulla (SvA) and ends as slender electron-translucent supports in membranous valve (SAv). A cell complex (CMC) surrounds base of valve. Neurosecretory granules (NG) are present in cells next to subventral gland ampullae. Some secretion granules (SG) in an ampulla appear partially empty. Wall of pump vestibule (PVe) narrows posteriorly to triradiate closed lumen (TL). In longitudinal section, one arm of triradiate lumen appears as pair of electron-translucent cuticular walls separated by electron-opaque lumen. A similar region is shown in cross section in fig. 96. NP, neural process. Bar=1.0 µm.


Figure 89. Transverse section of a closed subventral gland valve in a second-stage juvenile at a feeding site. Bar=0.5 µm.


Figure 90. Submedial longitudinal section showing nuclei (N) of cells associated with accumulations of neurosecretions lying dorsally in metacorpus (see fig. 84). Adjacent dorsal gland extension (Dx) contains cytoplasm with large accumulations of rough endoplasmic reticulum (RER) with dilated cisternae. Sphincter muscles (Spm) of anterior metacorpus are shown in tangential section. mpm, metacorpus pump muscle; SvA, subventral gland ampulla. Bar=1.0 µm.


Figure 91. Oblique longitudinal section showing an open subventral gland ampulla valve (SAv) supported by cuticularized arms and membranes (M). Contents of open valve are similar to electron-opaque contents of secretion granules (SG) in ampulla. Nerve processes (NP) of axons or dendrites surround the ampulla of subventral gland (SvA). Muscle elements of metacorpus pump (mpm) extend posteriad, partially surround ampullae, and terminate near sphincter muscles (Spm). Bar=1.0 µm.


Figure 92. Transverse section of metacorpus showing triradiate pump chamber and muscles, nuclei (N), and somatic or sarcoplasmic cells. Bar=1.0 µm.


Figure 93. Enlargement of metacorpus pump of fig. 92, showing attachment of pump muscles to pump chamber wall. Pair of electron-translucent "ridges" on each arm of pump wall are shown in figs. 86–88 as spinelike ridges (cuR) that follow contour of spindle-shaped valve. Paired muscle elements (mpm1, mpm2) are attached to each other by membrane junctions (MJ) and to pump walls (mPW) by hemidesmosomes (hd). Dorsal esophageal gland extension (Dx) has cytoplasmic components that include secretion granules (SG), dilated rough endoplasmic reticulum (RER), and microtubules (Mt). Bar=1.0 µm.


Figure 94. Transverse section through posterior metacorpus, showing triangular shape of central esophageal lumen (EL) and square cross-sectional shape of its branches (ELB) that end in each of two subventral gland ampullae. These cuticular wall structures are connected with a complex of cells (CMC) and membrane junctions. Dx, dorsal gland extension; mpm, metacorpus pump muscle; Mt, microtubules; NP, nerve process. Bar=1.0 µm.


Figure 95. Transverse section showing the merging of the base of a subventral gland valve with the wall of esophageal lumen. Bar=1.0 µm.


Figure 96. Transverse section of open valves (SAv) within subventral gland ampullae slightly posterior to section in fig. 94. Valve walls have characteristic single and double membrane boundaries (vM) that confine the electron-opaque material (EOM) which apparently accumulates from secretory granules (SG). Cuticularized triradiate esophageal lumen (TL) extends posteriad from terminus of metacorpus pump vestibule through isthmus and terminates at esophago-intestinal valve. Triradiate lumen wall is modified in shape and is stabilized by membrane junctions and cells associated with dorsal gland extension (Dx) and subventral gland ampullae (SvA). mpm, metacorpus pump muscle; NP, nerve process. Bar=1.0 µm.


Figure 97. One of a series of transverse sections through the isthmus and the anterior region of esophageal glands. Partially open triradiate lumen (TL) shows walls attached to membrane junctions that extend to sphincter muscles (Spm). Isthmus is encircled by cluster of nuclei (N) that lie in a region between metacorpus and nerve ring. SvA, subventral gland ampulla. Bar=1.0 µm.


