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Ultrastructure of the Esophagus of Larvae of the Soybean Cyst Nematode, Heterodera Glydnes

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Ultrastructure of the Esophagus of Larvae of the Soybean Cyst Nematode, Heterodera Glydnes Proc. Helminthol. Soc. Wash. 51(1), 1984, pp. 1-24 Ultrastructure of the Esophagus of Larvae of the Soybean Cyst Nematode, Heterodera glydnes BURTON Y. ENDO Nematology Laboratory, Plant Protection Institute, Beltsville Agricultural Research Center, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, Maryland 20705 ABSTRACT: The cell bodies of the stylet protractor muscles and of the tissue immediately surrounding the stylet shaft are located in the anterior procorpus alongside the cells of the procorpus proper. The protractor muscle cell bodies are in the dorsal and ventrosublateral sectors and those related to the shaft are in the dorsosublateral and ventral sectors. The dorsal gland duct ampulla lies in the anterior procorpus and from it, the sclerotized duct with its valve or end apparatus joins the esophageal lumen just behind the stylet knobs. Secondary muscle cells lie centripetal to the protractor muscle cells. Constraining muscles occur in the posterior region of the procorpus. The metacorpus consists of a pump chamber operated by a complex of muscle units with their perikaryons and innervation. The subventral gland processes end as ampullae from which the valved sclerotized ducts joint the esophageal lumen at the posterior triangular vestibule of the esophageal lumen. The isthmus is muscular anteriorly and the attenuated gland extensions are encircled by the nerve ring. The dorsal gland occupies most of the anterior of the gland lobe; the two subventral glands that appear as separate cells occupy the posterior region. The esophageal-intestinal valve is adjacent to the dorsal gland nucleus. The soybean cyst nematode Heterodera gly- gans and the stomatal region of//, glydnes. This dnes Ichinohe, 1952 is a major pest of soybeans. paper described the ultrastructure of the esoph- Host-parasite studies with emphasis on host re- agus with emphasis on the procorpus, metacor- sponses (Endo, 1964, 1965; Gipsonetal., 1971) pus, and glandular organs. The general mor- have been augmented recently by ultrastructural phology of the nerve ring is also included. studies on the morphology of males and larvae of the root-knot and soybean cyst nematodes Materials and Methods (Baldwin and Hirschmann, 1973, 1975a,b, 1976; Freshly hatched second-stage larvae of Heterodera glydnes Ichinohe, 1952 were prepared for electron mi- Endo and Wergin, 1973, 1977; Wergin and Endo, croscopic examination by using published procedures 1976; Baldwin et al., 1977; Endo, 1978, 1980). (Endo and Wergin, 1973; Wergin and Endo, 1976). Observations and reviews of other tylenchid Briefly, nematodes in a suspension of water were mixed species (Bird, 1967, 1968, 1971; Wisse and with warm liquified 2% water-agar and the mixture Daems, 1968; Yuen, 1968b; Byers and Ander- was poured into small grooves in agar-filled petri dish- es. The solidified agar, containing the nematodes, was son, 1972; De Grisse et al., 1974; Anderson and diced into 2- to 3-mm blocks that were transferred to Byers, 1975; De Grisse, 1977; Coomans, 1979b; glass vials containing 3% glutaraldehyde in 0.05 M Natasasmita, 1979; Shepherd et al., 1980; Bald- phosphate buffer (pH 6.8) at 22°C for chemical fixation win, 1982) have provided a substantial base for of the larvae. Subsequent rinsing and postfixation in osmium tetroxide were also carried out in 0.05 M phos- further investigations of these and other major phate buffer (pH 6.8). The glutaraldehyde fixation (for plant parasitic nematodes. Furthermore, in eval- 1.5 hr) was followed by washing in six changes of buffer uating the ultrastructure of plant parasitic nem- over a period of 1 hr. The agar blocks were then post- atodes, it is essential that information gained on fixed in 2% osmium tetroxide for 2 hr at 22°C, dehy- fundamental biology of the rhabditid nematode, drated in an acetone series, and infiltrated with a low viscosity embedding medium (Spurr, 1969). Silver-gray Caenorhabditis elegans, and a wide range of an- sections of selected nematodes were cut with a dia- imal parasitic species be applied to newly ac- mond knife and mounted on uncoated 75 x 300-mesh quired data on plant parasitic species (Yuen, copper grids. The sections were stained with uranyl 1968a; Wright, 1974, 1980; Ward et al., 1975; acetate and lead citrate and viewed in a Philips 301 electron microscope1 that was operated at 60 kV with Wareetal., 1975; Albertson and Thomson, 1976; a 20-Mm aperture. McLaren, 1976; Sulston, 1976). New terminol- ogy proposed by Coomans (1979a) has been used to describe certain regions of the nematode that show well denned triradiate symmetry. 1 Mention of a trademark, proprietary, product, or vendor does not constitute a guarantee or warranty of Previous ultrastructural observations of sec- the product by the U.S. Department of Agriculture and ond-stage larvae of the soybean cyst nematode does not imply its approval to the exclusion of other concentrated on the anterior neurosensory or- products of vendors that may also be suitable. 