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Changes in Esophageal Gland Activity During the Life Cycle of Nacobbus Aberrans (Nemata: Pratylenchidae) 1

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Changes in Esophageal Gland Activity During the Life Cycle of Nacobbus Aberrans (Nemata: Pratylenchidae) 1 Journal of Nematology 30(3):275-290. 1998. © The Society of Nematologists 1998. Changes in Esophageal Gland Activity During the Life Cycle of Nacobbus aberrans (Nemata: Pratylenchidae) 1 RICARDO M. SotrZA AND J. G. BALDWIN 2 Abstract: Electron and light microscopy were used to study the dorsal gland (DG) and the two sub- ventral glands (SvG) of seven developmental phases of Nacobbus aberrans: pre-parasitic second-stage juveniles (12), parasitic J2, third- (13) and fourth- (14) stages, migratory females, young sedentary females, and mature sedentary females. In each developmental phase the level of esophageal gland activity, was estimated by the abundance of organelles associated with secretory pathways, including endoplasmic reticulum, ribosomes, Golgi, multivesicular bodies, and secretory granules. All esophageal glands were metabolically active in all J2 examined, although only in parasitic J2 were there numerous secretory granules in the esophageal gland extensions and ampuUae. No evidence of secretory activity was observed in the esophageal glands of the coiled and relatively inactive J3 and J4, nor in migratory females; these stages apparently do not feed. Observations suggest that reserves stored by J2 sustain three ecdyses and the migratory female's search for a feeding site and induction of a syncytium. Feeding activity is resumed in young and mature sedentary females, in which the DG is highly active and enlarged. The SvG are metabolically active, but with little synthesis of secretory granules, suggesting that in sedentary females the SvG may have physiological roles other than digestion. Key words: esophageal glands, feeding biology, gland activity, Nacobbus aberrans, nematode, Pratylen- chidae, ultrastructure. Investigations of the dorsal gland (DG) Schuurmanns Stekhoven, none of the and the two subventral glands (SvG) of para- esophageal glands seem to be involved in sitic Tylenchida have begun to unveil the intracellular migration (Wyss, 1992; Wyss et complex role of these esophageal glands in al., 1992; Zunke, 1990). In all species exam- the life cycle and in parasitism (Baum et al., ined it appears that DG secretions play a 1996; De Boer et al., 1996; Endo, 1993; Hus- role in induction and maintenance of sed- sey and Mires, 1990; Ray et al., 1994; Willats entary feeding sites. SvG secretions, once et al., 1995; Wyss, 1992; Zunke, 1990). The thought to flow exclusively into the intes- SvG presumably play a role in hatching of tine, recently were detected as a component Meloidogyne javanica (Treub) Chitwood of stylet secretions (Day'is et al., 1994; Endo, (Bird, 1968). Video-recording studies of in- 1987, 1993; Goverse et al., 1994). fective second-stage juveniles (12) of Het- To perform such a range of functions, the erodera schachtii Schmidt and M. incognita esophageal glands must have a precisely (Kofoid & White) Chitwood suggest that timed developmental program, in which esophageal gland secretions are not used for perception of environmental conditions and root penetration (Wyss and Zunke, 1986; signals, neural coordination, genetic expres- Wyss et al., 1992). In M. incognita all three sion and suppression, and glandular secre- esophageal glands seem to participate in tory pathways are coordinated throughout the intercellular migration of parasitic J2 the life cycle of the nematode. Currently, through roots; conversely, in H. schachtii our limited understanding of developmen- and (Cobb) Filipjev & Pratylenchus penetrans tal biology of esophageal glands is based pri- marily on Meloidogyne and Heterodera, both Received for publication 24 November 1997. sedentary endoparasites. In these two het- 1 Part of the first author's dissertation for a Ph.D. degree in eroderids, the SvG seem to be most active in Plant Pathology. Research funds provided by grants from the UC/Pacific Rim Research Program and National Science Foun- the infective J2, with a reduction of secretory dation DEB-9318249. First author's full scholarship provided by activity coordinated with the onset of para- the Brazilian Conselho Nacional de Desenvolvimento Cien- tifico e Tecnol6gico. sitism. Conversely, days after the initial in- 2 Graduate student and Professor, University of California, Department of Nematology, Riverside, CA, 92521. duction of a feeding site the DG activity E-mail: [email protected], [email protected] reaches a peak and remains high through- The authors gratefully acknowledge Teresa Mullens for pro- riding Pratylenchus vulnus specimens, and Edward Platzer and out the life cycle (Endo, 1984, 1987, 1993; Philip Roberts for reviewing the manuscript. Endo and Wergin, 1988; Hussey