ultrastructure of modified root-tip cells in ficus carica, induced by the ...

J. Cell Sci. 4i, 193-208 (1980)
Printed in Great Britain © Company of Biologists Limited 1980
SUMMARY
ULTRASTRUCTURE OF MODIFIED ROOT-TIP
CELLS IN FICUS CARICA, INDUCED BY THE
ECTOPARASITIC NEMATODE
XIPHINEMA INDEX
U. WYSS,' H. LEHMANNf AND R. JANK-LADWIGf
• Institut fUr Pflanzenkrankhciten und Pflanzenschutz der Universitat Hannover,
Herrenhauser Str. 2, .D-3000 Hannover 21, FRG, and
f Botanisches Institut der Tieraratlichen Hochschule Hannover,
BOnteweg 17 d, D-3000 Hannover 71, FRG
The migratory ectoparasitic root nematode Xiphinema index, added to Ficus carica seedlings
in sterile agar culture, fed exclusively on the tips of the roots. As a response the tips started to
swell and became transformed into terminal galls as long as feeding was continued.
When the cytology of swollen root-tips was examined 24 h after the first nematode attack,
necrotic cells, scattered singly or in small groups within the root apex, were found in ultrathin
sections. These cells, whose protoplasts showed features of a hypersensitive reaction, were most
probably those fed upon by the nematodes. Each necrotic cell was surrounded by several
enlarged, mostly binucleate cells with dense cytoplasm. One day later the binculeate cells
were multinucleate, containing 4 or even 8 nuclei. The clear-cut demarcation between necrotic
and modified cells indicated that only the stimulus for the induction of modified cells but not
the stimulus for cell necrosis passed into neighbouring cells.
Root-tip galls that provided the appropriate food for egg production in nematodes contained
greatly enlarged multinucleate cells between necrotic cells. The modified cells showed features
of high metabolic activities, expressed in nuclear and nucleolar hypertrophy, invagination of
the nuclear envelope, increased cytoplasmic density, abundance of mitochondria, plastids and
rough endoplasmic reticulum. Wall ingrowths, typical of transfer cells, were rare and if present
occurred only adjacent to necrotic cells. In older modified cells new cell plates, surrounded
by phragmoplasts, were formed.
INTRODUCTION
Xiphinema index Thorne & Allen, 1950, with a world-wide distribution in soils
where vines are grown, was the first nematode species proved to be the vector of a
plant pathogenic virus (Hewitt, Raski & Goheen, 1958), and various aspects of its
biology, ecology and pathogenicity have since been studied in more detail. The host
range appears to be restricted to a few plants amongst which vine (Vitis vinifera L.)
and fig (Ficus carica L.) support a rapid population increase under controlled conditions
in glasshouses with temperatures above 20 °C. Attacked root-tips of both
plants become transformed into terminal gals. Sections through these galls reveal
modified enlarged multinucleate cells (Radewald & Raski, 1962; Weischer & Wyss,
1976; Wyss, 1978; Lehmann & Wyss, 1978; Rumpenhorst & Weischer, 1978) which