1 Copyright © 2011, The Helminthological Society of Washington PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY Results ampulla (Fig. 6). Microtubules (Mt) that occur The anterior cells of the procorpus were closely in the elongated cytoplasmic extension of the associated with the stylet protractor muscles dorsal gland appear to converge and terminate (Endo, 1983). The myofilamentous region of each at the base of the tetraradiate valve in the dorsal muscle cell is continuous with the sarcoplasmic gland ampulla (Figs. 6, 6a, 9). In the vicinity of region that lies adjacent and posterior to the sty- the valve, neurosecretion-laden nerve processes let knobs (Figs. 1-4). The cytoplasm around the (NP) lie close to the dorsal surface of the ampulla zone of attachment to the knobs is largely elec- (Fig. 8). Internally, the cytoplasm of the ampulla tron translucent except for the tonofilaments. A is interspersed with numerous dense secretory region of abundant mitochondria lies behind this granules with closely adhering membranes (Figs. zone (Figs. 2-4). 6, 8). The ampulla (Fig. 8) and the supporting dorsal Procorpus gland extension (Fig. 9) lie in contact with cells Two protractor muscle cells, one with its nu- that border the perimeter of the esophageal lu- cleus in view (Fig. 2), are shown to be separated men wall. Thus, when the stylet is retracted, the by another wedge-shaped cell—one of three such dorsal gland process takes the same sinuous route cells that have anterior extensions that traverse through the procorpus as the lumen (Figs. 6, 9). between the three stylet knobs. Their anterior The multicellular procorpus contains six nu- extensions surround the shaft of the stylet (Figs. clei that lie in the extreme anterior region, three 1-4) and slightly posterior to the stylet knobs, are associated with the stylet protractor muscles these same cells appear perradial in cross section and three with the stylet shaft tissues. In addi- and extend from the lumen wall to the basement tion, five nuclei occur in the midregion, and five membrane of the procorpus (Fig. 5). Each of the in the narrow posterior region of the procorpus, three perradial cells (ShC) and the three inter- just anterior to the metacorpus (Figs. 9, 10). radial protractor muscle cells (PMC) contain nu- "Constraining muscles" (CM) are present in merous mitochondria and a nucleus. The sar- the posterior region of the procorpus. These mul- coplasm of the secondary stylet protractor tidirectional muscle elements are primarily cir- muscles (ScC) lies between the arms of the per- cular in orientation with certain muscle elements radial muscle cells (ShC) and is bordered on the directed anteriorly (Figs. 1,9, 10, 12). These con- outside by the protractor muscle cells (PMC) straining muscles may affect the lateral limits of (Figs. 4, 5). the dorsal gland extension as it passes from the An integral part of the procorpus is the dorsally metacorpus into the procorpus. The esophageal located branch of the esophageal lumen that ends lumen (EL) is circular in cross section through in a tetraradiate valve within the ampulla of the this region and becomes triradiate at the meta- dorsal esophageal gland (Figs. 1, Ic, 6, 6a, 6b, 7, corpus pump (Figs. 12-14, 17-19). In cross sec- 8). The valve is shown in a closed position in tion, the constraining muscles are shown without longitudinal-oblique view (Figs. 6, 6a) and in hemidesmosomal contacts with the tubular lu- cross sections ranging from the highly sclerotized men wall (Fig. lOa). basal region (Figs. 6a, 7) to its distal regions (Figs. 6b and 8). In cross section, the distal parts of the Metacorpus closed valve form a cloverleaf pattern of multiple Posterior to the constraining muscles of the and single membranes (Fig. 6b). Ai; the junction procorpus, the lumen wall (ELW) is supported with the dorsal gland duct, the valve is contin- by multiple membranes (MM) and is surrounded uous with the anterior wall of the dorsal gland by longitudinally oriented elements of the pump Figure 1. Diagrams of longitudinal views (LV) through the esophagus of H. glycines. (a) LV of the anterior region. Numbers of the diagram correspond to the micrographs in the text, (b) Terminology of body regions of nematodes with emphasis on triradiate symmetry of the esophagus (after Coomans, 1979a; Grootaert and Coo- mans, 1980). (c) LV showing a closed valve or end apparatus within a dorsal gland ampulla. Note the infolded valve membrane curves into the valve duct lumen, (d) LV showing the open valve or end apparatus within one of a pair of subventral gland ampullae. Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 51, NUMBER 1, JANUARY 1984 DORSAL GLAND ORIFICE & VALVE 2,3, —5 4,6 7, 8 DORSAL GLAND AMPULLA SUBVENTRAL GLAND ORIFICE & VALVE 28 SUBVENTRAL GLANDS INTESTINE Copyright © 2011, The Helminthological Society of Washington 4 • PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY muscle (Fig.
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