Figure 98. Anterior region of nerve ring (NR) lying posteriad to sphincter muscle (see fig. 103) and surrounded by cluster of nuclei as shown in fig. 97. Dx, dorsal gland extension; Svx, subventral gland extension. Bar=1.0 µm.


Figure 99. Central region of isthmus (i) showing triradiate esophageal lumen (TL) surrounded by dorsal (Dx) and subventral gland extensions (Svx). Nerve ring (NR) completely surrounds isthmus, with more neural processes in dorsal region than in ventral. Bar=1.0 µm.


Figure 100. Dorsal esophageal gland (Dg) dominating anterior of gland lobe, where it is bordered laterally by nuclei and sublaterally by subventral gland extensions (Svx) that are filled with prominent secretion granules (SG). VnP, ventral nerve processes. Bar=1.0 µm.


Figure 101. Cross section of irregularly shaped anterior glandular lobe (agl). Lumen is encircled by slender supporting cells and anterior regions of dorsal (Dg) and subventral glands (Svg). Bar=1.0 µm.


Figure 102. Transverse section of gland lobe showing different types of secretion granules (SG) in the dorsal (Dg) and subventral glands (Svg). Bar=1.0 µm.


Figure 103. Oblique longitudinal section through isthmus, showing dorsal gland extension (Dx) with nerve ring tissue (NR) on either side. Nuclei (N) adjacent to nerve ring and isthmus are part of cluster that encircles this region in transverse section (see figs. 97, 98). Bar=1.0 µm.


Figure 104. Transverse section showing neurosecretions (NS) within nerve processes of nerve ring (NR). Electron-opaque sites (arrows) indicate axon-axon or axon-dendrite synapses. Secretory granules (SG) synthesized in dorsal gland (Dg) differ from those in subventral glands (Svg), with the former being more homogeneous and having less distinct limiting membranes (M). EL, esophageal lumen. Bar=1.0 µm.


Figure 105. Longitudinal section of gland lobe showing portions of esophago-intestinal valve (Eiv) and secretion granules (SG) accumulated in dorsal gland (Dg) and subventral gland (Svg). Bar=1.0 µm.


Figure 106. Longitudinal section of gland lobe showing terminus of open cuticle-lined esophageal lumen (EL) and its relationship to intestinal lumen (IL). Dg, dorsal esophageal gland; DN, dorsal esophageal gland nucleus; Eiv, esophago-intestinal valve. Bar=1.0 µm.


Figure 107. Transverse section slightly anterior to dorsal gland nucleus showing apposed membranes (arrows) of esophago-intestinal valve (Eiv). Subventral gland (Svg) cells are slender and appear like discrete cells that lie adjacent to esophago-intestinal valve and dorsal esophageal gland (Dg). Bar=1.0 µm.


Figure 108.Transverse section of central region of dorsal esophageal gland (Dg) filled with densely packed, dilated rough endoplasmic reticulum (RER), mitochondria (Mc), Golgi apparatus (GA), and some secretion granules (SG). Esophago-intestinal tissue is composed of three cells (Eic1, Eic2, Eic3) and adjoining membrane junctions near intestinal lumen. The two subventral glands (Svg1, Svg2) and the dorsal gland are clearly defined by their respective cell membranes. Bar=1.0 µm.


Figure 109. Golgi apparatus (GA) in early stages of formation of secretion granules, some of which are shown in figs. 108 and 110. Bar=0.5 µm.


Figure 110. Transverse section through dorsal esophageal gland (Dg) and nucleus (DN) with adjacent intestinal lumen (IL) and intestinal epithelial cells (IEc). SG, secretion granules. Bar=1.0 µm.


Figure 111.Longitudinal section of posterior gland lobe, showing nuclei (N1, N2) and secretion granules (SG) of paired subventral esophageal gland cells (Svg1, Svg2). Slender intestinal region (int) broadens immediately posterior to gland lobe. IL, intestinal lumen. Bar=1.0 µm.


Figure 112. Transverse section of gland lobe showing many membrane-bound granules (SG) with wide ranges of electron-opacity in the two subventral gland cells (Svg1, Svg2), and intercellular membranes (arrows) between dorsal (Dg) and subventral gland cells. Sm, somatic muscles. Bar=1.0 µm.

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Last Modified: 8/12/2016
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