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United States Department of Agriculture

Agricultural Research Service

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Chapter 6

Ultrastructure of Subventral Gland Secretory Granules in Parasitic Juveniles of the Soybean Cyst Nematode, Heterodera glycines5

Subventral and dorsal glands are prominent features of the esophagus of tylenchid nematodes. Secretory granules formed in these glands are of major interest in understanding host-parasite interactions of plant-parasitic nematodes of major crop plants (Bird 1968a,b, 1969; Rumpenhorst 1984; Wyss et al.1984; Hussey 1989a; Endo 1991). The extensions of the subventral glands in second-stage juveniles (J2) of the root-knot nematode, Meloidogyne javanica, accumulated secretory granules shortly before hatching, and the granules changed in morphology within 1–3 days after entry into the host. During this time there was a threefold enlargement of the dorsal and subventral glands (Bird 1967). These studies stimulated interest in esophageal gland structure-function relations in other species of endoparasitic nematodes.

Changes in morphology of secretory granules in the dorsal esophageal gland occurred between preparasitic and parasitic J2 stages of development in the cyst nematode, Heterodera glycines. As feeding occurred, secretory granules in dorsal glands of parasitic J2 varied substantially in size and in electron density—from small and moderately electron-opaque secretory granules to large and low-density secretory granules as feeding occurred (Endo 1987). Previous work on M. javanica (Bird 1967, 1975; Bird and Saurer 1967) and in vivo observations of Heterodera schachtii (Wyss 1992) emphasized that subventral glands play an active role in the parasitic behavior of these and related nematodes. This chapter emphasizes the changes in morphology of secretory granules of subventral esophageal glands and their sites of synthesis and modification during the infection of soybean by the soybean cyst nematode.

Secretory granules of the subventral esophageal glands of H. glycines showed considerable changes in morphology soon after penetration and following initiation of syncytia in soybean roots. Within 3 hours after inoculation, the electron-opaque secretory granules—usually found in subventral gland cells and their extensions—became electron-transparent except for small electron-opaque residues within the secretory granule membranes. In samples taken 18 hours after inoculation and later, subventral gland extensions of parasitic second- and third-stage juveniles contained small, electron-opaque secretory granules. The subventral glands were also characterized by the presence of moderate to very large flocculate secretion bodies within a dense matrix of rough endoplasmic reticulum, mitochondria, and Golgi apparatus.

The activity of the Golgi apparatus was directly related to the formation and accumulation of condensing vesicles that appeared to merge with each other to form the larger secretory granules occurring in the subventral glands of parasitic stages of the nematode. The large flocculate secretion bodies were observed as early as 10 hours after inoculation and contrasted with the dense cytoplasm of the subventral glands observed 6 days after inoculation. The synthesis, assembly, accumulation, and transport of secretory granules within the subventral glands of the soybean cyst nematode appeared to change during parasitism.

Considerable progress has been made in developing monoclonal antibodies for various components of esophageal glands of H. glycines (Atkinson et al. 1988, Atkinson and Harris 1989, Goverse et al. 1994), Meloidogyne incognita (Hussey 1989b; Hussey et al. 1990; Davis et al. 1994), and various other species of Meloidogyne (Davis et al. 1991). This technology will provide ways to understand the mechanism of parasitism by localizing the site of nematode secretions in or within syncytia and giant cells induced by cyst and root-knot nematodes, and will also provide ways to determine the function of secretory components synthesized in the esophageal glands.

Ultrastructure of the subventral gland secretory granules in parasitic juveniles of the soybean cyst nematode is shown in figure 126, figures 127-128, figures 129-131, figures 132-134, figures 135-136, figures 137-138, figure 139, figures 140-141, figures 142-143, and figures 144-145.

5 Reprinted in modified form with permission of the Helminthological Society of Washington from Journal of Helminthological Society of Washington 60:22–34, 1993a.

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