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Plant Physiol. Apr 2005; 137(4): 1182–1188.
PMCID: PMC1088311

Nematodes. Sophisticated Parasites of Legumes

From an agronomic perspective, the interactions of phytoparasitic nematodes with leguminous crops can be devastating (Barker, 1998). On a cellular and molecular level, the complexities of the interactions of these microscopic worms with legumes are comparable to those of well-known symbionts (Mathesius, 2003). Because of their agricultural importance, the soybean cyst nematode Heterodera glycines and species of root-knot nematodes (Meloidogyne spp.) that infect soybean (Glycine max) and other legumes have emerged as primary research models to understand the signaling, perception, and response events during plant-nematode interactions (Davis et al., 2004). The recent advances in our understanding of the cellular, physiological, and molecular basis of legume-nematode interactions are merging at the crossroads of plant-microbe interactions and plant developmental biology.

All plant-parasitic nematodes have evolved a hollow, protrusible mouth spear called a stylet that is used to inject secretions into host tissues and pierce plant cell walls to withdraw nutrients (Hussey and Grundler, 1998). Some phytonematode species feed upon and quickly destroy plant cells as migratory parasites, whereas other nematode species become sedentary in later life stages and must modify plant cells to provide a sustained local source of nutrition for parasitic success. Although species within a few nematode genera, such as Ditylenchus and Aphelenchoides, plague the shoot tissues of cultivated legumes such as alfalfa (Medicago sativa), the majority of phytonematode species are parasites of plant roots (Hussey and Grundler, 1998).

The root-knot nematodes and cyst nematodes (Heterodera and Globodera spp.) are sedentary endoparasites of plant roots and the primary nematode pathogens of most crop species worldwide, including many cultivated legumes (Barker, 1998). The major species of Meloidogyne have a wide host range that includes at least 1,700 plant species (Barker, 1998). By contrast, individual species of cyst nematodes are relatively host specific, such as the soybean cyst nematode H. glycines that infects relatively few plant species beyond soybean (Hussey and Grundler, 1998). As members of the same family (Heteroderidae), however, both root-knot and cyst nematodes share similar parasitic habits, most notably the induction of elaborate modifications of selected plant root cells into complex feeding sites (Fig. 1).

Figure 1.
Cross sections of feeding cells induced in plant roots by sedentary endoparasitic nematodes. A, Multinucleate giant cells (GC) induced by the root-knot nematode Meloidogyne incognita, derived from karyokinesis uncoupled from cytokinesis of plant cells ...

MUTUALISM AND PARASITISM

The conspicuous galls (knots) formed on plant roots by species of Meloidogyne draw immediate comparisons to root nodules formed on legumes by rhizobia (Mathesius, 2003; Bird, 2004). Mycorrhizae and cyst nematodes (Hussey and Grundler, 1998; Parniske, 2004) also form complex cellular relationships within plant root tissues, but neither biotroph forms galls on roots. What are the molecular mechanisms and developmental pathways in the plant that ultimately determine the different outcomes of these interactions, and do they share any common features? Is there a fine line between mutualism and parasitism, or are they distinct phenomena? These questions provide a central theme for this treatise as we explore the interaction of nematodes with legumes.