194 U. Wyss, H. Lehmann and R. Jank-Ladwig
are thought to play an important role in the successful development of the parasite
(Weischer & Wyss, 1976; Wyss, 1978).
X. index is a migratory ectoparasitic nematode which frequently changes its
feeding sites. The feeding behaviour on vine and fig roots has been studied (Fisher
& Raski, 1967; Weischer & Wyss, 1976; Wyss, 1977 a, b) and recorded in a research
film (Wyss & Inst. wiss. Film, 1977). Roots of fig seedlings grown in agar are usually
first attacked in the region of cell elongation or in the transition zone between the
root apex and cell elongation. The nematode inserts its odontostyle 3-4 cells deep
before it starts feeding on a column of cells, with ingestion periods rarely exceeding
10 min per individual cell during the initial attacks on root-tips. Root growth is soon
retarded if feeding by a single female or late larval stage (L4) is continued for several
hours at different sites along the root-tip. The tip starts to swell and gradually
becomes transformed into a terminal gall as long as the nematode maintains its
attack for several days. Galled root-tips remain strongly attractive to feeding nematodes
and obviously provide the appropriate food source for egg production in
females. Meristematic activities within the root-tip swellings and galls are usually
only temporarily arrested (Wyss, 1978).
The main purpose of this study was to obtain a deeper insight into the development
and ultrastnicture of modified root cells induced by a migratory ectoparasitic nematode
and to compare these cells with the well-known cellular adaptations induced by
sedentary endoparasitic nematodes.
MATERIALS AND METHODS
Dried Ficus carica fruits (Izmir figs) were soaked overnight in distilled water. On the
following morning the seeds were removed, washed and surface-sterilized for 20 min in a
filtered 4% Ca(OCl)i. 4HtO solution. The seeds were then washed for 1 h in sterile water
and transferred on to o-8 % distilled water agar in plastic Petri dishes for germination under
artificial light or in daylight at about 25 °C. When the seedlings were 2-3 weeks old they were
inserted singly into a layer 2 mm thick of o-6 % distilled water agar in plastic Petri dishes and
a few drops of Hoagland's solution No. 1 were added. The plates were sealed with ParafUm
and stored at 25 °C and about 3000 lux (16 h exposure/day) until they were inoculated with
sterile nematodes.
Stock cultures of nematodes were kept in growth chambers (25 °C) on fig plants, cultured
in sand with little organic matter, in which high population densities of up to 800 nematodes/
100 ml soil developed. After extraction, batches of about 100 females and late larval stages
(L4) were transferred into a 0-03 % NaNs solution in sterile staining blocks where the nematodes
were soon immobilized. After 1 h the sterilant was replaced twice in. quick succession by
sterile distilled water and the nematodes were transferred on to agar in Petri dishes. One day
later the most active females and late larval stages were removed with a microneedle and placed
singly or in batches of 10 on to fig seedlings with roots that had just started to grow well.
The cultures were then kept at 25 °C, but now the light intensity was reduced to 500-700 lux
(16 h exposure/day). Nematode feeding was examined daily and attacked root-tips of different
developmental stages from the first nematode attack were cut and processed for electronmicroscopic
studies.
Excised root-tips were fixed for 2 h in 3% glutaraldehyde in 0-05 M sodium cacodylate
buffer (pH 6-8), washed in 12 changes of buffer and postfixed for 2 h in 2 % osmium tetroxide,
all at room temperature. After a few washings in buffer, the postfixed root-tips were dehydrated
in an acetone series, followed by propylene oxide, and embedded in Durcupan (Fluka).
Ultrathin sections were cut on a LKB Ultratome I with glass knives and mounted on Formvar-

, > , • • . - .
Modified root-tip cells in Ficus
1/V.S
••'1 i / m
Fig. i. LS through a parasitized swollen root-tip, i day after the first nematode
attack. Necrotic cells (TIC) within the transition zone between root apex and cell
elongation are surrounded by modified, mostly binucleate cells with lobed nuclei
(arrows). The modified cells bulge into the necrotic cells whose contents have most
probably been removed by nematode feeding. Nucleoli (mi) are occasionally left in
the necrotic cells. Binucleate cells with wall stubs (tos) attached to the mother cell wall
occur at some distance from the necrotic cells, x 1700.
WS
1

