Parthenogenetic root‐knot nematodes ( Meloidogyne spp.); how can these biotrophic endoparasites have such an enormous host range?

Abstract

Many nematodes feed briefly and ectoparasitically on root hairs or epidermal cells. However, others invade the roots and some are sedentary endoparasites that feed for all their life at one site. These sedentary species, which include cyst (Globodera, Heterodera) and root-knot (Meloidogyne) nematodes, have a highly specialized, biotrophic interaction with their hosts in which their juveniles invade plant roots and settle to feed on one, or a small group of modified, living plant cells. These sedentary species cannot be cultured away from their hosts, and their development is dependent on the cells at their feeding sites remaining alive. Ectoparasitic species generally have wide host ranges and there appears to be little specific resistance against them. In contrast, race-specific resistance is often available against sedentary endoparasitic species, and gene for gene interactions have been demonstrated (Janssen et al., 1991; see also Trudgill, 1991). The sedentary endoparasitic species of cyst nematode mostly reproduce sexually (amphimictically) and are hostspecific, as is reflected by their common names e.g. potato cyst nematodes (Globodera pallida and G. rostochiensis) which are restricted to species within the Solanaceae (Stone, 1983), cereal cyst nematode (Heterodera avenae) restricted to the Gramineae etc. Similarly, most species of root-knot nematode are amphimictic and are host-specific e.g. Meloidogyne pinus whose host range is restricted to Pinus spp. (Jepson, 1987). However, a small group of tropical, mitotically parthenogenetic species (typified by Meloidogyne incognita and M. javanica), which are the subject of this letter, have enormous host ranges that include most families of flowering plants (Goodey et al., 1965; Jepson, 1987). In addition, these species also appear to be remarkably homozygous (Fargette et al., 1996). This letter seeks to address the question of how such a wide host range might be achieved when most biotrophic species of plant pathogens tend to be host-specific. Whilst this generalization covers a considerable diversity, the enormous host range (involving many thousands of plant species) of the these parthenogenetic root-knot nematodes is quite exceptional for a biotrophic species. The relevance to the wide host range of the parthenogenetic root-knot nematodes (P-RKN) of their apparent genetic homozygosity is considered in comparison to the heterogeneity found in host-specific species of cyst nematodes. As a narrow host range could be imposed on a biotrophic pathogen by its inability when in non-hosts either to avoid their defences, or to induce the appropriate susceptible reaction, these two aspects are particularly assessed with a view to understanding how P-RKN species might overcome the limitations either mechanism might impose. As a background it is useful to note that, compared with aerial pathogens, soil nematodes are relatively immobile and hence amphimictic species will tend to inbreed and that nematode populations increase, mix and spread slowly and hence are relatively isolated. Consequently, the processes involved in nematode epidemiology are often less dynamic, and the opportunities for rapid gene flow, and the contribution of genetic drift, are much less than have been suggested for airborne pathogens (Thompson & Burdon, 1992). Plant Pathology (1997) 46, 26–32 Accepted 22 August 1996. BIOLOGICAL COMPARISONS BETWEEN CYST AND PARTHENOGENETIC ROOTKNOT NEMATODES (P-RKN) There are marked similarities, and some important differences in the interactions of cyst and of root-knot nematodes with their hosts. The patterns of root invasion differ. Juveniles of cyst nematodes, such as the potato cyst nematodes (PCN), invade growing roots intracellularly, causing considerable cell death and the generation of PR proteins within a few hours (Bowles et al., 1991). Juvenile P-RKN invade roots intercellularly and consequently often cause no obvious direct damage. The juveniles of both groups become sedentary at their feeding sites close to, or within the stele. Here they induce changes in the cells around their heads to increase their nutritional value. Those fed upon by cyst nematodes enlarge, their dividing walls partially break down and they combine to form a multinucleate, metabolically active ‘syncytium'. Cells fed upon by root-knot nematode juveniles enlarge and their nuclei repeatedly divide to form multinucleate ‘giant cells'. The nuclei within syncytia and giant cells become polyploid (Endo, 1987), further increasing the metabolic capacity of the feeding site. Both syncytia and giant cells take on features of transfer cells (Endo, 1987) and provide the sedentary nematode with a constant supply of nutrients. These nutrients are extracted via a ‘feeding tube', a spiral structure secreted from the tip of the nematode stylet into the cytoplasm of the syncytium or giant cell. The feeding tube is thought to protect the feeding site by acting as a molecular sieve whereby only low molecular weight compounds can be withdrawn (Bockenhoff & Grundler, 1994). The sex of juveniles of both groups is not predetermined; those with syncytia or giant cells whose size is restricted by competition, a resistant reaction, or the confines of being in a lateral root, become males; those with larger syncytia or giant cells become females (Ross & Trudgill, 1969; Trudgill et al., 1970; Trudgill, 1972; Mugniery & Fayet, 1981). This adaptation presumably has value by preventing the further increase of large, damaging populations, thereby preventing the host from being killed. Host specificity in cyst nematodes is reinforced by certain adaptive processes by which, prior to root invasion, the juveniles in the eggs or soil distinguish the roots of hosts from non-hosts. With many cyst nematode species this ‘recognition' involves specific ‘hatching factors', produced by host plants, which induce the dormant nematode eggs to hatch. Between host crops the majority of the juveniles remain dormant, enabling infestations to persist for many years. In contrast, the majority of P-RKN eggs hatch immediately they are fully embryonated and, in the absence of a host, they persist much less well than do cyst nematodes. INDUCTION OF SYNCYTIA AND GIANT CELLS Juvenile cyst and root-knot nematodes inject secretions from their oesophageal gland cells into the cells at their feeding sites (Hussey, 1987; Wyss, 1987). The role of these secretions in the induction of syncytia or giant cells respectively is the subject of much current research, but the introduction of genetic information from the nematode into the plant, as happens with some bacterial interactions, is not thought to be involved. Rather, the secretions from the feeding juveniles appear to trigger the susceptible response by locally altering the expression of host genes. Studies on plants transformed by the addition of the promoter-less, ‘GUSreporter' gene (promoter tagging) have shown that in both syncytia and giant cells the regulation, and hence expression of a considerable number of plant genes (often the same, but sometimes different genes) is modified, probably as part of a cascade of interacting events. Expression of some genes is greatly increased whereas that of others is suppressed (Goddijn et al., 1993; Sijmons,1993). The primary triggers initiating, and processes controlling these cascades are still unknown, but it is hypothesized that they must involve interactions between the products of nematode genes and specific host genes/products leading to a susceptible (compatible) response (Trudgill, 1991). SPECIFICITY OF THE SUSCEPTIBLE RESPONSE It is unknown how many, what kinds of, and what changes in plant gene expression are involved in syncytium or giant cell induction. However, as the P-RKN have wide host ranges it seems clear that the plant genes whose expression is directly modified by the nematode, and which initiate giant cell formation (hereafter termed ‘susceptibility' genes), must be highly conserved. Variations in host status could still, however, be due to allelic variation which would affect the ‘goodness' of fit. Because of the profound changes induced it Meloidogyne spp. and wide host ranges 27