An overview of the parasitic relationship of root-knot and cyst nematodes with their plant hosts allows us to put these interactions into perspective. The infective (preparasitic) stage of root-knot and cyst nematodes is the motile second-stage juvenile (J2) that hatches from the egg in soil and penetrates the root directly behind the tip at the zone of elongation (Hussey and Grundler, 1998). The parasitic J2 of cyst nematodes migrate through root cortical cells (intracellularly) using thrusts of their stylet to breach cell walls, while the J2 of root-knot nematodes migrate between root cortical cells (intercellularly), to reach the root vascular cylinder. The esophageal gland cells of both nematodes actively synthesize and mobilize secretions from the stylet during migration within tissues and subsequent formation of feeding cells (Hussey, 1989). Parasitic J2 of root-knot nematodes induce the formation of three to six multinucleate giant cells (Fig. 1A) from individual root xylem parenchyma cells surrounding the nematode head that serve as the feeding site for the progression of swollen nematode sedentary stages to reproductive adult stages. Giant cells form from repeated nuclear division without cellular division, giving rise to multinucleate, hypertrophied feeding cells up to 100 times the size of normal root vascular parenchyma cells. In many but not all hosts, pericycle and cortical root cells immediately surrounding the giant cells are stimulated to divide (hyperplasia), giving rise to the gall characteristic of root-knot nematode infection. Parasitic J2 of cyst nematodes select a single root vascular parenchyma or pericycle cell to induce an initial syncytial cell. Enzymes of plant origin (Goellner et al., 2001) promote coordinated dissolution of cell walls neighboring the initial syncytial cell and subsequently give rise to a multinucleate feeding site for the cyst nematode called a syncytium (Fig. 1B). The syncytium continues to incorporate up to several hundred cells along the root vasculature as the nematode begins to feed and swells to a rounded, sedentary state through a series of molts to become a reproductive adult.

Although the ontogeny of syncytia and giant cells differ fundamentally, these nematode-induced feeding cells do share many common features similar to natural plant transfer cells (Offler et al., 2003), including multiple lobed nuclei, dense cytoplasm with increased metabolic activity, and thickening and numerous ingrowths of the peripheral cell walls to increase solute transport and structural integrity. Similar modifications of plant cell walls and plasma membranes to accommodate solute transport to either colonizing rhizobia or vesicular arbuscular mycorrhizae are common features of symbioses (Parniske, 2004). Both phytoparasitic nematodes and rhizobia induce the expression of host plant cell wall-modifying enzymes at the infection site, but, interestingly, induction of this endogenous mechanism of plant cell wall modification has not been detected during mycorrhizal infection of roots (Goellner et al., 2001; Gheysen and Fenoll, 2002; Parniske, 2004). The localized hypertrophy and hyperplasia of plant cells induced during infection by rhizobia, Agrobacterium, and even the clubroot root fungus Plasmodiophora produce tissue swellings similar to the galls of root-knot nematodes (Agrios, 1997), but the giant cells induced within galls by Meloidogyne are distinctly multinucleate. Studies may need to distinguish between the formation of essential feeding cells versus associated gall tissues when drawing comparisons to Rhizobium nodules since giant cells can support normal root-knot nematode growth and development in the absence of surrounding galls (Webster, 1969). In total, the giant cells and syncytia formed by root-knot and cyst nematodes, respectively, are unique plant host modifications induced by these parasitic nematodes. The parasitic J2 of both cyst and root-knot nematodes are absolutely dependent on feeding site formation to progress through subsequent parasitic stages, and, conversely, the integrity of the feeding site is dependent on the presence of the nematode. The feeding sites serve as a nutrient sink for the parasitic needs of the nematodes resulting in disease of the host. This interaction is in stark contrast with the mutual benefits derived by both the microbe and plant during mycorrhizal colonization of plant roots or nodulation of legume roots.

NEMATODE PARASITISM GENES

Proteinaceous stylet secretions from nematodes that are synthesized in the esophageal gland cells are considered as primary signaling molecules at the plant-nematode interface because the morphology, contents, and activity of the gland cells change in relation to nematode migration within plant tissues, feeding cell formation, and nematode feeding activity (Hussey, 1989; Davis et al., 2004). The genes encoding these secretions have been termed parasitism genes (Davis et al., 2000), and a number of different research strategies have identified multiple parasitism genes encoding secreted products in several nematode species (for review, see Jasmer et al., 2003; Davis et al., 2004). The first phytonematode parasitism genes identified encoded cellulases (endoglucanases) synthesized in the esophageal gland cells of cyst nematodes (Smant et al., 1998) that were expressed and secreted only during nematode migration within roots (Davis et al., 2004). These were the first endogenous endoglucanase genes cloned from an animal, and phylogenetic analyses (Yan et al., 1998) indicated strong similarity to cellulase genes of soil bacteria, suggesting the potential for ancient horizontal gene transfer as a mechanism of gene acquisition in nematodes (Smant et al., 1998; Davis et al., 2000). A number of nematode parasitism genes encoding other cell wall-modifying proteins, including the first non-plant expansin (Qin et al., 2004), have since been identified that are expressed in the esophageal gland cells during nematode migration in plant tissues (Jasmer et al., 2003).