196 U. Wyss, H. Lehmann and R. Jank-Ladwig
coated copper grids. The sections were stained for 10 min with 5 % aqueous uranyl acetate
and then for 15 min with lead citrate. The ultrathin sections were examined in the EM 10A
(Zeiss) or Elmiskop IA (Siemens).
RESULTS
Modified cells in swollen root-tips, 1-3 days after the first nematode attack
Sections through the apical region of unattacked, well growing root-tips of Ficus
carica seedlings displayed characteristic features of meristematic cells. All cells were
uninucleate and contained relatively large, more or less spherical nuclei embedded
in dense cytoplasm. However, when parasitized swollen root-tips were examined
12-14 h after the first attack by a single nematode or several individuals, distinct
cellular alterations were observed in the transition zone between the root apex and
cell elongation. A general view of these changes is given in Fig. 1. A few necrotic
cells, either devoid of cytoplasm or still partially filled with degraded contents, were
surrounded by cells undergoing modification. These cells were now 2-3 times as
large as corresponding cells in unattacked well growing root-tips, and they were
usually binucleate. Their nuclei were now considerably lobed and slightly enlarged
and were embedded in dense cytoplasm. There was always a clear-cut demarcation
between the necrotic and modified cells (Figs. 1, 2), a necrotic response was never
seen to spread into cells bordering the site of necrosis. The necrotic cells resulted
most probably from direct injury by the nematode's odontostyle and from the
subsequent injection of saliva and removal of cell contents during ingestion. In an
earlier light-microscopic study on X. index-feeding sites (Wyss, 1978) necrotic cells
were occasionally found whose walls were perforated by holes of approximately the
same diameter as that of the nematode's odontostyle. Fig. 2 shows characteristic
features of necrotic cells, still partially filled with degraded contents. Disorganized
nuclei, nucleoli and cytoplasm were more electron-dense in these than in adjacent
modified cells. The numerous vacuoles appeared to have fused, and myelin-like
multilamellar dense structures were common (Fig. 2, inset). Organelles such as
mitochondria and plastids were no longer recognizable.
In spite of numerous examinations, no stages of cell-plate development could be
detected between daughter nuclei of binucleate cells adjacent or close to the necrotic
Figs. 2-4. Feeding of Xiphinema index on root-tips of Ficus carica seedlings. LS
through parasitized swollen root-tips.
Fig. 2. Necrotic cells (nc) surrounded by modified cells, 1 day after the first nematode
attack. Note the clear-cut demarcation between the 2 cell types. The degraded cytoplasmic
contents and nuclei (n) of the necrotic cells are more electron-dense than
those of the modified cells. Vacuoles in the necrotic cells have fused, and multilamellar
dense structures are common. These structures (within white outline) are
shown at higher magnification in the inset, x 4800; inset, x 17000.
Fig. 3. Two binucleate cells, a few cell layers distant to the necrotic cells, 2 days
after the first nematode attack. Wall stubs (ws) are attached to the mother cell wall in
the region of the equatorial plane, x 3900.
Fig. 4. Magnification of a wall stub shown in Fig. 4. Plasmodesmata (pd) are
present, and the end of the stub is bent and slightly swollen, x 11000.

•i*
Modified root-tip cells in Ficus

198 U. Wyss, H. Lehmann and R. Jank-Ladwig
Figs. 5, 6. Feeding of Xiphinema index on root-tips of Ficus carica seedlings. LS
through parasitized swollen root-tips.
Fig. 5. Necrotic cells (nc) with remaining nucleoli (nu) surrounded by enlarged
modified cells with up to 4 nuclei at the plane of section, 2 days after the first nematode
attack. Numerous small vacuoles are dispersed in the cytoplasm of the modified cells,
x 2000.
Fig. 6. Illustration of 2 enlarged nuclei with invaginated envelopes, 3 days after the
first nematode attack, x 6000.
cells. Wall stubs were, however, seen at some distance from necrotic cells (Fig. 1).
These wall stubs were always attached to the mother cell wall, approximately in the
region of the equatorial plane. Fig. 3 shows 2 binucleate cells with such wall stubs at
a higher magnification. In a number of cells, stubs opposite to each other were present
on the mother cell walls. Plasmodesmata were fully developed in the stubs (Fig. 4).
Sections through 2- to 3-day-old root-tip swellings revealed modified cells that had
increased in size and which were now multinucleate, possessing 4-8 enlarged nuclei
(Fig. 5). Again, no cell wall stubs were present in the modified cells adjacent to
necrotic cells. The necrotic cells, devoid of cytoplasm, frequently contained several
well preserved but rather compact nucleoli which indicated that these cells were
multinucleate before they were disorganized by nematode attack.
Modified cells in root-tip galls, 6-12 days after the first nematode attack
When single or several nematodes continued feeding on the same root-tip, the
terminal swelling became gradually transformed into a gall which in many cases
remained strongly attractive to the feeding nematodes. Five to six days after the first
attack some galls were fed upon by females which in the meantime started to produce

