Movement through plant tissues

The tissue migrations, feeding sites and reproduction of animal and plant parasites have been studied in some cases for more than 100 years. The last two decades have seen increased interest in the evolution of parasitic behaviours, particularly in relation to host finding, site finding and feeding-site establishment. A recent conceptual advance has been to explain differential migrations in terms of a small number of fixed action patterns elicited by different stimuli in different nematode species or at different times during development (Sukhdeo, 1997). Examples include the characteristic sequences of activities exhibited by plant-parasitic nem-atodes during hatching and root invasion, the resumption of spontaneous activity by S. carpocapsae and Ancylostoma caninum when vibrated or by Trichonema sp. and Agamermis catedecaudata when illuminated, nictating by S. carpocapsae and A. caninum in response to CO2, conversion from tortuous to straight locomotion by males of Panagrellus redivivus on agar when exposed to sex attractant (Samoiloff et al., 1973) and accelerated movement by animal parasites in response to bile (Sukhdeo, 1997).

VonMende (1997) reviewed movement of juvenile stages of sedentary root parasites through roots, emphasizing work with the model plant, Arabidopsis thaliana. Wyss (1997) examined literature for feeding-site establishment in roots across a continuum of parasitic specialization among 14 illustrated types of feeding patterns or nematode-induced feeding sites. Scheres et al. (1997) have discussed nematode-elicited cellular and tissue modifications in plants in relation to contemporary genetic analysis of cell determination in roots.

Based on interpretations of tissue migrations by animal parasites, it seems plausible that a small group of fixed action patterns evoked in plant-parasitic nematodes at key points during plant tissue development and invasion may guide nematodes through tissue and regulate their involvement in feeding-site establishment. In 11 species of Tylenchida, contact with roots led to a predictable sequence of actions referred to as local exploration (lip rubbing and stylet probing), followed by a cell-wall cutting cycle (body immobilization and rhythmic stylet thrusting to cut a slit in the cell against which the lips are appressed) and then cell penetration (Doncaster and Seymour, 1973). Once inside the root and a cell to be fed on was encountered, a different sequence occurred. Feeding by Aphelenchus avenae (Fisher, 1975) in liquid culture showed that membrane penetration is not necessary for feeding, but several activities are: cessation of body movement, followed by bending of the head, stylet thrusting and protracted stylet exsertion during pumping of the oesophageal metacorpus.

A given species typically exhibits the same migration and feeding pattern in a wide range of plant hosts, and a small set of stimuli and responses probably guide these activities. It has been suggested that CO2 mediates the acropetal migration of Meloidogyne spp. intercellularly through the root cortex following root entry in cotton (McClure and Robertson, 1973). After reaching the meristematic tissue just behind the growing tip, these nematodes turn basipetally to rest and feed on one or several cells, which are induced to develop into enlarged hypermetabolic nurse cells, usually called giant cells. The same migration pattern is seen in many hosts (Wyss et al., 1992; VonMende, 1997). As one of many possible contrasting examples, root entry by the infective, vermiform females of the reniform nematode (R. reniformis) is largely intracellular, rather than intercellular through the cortex, and perpendicular, rather than parallel to the root axis. In a wide range of hosts, the infective female usually comes to rest and feeds permanently on an endodermal cell, eliciting the formation of a nurse syncytium comprised of several contiguous pericycle cells, without the nematode ever perforating the pericycle. This same feeding-site establishment behaviour, like that of root-knot nematodes, is exhibited in dozens of distantly related plant hosts (Robinson et al., 1997).

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