Beyond cell wall modifications, phytoparasitic nematodes appear to be armed with a suite of stylet secretions (Fig. 2) to modulate many of the features observed in nematode feeding cells (Davis et al., 2004). Genes encoding secreted chorismate mutase (CM) that are most similar to bacterial CM have been isolated from root-knot and soybean cyst nematodes (Doyle and Lambert, 2003). CM is a pivotal enzyme in the shikimic acid pathway that modulates synthesis of Phe and Tyr, having pleiotropic effects on cellular metabolism, auxin synthesis, and as precursors of plant defense compounds. Expression of nematode CM in soybean tissues affected vascular tissue differentiation and was indirectly related to local indole-3-acetic acid concentrations and cellular partitioning of chorismate (Doyle and Lambert, 2003). Another group of candidate secreted nematode parasitism gene products that may also augment host cellular metabolism includes members of the proteasome (Skp-1, RING-H2, and ubiquitin extension protein) with significant similarity to plant genes involved in selective host cell protein degradation (Gao et al., 2003; Tytgat et al., 2004). If secreted into plant cells by nematodes, mimics of the plant proteasome may regulate host cell phenotype at the protein level to promote a compatible plant-nematode interaction.

Figure 2.
A model of potential interactions of secreted products of phytonematode parasitism genes with host plant cells. Nematode esophageal gland cell secretions are released through valves within ampulla for transport out of the stylet (feeding spear) into host ...

Two other intriguing observations have been made among putative parasitism genes isolated from H. glycines. More than 25% of the predicted nematode parasitism proteins encode putative nuclear localization signals (NLS; Gao et al., 2003), some of which contain DNA-binding motifs, suggesting that the secreted nematode products could be targeted to interact directly within the recipient host cell nucleus. Transient expression of some of the H. glycines NLS parasitism proteins as green fluorescent protein/β-glucuronidase fusion proteins in onion (Allium cepa) epidermal cells has localized the nematode gene products within the plant cell nucleus (A. Elling and T.J. Baum, personal communication). The most abundantly expressed candidate parasitism gene in H. glycines (Gao et al., 2003) was first isolated as clone HG-SYV46 (Wang et al., 2001) through secretion signal-peptide selection of an esophageal gland cell cDNA library. Computational analyses predicted that the C-terminal domain of HG-SYV46 is related to members of the CLAVATA3-ESR-like (CLE) family of signaling proteins in Arabidopsis (Arabidopsis thaliana; Olsen and Skriver, 2003) involved in controlling the balance between shoot meristem cell proliferation and differentiation by interacting with the CLAVATA1 (CLV1)/CLAVATA2 (CLV2) receptor complex (Brand et al., 2000). WUSCHEL is a homeodomain transcription factor (Mayer et al., 1998) that acts antagonistically to the CLV pathway to promote stem cell formation and maintenance (Brand et al., 2000). Remarkably, a WUSCHEL phenotype that includes premature termination of the shoot apical meristem and development of flowers lacking the central gynoecium (Laux et al., 1996) is observed when HG-SYV46 is expressed at high levels in wild-type Arabidopsis (Wang et al., 2005), similar to overexpression of CLV3 (Brand et al., 2000). In addition, expression of HG-SYV46 in a clv3 mutant in which the mutant plants have enlarged shoot and floral meristems with extra floral organs in each whorl (Clark et al., 1995) restored the wild-type phenotype (Wang et al., 2005). Although it is unclear if secreted nematode CLEs promote parasitism in roots via similar CLV1-like receptor-mediated cell differentiation as proposed for plant root CLEs (Casamitjana-Martinez et al., 2003), several models have been proposed (Wang et al., 2005). One possibility is that the secreted HG-SYV46 from the nematode is a CLE mimic that functions as one component of a pathway to redirect and maintain the differentiation of root vascular cells into elaborate feeding cells, potentially via a CLV1-like receptor complex. Alternatively, HG-SYV46 may function through competitive inhibition of a similar endogenous root-expressed CLE ligand for a host CLV1-like receptor in the roots to augment normal root vascular cell redifferentiation into feeding cells (Wang et al., 2005). Interestingly, the Lotus japonicus HAR1 gene encodes a Leu-rich repeat (LRR) receptor-like kinase with the highest level of similarity to the Arabidopsis CLAVATA1 gene (Krusell et al., 2002; Nishimura et al., 2002). The har-1 mutant displays a hypernodulating phenotype and was recently reported to be hyperinfected by root-knot nematodes (Lohar and Bird, 2003), implicating the involvement of the CLAVATA pathway in both rhizobia and nematode-plant interactions. In addition to potential nematode-secreted CLE ligand mimics, a NodL ortholog was recently identified among expressed sequence tags of the root-knot nematode (McCarter et al., 2003), and initial evidence suggests that signals from infective juveniles of root-knot nematodes can have similar effects as Nod factor on developing root hairs of the legume model L. japonicus (Weerasinghe et al., 2005). The combined evidence suggests that phytoparasitic nematodes may have evolved an extraordinary ability to modulate cellular processes of their host plants to promote parasitism.