Modified root-tip cells in Ficus 199
eggs. Egg production was maintained for several days or even weeks as long as the
females continued feeding on these galls. Depending on the age of the gall, modified
cells within it were now greatly enlarged. Expansion of the multinucleate cells was
so pronounced that early necrotic cells were heavily crushed, nearly disappearing
between the expanding cells. Fig. 7 shows the probable fate of early necrotic cells,
now degraded at the plane of section to 'intercellular spaces' between 2 expanding
modified cells. The spaces are filled with dense multilamellar structures which, as
described before, are typical constituents of necrotic cells. Modified cells in 10- to
12-day-old galls could reach dimensions 10-15 times the size of early binucleate
interphase cells. In some of them more than 16 nuclei, clustered together, were
counted.
Many nuclei within modified cells had a highly invaginated, nearly amoeboid
profile (Fig. 6). Their nucleoli were hypertrophied and most had large vacuoles.
Mitochondria and plastids had increased in number in modified cells and their
shapes became strikingly heteromorphic. Massive aggregations of these organelles,
mainly near cell walls, were common (Figs. 7, 11). A large proportion of the densely
staining plastids contained starch grains (Figs. 8, n) and most of them possessed an
interplastidial membrane system (Fig. 8). Apart from these features, high metabolic
activity in transformed cells was further expressed by the dense cytoplasm and the
abundance of rough endoplasmic reticulum commonly arranged in parallel strands
(Figs. 11, 12). Occasionally the strands were arranged in concentric whorls around
vacuoles (Fig. 9). The high cytoplasmic density of modified cells in root-tip galls
supporting nematode reproduction is clearly illustrated in Fig. 12. The cytoplasm of
the cell with 3 nuclei in the plane of section is so dense that, at this level, the total
area of the numerous vacuoles scattered within the cytoplasm would hardly exceed
that of the smallest nucleus.
Enlarged, previously active, but now necrotic cells were found next to metabolically
highly active cells (Fig. 11). Again the necrotic response did not spread into these
cells. Occasionally, however, ingrowths were noted on the walls of modified cells
adjacent to necrotic cells (Figs. 10, 11). These wall protuberances were only found in
modified cells near the periphery of necrotic root-tip galls. Some protuberances, with
anastomosing branches extending relatively deeply into the cells (Fig. 10), were well
developed. As in typical wall ingrowths of 'transfer cells' the plasmalemma surrounding
the protuberances was not ruptured.
In older modified cells stubs attached to the cell walls were commonly noted
(Figs. 13-17), and, less frequently, wall fragments embedded in cytoplasm (Fig. 13)
were also recorded. An interesting feature within some older cells was the formation
of new cell plates, surrounded by typical phragmoplasts with newly formed nuclei at
their poles (Figs. 15, 17) and associated with dictyosomes (Fig. 16). The detection of
new cell plates in older cells suggests that thin-walled long stubs (Figs. 14, 15) or
irregular thin walls fusing with thicker walls (Fig. 15, arrow) might have been formed
recently by the fusion of the cell-plate vesicles. Fig. 16 shows a cell plate apparently
growing towards an old wall stub.

