Chapter 10

Ultrastructure of Initial Responses of Susceptible and Resistant Soybean Roots to Infection by the Soybean Cyst Nematode, Heterodera glycines ⁹

The initiation and development of syncytial nurse cells in host tissues are critical for the survival of infective cyst nematodes. The host-parasite relationship of the soybean cyst nematode, Heterodera glycines, in soybean (Glycine max [L.] Merr.) roots has been observed through light microscopy (Ross 1958; Endo 1964, 1965; Endo and Veech 1970; Veech and Endo 1970; Acedo et al. 1984), transmission electron microscopy (Gipson et al. 1971, Riggs et al. 1973, Endo 1978, Kim et al. 1987), and scanning electron microscopy (Jones and Dropkin 1976).

The feeding plugs—formed at the feeding sites of soybean roots infected by the soybean cyst nematode (Endo 1978) and other host-parasite interfaces (Wyss et al. 1984)—function as a seal between the stylet and host syncytium during feeding and at molt. The fine-structural observations of H. glycines infecting susceptible and resistant cultivar roots provide important data on the mechanisms of resistance and susceptibility (Gipson et al. 1971, Riggs et al. 1973, Kim et al. 1987). Syncytia induced by cyst nematodes contain a greater number of organelles than do the normal cells from which they are derived. At advanced stages of infection, syncytium walls adjacent to xylem vessels are modified into fingerlike ingrowths that resemble those of transfer cells (Jones and Northcote 1972, Jones and Gunning 1976, Stender et al. 1982, Wyss et al. 1984).

Light microscopy observations of syncytia and giant cells emphasize the presence of feeding tubes near the feeding site of these nurse cells (Rumpenhorst 1984). In vivo studies of the feeding process showed the interactions of stylet movement and secretion, cytoplasmic streaming, and food ingestion (Wyss and Zunke 1986). The ultrastructure of feeding tubes shows that the hardened salivary secretions are attached to the stylet of H. schachtii and indicates the continuity between the secretions emanating from the stylet and the feeding tube. Wyss and Zunke (1986) and Wyss et al. (1984) also reported that continuous food uptake lasts for up to 1 hour, including short pauses when the nematode salivates. Similar feeding-tube formation and accumulation of secretion granules in the dorsal gland ampulla occur in H. glycines during the infection of soybean roots (Endo 1987).

Although light and electron microscopic observations have provided new information on the interactions of the soybean cyst nematode and the soybean, the initial stages of infection and their relation to subsequent cytological modifications of host tissues have not been systematically examined. This chapter describes the ultrastructure of the initial stages of host-parasite interactions between the soybean cyst nematode and the roots of susceptible and resistant cultivars, with emphasis on nematode secretions (salivation) and host responses in the initial syncytial cell and adjacent cells.

Early responses of susceptible and resistant soybean cultivars to infection by the soybean cyst nematode, Heterodera glycines, are expressed by the accumulation of smooth and rough endoplasmic reticulum within a thick-walled initial syncytial cell. Nematode secretions are surrounded by a narrow region of endoplasmic reticulum that integrates with the rough endoplasmic reticulum of the host cytoplasm. The initial syncytial cell and adjacent cells that form the syncytium show slight enlargement at 18 hours after inoculation but have definite disruptions in their connecting cell walls. Although the endoplasmic reticulum closest to the stylet and associated secretions is not associated with mitochondria, the surrounding cytoplasm has rough endoplasmic reticulum interspersed among numerous mitochondria, plastids, and other organelles.

In most resistant cultivars, the syncytial cytoplasm contains extensively distributed wide cisternae, extending throughout the rough endoplasmic reticulum. These cisternae are less prevalent in syncytia induced in susceptible cultivars. Secretions varying greatly in electron density are found in infections at 18 hours to 2 days. The secretions nearest the nematode stylet appear uniform in distribution, whereas others have darkened peripheral cylindrical boundaries with clear to partially occluded centers. Syncytia in susceptible and resistant cultivars at 18 hours to 4 days after inoculation were hypertrophied and hyperplastic, contained expanded regions of cell-wall dissolutions and cell-wall depositions of callose, and sometimes included lysosomelike particles.

The advances in video-enhanced light microscopy coupled with electron microscopy should provide ways to further understand the process involved in host-parasite interaction of cyst nematode infection and to explore means of nematode control by interrupting these infection processes.

Ultrastructure of the initial responses of susceptible and resistant soybean roots to infection by the soybean cyst nematode is shown in figures 216–218, figure 219, figures 220–221, figures 222–223, figure 224, figure 225, figure 226, figure 227, figure 228, figure 229, figures 230–231, figure 232, figures 233–234, figure 235, and figure 236.

⁹ Reprinted in modified form with permission of the editor-in-chief, Révue du Nématologie 14:73-94, 1991.

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