and Mires, 275 276 Journal of Nematology, Volume 30, No. 3, September 1998 1990). In all other parasitic Tylenchida, rep- source of specimens at seven developmental resenting many parasitic habits, the develop- phases examined in this study: active pre- mental biology of esophageal glands re- parasitic J2; active parasitic J2, J3, J4; migra- mains virtually uninvestigated, except for tory females; young sedentary females; and two electron microscopy studies that suggest mature sedentary females. Active pre- that all three esophageal glands remain ac- parasitic J2 were obtained by hatching eggs tive throughout the life cycles of the migra- in water, and subsequently they were kept tory endoparasites P. penetrans and Di- for 48 hours at room temperature for full tylenchus dipsaci (Kuhn) Filipjev (Endo et al., extension of the esophageal glands. Active 1997; Shepherd and Clark, 1983). parasitic J2 and active migratory females To expand the understanding of the role were obtained by gentle blending of in- of esophageal glands in parasitism in a fected roots, followed by sieving and selec- broader range of taxa and parasitic habits, tion of specimens under a dissecting micro- we selected Nacobbus aberrans (Thorne) scope. The J3, J4, young sedentary females Thorne & Allen (Pratylenchidae), an eco- with up to 10 laid eggs, and mature seden- nomically important parasite of sugarbeet tary females with large egg masses were re- and vegetables in the United States and in moved from infected roots under a dissect- some Latin American countries (Inserra et ing microscope. The vitality of sedentary fe- al., 1985). In its life cycle of 36 to 38 days at males was inferred by absence of fungi 25°C, the migratoryJ2 molts into a relatively colonizing their bodies and by the presence inactive, coiled, third- (]3) and fourth- (J4) of visiting active males. The specimens were stage juvenile. The vermiform, immature fe- transferred to 1% sodium chloride solution males are migratory endoparasites that, in and immediately prepared for microscopy. response to an unknown signal, become ses- For light microscopy, the specimens were sile, swell for production of eggs, and induce mounted on temporary slides with the anes- the formation of a syncytium that exhibits thetic 0.1 M sodium azide, modified from only minor differences from the syncytia of Sulston and Hodgkin (1988), and observed Heterodera (Inserra et al., 1985). with an interference-contrast microscope Since the life cycle of N. aberrans includes (IM). At least 15 specimens of each develop- a migratory phase similar to pratylenchids mental phase were observed with IM. For and a sedentary phase to heteroderids, we comparison, the same procedure was used suggest that this species is a useful model for to observe different life stages of P. vulnus. understanding the role of esophageal For transmission electron microscopy, all glands in both feeding biologies. In this de- developmental phases were fixed at room velopmental study of esophageal glands we temperature with 2% osmium tetroxide so- combined electron and light microscopy to lution in 0.1 M sodium cacodylate buffer at estimate the esophageal gland activity pH 7.2, with 1.5 mM of calcium chloride throughout seven developmental phases in added. Depending on the life stage, 20 to 40 five life stages of N. aberrans. We also briefly minutes later the specimens were cut in two examined the esophageal gland activity of and returned to the fixative for a total fixa- Pratylenchus vulnus Allen & Jensen to allow tion time of 2.5 hours. Following a thorough comparison with an exclusively migratory rinse with 1% sodium chloride, the speci- parasitic habit. mens were stained with aqueous 1% uranyl acetate at 4°C for 15 hours, and rinsed MATERIALS AND METHODS again. Specimens were placed in 5% agar blocks, dehydrated with serial acetone solu- A single Mexican isolate of N. aberrans tions, and infiltrated and embedded in maintained on tomato (Lycopersicon esculen- Spurr resin (Spurr, 1969). turn Mill) in the University of California- An MT 6000 Sorval ultramicrotome and Riverside (UCR) Quarantine Facility was the diamond knife were used to obtain serial sil- Esophageal Gland Activity in Nacobbus aberrans: Souza, Baldwin 277 ver-to-gold sections, which were post-stained RESULTS with lead citrate (Reynolds, 1963). A Hitachi Nacobbus aberrans H600 transmission electron microscope (TEM) was operated at 75 kV. Four to eight Pre-parasiticJ2: The DG and SvG ampullae specimens in each developmental phase and extensions of pre-parasitic J2 were slen- were examined with TEM, and at least two der and appeared to lack contents (Fig. 1A). specimens in each phase were examined The larger, basal portions of the esophageal throughout the entire length of the esopha- glands, herein referred to as lobes, were well gus. extended, and each lobe had a distinct A B 0 FIG. 1. Diagrammatic
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