U. Wyss, H. Lehmann and R. Jank-Ladwig

DISCUSSION
Modified root-tip cells in Ficus 201
The cellular modifications induced by the ectoparasitic and migratory dorylaimid
nematode Xiphinema index resemble in many respects those induced by the specialized
endoparasitic and sedentary tylenchid nematodes of the genera Globodera, Heterodera,
Meloidogyne (Heteroderidae) and Nacobbus, Rotylenchulus (Nacobbidae) so far
examined. At the ultrastructural level the feeding sites of the genera mentioned and
of X. index show characteristic features of metabolically active cells. This is expressed
especially in the enlarged nuclei with usually irregular, lobed outlines and with
hypertrophied nucleoli, in increased cytoplasmic density with the cytoplasm containing
numerous small vacuoles, in the proliferation of rough endoplasmic reticulum and in
increased numbers of mitochondria and plastids. Apart from considerable changes in
size and form, the plastids of X. »n&.v--transformed cells, but not of control root cells,
contained thylakoids. This is probably not so surprising (though inexplicable), as the
Ficus carica seedlings were exposed to light, bearing in mind that chloroplasts with
few lamellae developed in Meloidogyne incognita-infected tomato root galls, but only
when these were exposed to light (Orion, Gommers & van Bezooijen, 1973). Syncytia
of Heterodera schachtii-'mfected roots turn green when these are exposed to light
(J. Miiller, personal communication).
Well developed wall ingrowths occur in the syncytia and giant cells induced by
Heteroderidae but not in the syncytia induced by Nacobbidae (Jones & Payne, 1977).
Wall ingrowths with anastomosing branches were occasionally also observed in
X. in^fet-transformed cells, at the periphery of the galled root-tips and only on
limited areas in the immediate vicinity to empty necrotic cells. Wall ingrowths are
thought to develop as a response to the flow of solutes from conducting elements of
the xylem and phloem across the plasmalemma of adjacent cells, and it is suggested
that their function is to increase the surface area of the plasmalemma for the uptake
of solutes (cf., for example, Jones & Dropkin, 1975). Cells with such characteristics
are common in plants and are termed transfer cells (Gunning & Pate, 1969). The
hypothesis that syncytia or giant cells, induced by sedentary Heteroderidae are
Figs. 7-10. Feeding of Xiphinema index on root-tips of Fiais carica seedlings. LS
through 6- to 12-day-old root-tip galls.
Fig. 7. The intercellular space (tip) between greatly enlarged modified cells is
filled with lamellar structures which are most probably degraded remnants of crushed
necrotic cells. The lamellar structures (within black rectangle) are shown at higher
magnification in the inset. Note the aggregation, of mitochondria and plastids, the
latter with interplastidial membranes, x 8000; inset, x 40000.
Fig. 8. Single plastid with 2 starch grains (st) and showing the interplastidial
membrane system, t, thylakoids x 41000.
Fig. 9. Modified cells are rich in endoplasmic reticulum (er). Here it is arranged in
concentric whorls around a vacuole. x 9000.
Fig. 10. Wall ingrowths (1) invested by an intact plasmalemma (/>) are occasionally
formed adjacent to necrotic cells. In this case the intercellular space between 3
modified cells is a necrotic cell (nc), x 7000.
14 CEL 41

