Plant Molecular Biology 43: 747–761, 2000.
Dirk Inzé (Ed.), The Plant Cell Cycle.
© 2000 Kluwer Academic Publishers. Printed in the Netherlands.
Cell cycle activation by plant parasitic nematodes
, Janice de Almeida Engler
, John Verhees
, Sander van der Krol
and Godelieve Gheysen
Laboratory of Nematology, Wageningen University, P.O. Box 8123, 6701 ES Wageningen, Netherlands (
Laboratory of Genetics, University of Gent / VIB, K.L. Ledeganckstraat 35, 9000 Gent,
Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen,
Department of Plant production, Faculty of Agricultural and Applied Biological Sciences,
University of Gent, Coupure links 653, 9000 Gent, Belgium
Key words: auxin, cell cycle, feeding cell, plant-nematode interaction, plant parasitic nematodes
Sedentary nematodes are important pests of crop plants. They are biotrophic parasites that can induce the
(re)differentiation of either differentiated or undifferentiated plant cells into specialized feeding cells. This
(re)differentiation includes the reactivation of the cell cycle in speciﬁc plant cells ﬁnally resulting in a transfer
cell-like feeding site. For growth and development the nematodes fully depend on these cells. The mechanisms un-
derlying the ability of these nematodes to manipulate a plant for its own beneﬁt are unknown.Nematode secretions
are thought to play a key role both in plant penetration and feeding cell induction. Research on plant-nematode
interactionsis hampered by the minute size of cyst and root knot nematodes, their obligatorybiotrophic nature and
their relatively long life cycle. Recently, insights into cell cycle control in Arabidopsis thaliana in combination
with reporter gene technologies showed the differential activation of cell cycle gene promoters upon infection
with cyst or root knot nematodes. In this review, we integrate the current views of plant cell fate manipulation
by these sedentary nematodes and made an inventory of possible links between cell cycle activation and local,
nematode-induced changes in auxin levels.
Virtually without exception, sediment and soil ecosys-
tems are inhabited by tremendous numbers of nema-
todes. The molecular diversity among the members
of the phylum Nematoda is much larger than their
morphological diversity: most of them look alike. In
general, nematodes are relatively small (<2 mm),
transparent and vermiform. Co-evolution between ne-
matodes and bacteria, fungi or plants resulted in bac-
terial feeders such as the well-known Caenorhabditis
elegans,in fungivorousnematodespeciesand in oblig-
atory plant parasites. Though representing a small
minority within this huge phylum, the plant parasitic
nematodes receive ample attention, mainly because
they are a major yield-limiting factor in crops such as
potato, beet, soybean and tomato.
When obligatory plant parasitic nematodes are
considered, a number of different feeding strategies
can be discriminated. One could be indicated as the
hit-and-run strategy; this approach is employed, for
example, by Trichodorus species. This nematode uses
a stylet to penetrate the cell wall of the rhizodermis
and to ingest the cell contents. Subsequently another
cell, not necessarily from the same plant, is visited.
A more lasting strategy is employed by endoparasites.
These nematodesenterthe plant andinduce the forma-
tion of a feeding site. Once a feeding site is induced,
the nematodefully dependson it for growth anddevel-
opment. If the feeding site becomes non-functional,
the nematode by which the feeding structure was in-
duced will die. This durable strategy is successful:
endoparasitesinvadea wide range of plant species and