2O2 U. Wyss, H. Lehmann and R. Jank-Ladwig

Modified root-tip cells in Ficus 203
multinucleate transfer cells and that the wall ingrowths are formed as a consequence
of continuous nematode demands for nutrients (Jones & Northcote, 1972) is now
widely accepted. Fingerlike wall ingrowths were also observed in root-tip cells of
celery, parasitized by the ectoparasitic and migratory dorylaimid nematode Longidorus
apulus (Bleve-Zacheo, Zacheo, Lamberti & Arrigoni, 1977) which belongs to the
same family as X index. The authors suggest that in this particular case, in which
the feeding site of the parasite is not fixed (and where thus the nutrient demand is not
continuous), the ingrowths may have a double function: to stop the spread of the
necrotic area adjacent to the cells and to improve the cell-to-cell transport when the
meristematic tissue of the root-tip is inactivated. In this connexion it is worthwhile
mentioning the unusual finding by Gunning, Pate & Green (1970), who observed
tufts of wall ingrowths of yet unknown function around intercellular spaces in leaf
traces of the goosegrass (Gallium aparine).
Modified root-tip cells induced by X. index on its host F. carica also show similarities
in their ultrastructure to cells of the nutritive tissue in galls induced by zoocecidia
such as by Cecidomyidae (Rohfritsch, 1971), Chermesidae (Rohfritsch, 1977) and
Cynipidae (Rohfritsch, 1974). The nutritive cells of these zoocecidia are characterized
by a large lobed nucleus, nuclear hypertrophy, abundant cytoplasm, reduction and
fragmentation of the vacuome, abundance of ribosomes, plastids and mitochondria.
X. index-modified cells show even greater similarities to nutritive cells in galls
induced by certain acarocecidia which disturb cytokinesis so that bi- or multinucleate
cells with wall fragments attached to the mother-cell wall are formed (Westphal, 1977).
Multinucleate cells induced by X. index are apparently formed by repeated mitoses
without cytokinesis (Wyss, 1978; Rumpenhorst & Weischer, 1978), and they thus
resemble in this respect giant cells induced by Meloidogyne spp. (Huang & Maggenti,
1969; Jones & Payne, 19780). According to Bird (1979), the term coenocyte should
be used for multinucleate cells formed by repeated mitoses without cell division,
whereas any enlarged uninucleate cell may be a giant cell. The multinucleate state
of X. zncfoc-induced coenocytes arises by synchronous mitoses (Rumpenhorst &
Weischer, 1978; Wyss, unpublished) which are typical of most naturally and artificially
created multinucleate cells (Fowke, Bech-Hansen, Gamborg & Constabel,
Figs. 11-13. Feeding of Xiphinema index on. root-tips of Ficus carica seedlings. LS
through 6- to 12-day-old root-tip galls.
Fig. 11. Enlarged modified cells adjacent and near a necrotic cell (nc). The large
cell at the centre contains dense cytoplasm and endoplasmic reticulum (er) arranged
in parallel strands. Wall ingrowths (i) grow into the cell adjacent to the necrotic cell.
Note the aggregation of plastids (p) with starch grains in a neighbouring cell, x 3200.
Fig. 12. A necrotic cell (nc) surrounded by modified cells. The cell with 3 nuclei
at the plane of section is filled with extremely dense cytoplasm (compare the small
vacuoles (uj) with those (t>j) of a neighbouring cell), x 2000.
Fig. 13. Wall stubs (foi) are quite commonly found in older modified cells.
Occasionally wall fragments, not attached to cell walls, are also found, x 2300.
14-2

204 U. Wyss, H. Lehmann and R. Jank-Ladwig

Modified root-tip cells in Ficus 205
In the early stage of X. index-coenocyte formation cell wall stubs, attached to the
mother cell wall, were seen to protrude into binucleate cells at some distance from
parasitized necrotic cells. These stubs resulted most probably from incomplete fusion
of cell plate vesicles. Similar protruding wall fragments are formed when roots are
treated with caffeine (Roper & Roper, 1977; Jones & Payne, 19786) which does not
affect mitosis. From the description by Jones & Payne (19786) o-i % caffeine applied
to growing roots of Impatiens balsamina inhibited root growth and caused root-tips
to swell. This effect is very similar to the early stage of root response to X. index
attack (Wyss, 1978). Cell wall fragments observed in older X. in^ex-coenocytes were
attributed to cell wall dissolution (Wyss, 1978; Lehmann & Wyss, 1978). We now
hesitate to maintain this statement, as holes in a continuous wall were very rare and
as such striking symptoms of cell wall lysis as shown in affected cells by Rotylenchuhis
reniformis (Rebois, Madden & Eldridge, 1975) and Longidorus apulus (Bleve-Zacheo
et al. 1977) were never observed. Thin and rather irregular cell walls in older coenocytes
are undoubtedly formed by renewed cytokinesis. To our knowledge this
feature, involving typical phragmoplast and cell plate formation, is unique in
nematode-transformed plant cells. It possibly represents the initial stage of renewed
meristematic activities at the onset of new lateral root formation. As described earlier
(Wyss, 1978) lateral roots were often seen to emerge from X. index-mduceA root-tip
galls.
Modified feeding sites are also induced by invertebrate - (e.g. Poinar & Hess, 1974)
and vertebrate-parasitic nematodes (Wright, 1974; Lee & Wright, 1978). The
migratory trichurid nematode Capillaria hepatica induces for instance in the liver of
its host mouse a syncytial feeding site, consisting of multinucleate food cells whose
contents are ingested and which ultimately degenerate (Wright, 1974). It is suggested
that the parasite progressively induces new feeding sites on its migration through the
liver. A similar host-parasite relationship was shown for Trichuris muris in the
caecum and colon of its mouse host (Lee & Wright, 1978). In this respect X. index
shows in its behaviour and in conjunction with associated responses of the host
tissue, closer affinities to the mammal parasites mentioned than to sedentary plant
parasitic nematodes which, as long as they live, do not destroy the cellular alterations
they induce and maintain.
Figs. 14-17. Feeding of Xiphinema index on root-tips of Ficus carica seedlings. LS
through 6- to 12-day-old root-tip galls.
Fig. 14. Modified cells with several wall stubs (tos). x 1600.
Fig. 15. Two older modified cells with new cell plates {cp), each surrounded by a
phragmoplast. Nuclei (n) are found at both poles of the phragmoplasts. Note the two
thin and irregular walls, one fusing with a thick wall with a stub (tos) at its end
(arrowhead), x 3000.
Fig. 16. A new cell plate (cp), surrounded by dictyosomes (d), is orientated towards
the stub (tus) of an older cell wall, x 13000.
Fig. 17. New cell plate (cp) surrounded by a phragmoplast between 2 newly formed
nuclei (w). The figure shows the same cell plate as the vertical plate in Fig. 15, but at
a slightly different plane and at a higher magnification, x 6000.

206 U. Wyss, H. Lehtnann and R. Jank-Ladtmg
The cells killed by X. index feeding show similarities to the degenerated cells that
result as a hypersensitive response to Meloidogyne incognita infection in resistant
tomato roots (Paulson & Webster, 1972), especially with respect to the rather rapid
increase in electron-density of the affected cytoplasm. In addition the stimulus that
causes the disorganization of the parasitized cells does not spread to adjacent cells.
The trigger, however, which initiates the mitotic and cytokinetic aberrations obviously
passes into neighbouring cells. This implies a symplastic movement of the trigger,
i.e. via plasmodesmata, which in turn implies a relatively low molecular weight. The
expansion of the neighbouring cells is later facilitated by the necrotic, easily crushable,
cells that surround them.
Little is yet known about the chemical nature of the trigger that induces modified
cells in specific plant-nematode interactions. In X. index the trigger can only be
released into perforated cells via the parasite's odontostyle, having been produced in
secretory gland cells that open into the food canal. In a recent study (Robertson &
Wyss, 1979) it was shown that X. index possesses in its basal oesophageal bulb a
large and very active gland cell whose duct system was seen to deplete after the last
perforation thrust of the stylet and during ingestion pauses. There are several
indications that only secretions from this cell will be injected into perforated plant
cells. Microanalytical studies on biochemical events at the site of the host-parasite
interaction: F. carica-X. index are in progress (Poehling, Wyss & Neuhoff, 1979)
and it is hoped that they will finally provide an answer.
This study, financed by the Deutsche Forschungsgemeinschaft, was made in the Arbeitsgemeinschaft
fur Elektronenmikroskopie der Tierarztlichen Hochschule Hannover. The
authors thank Ulrike Ahrendt for technical assistance and Dr M. G. K. Jones, Department of
Biochemistry, University of Cambridge, England, for helpful comments.
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(Received 21 May 1979)