PLANT RESPONSE DURING NEMATODE PARASITISM

The morphology of syncytia and giant cells is similar among plant hosts, including legumes, suggesting that fundamental mechanisms of plant cell development are manipulated during feeding cell ontogeny across diverse plant species. The limited host range of most cyst nematode species contrasts with the observed similarity in syncytial morphology among hosts, suggesting coevolutionary selection for an intrinsic level of specificity in cyst nematode-plant signaling events. Do phytoparasitic nematodes tap, directly or indirectly, into host developmental pathways similar to those recruited by other microbial symbionts of legumes? Evidence above suggests that the CLE/CLV1 developmental pathway may be a common mechanism exploited by both cyst nematodes and rhizobia during infection of roots. Orthologs of the PHAN and KNOX genes involved in transcript regulation and meristem maintenance in tomato (Lycopersicon esculentum), respectively, are expressed in giant cells and developing nodules in roots of the model legume Medicago truncatula (Koltai et al., 2001). Likewise, the early nodulation mitogen ENOD40 and the cell cycle regulator ccs52 active in nodules are also stimulated in giant cells and galls induced in M. truncatula by root-knot nematodes (Koltai et al., 2001; Favery et al., 2002). ENOD40 is involved in both the initiation and stimulation of cortical cell division for nodule formation and may play a similar role in stimulating the proliferation of cells around giant cells for gall formation. In nodules, CCS52 functions as a cell cycle regulator that promotes endoreduplication and cell enlargement in the nondividing submeristematic cell layers of zone II (Cebolla et al., 1999), two major characteristics of nematode-induced giant cells. By contrast, expression of the auxin-regulated cell cycle A2-type cyclin gene (cycA2;2) of M. truncatula, shown to play a role exclusively in the mitotic cycles and not expressed during cell differentiation coupled to endoreduplication, was suppressed in the endoreduplicating, nondividing cells of developing nodules and nematode-induced giant cells (Roudier et al., 2003). Further analysis of 192 nodule-expressed genes of M. truncatula revealed only two additional genes induced in both nodules and galls (Favery et al., 2002), suggesting that the morphological divergence in symbiotic phenotype is reflected at the molecular level.

Like M. truncatula, L. japonicus has potential as a model legume host for root-knot nematodes (Lohar and Bird, 2003), and, most recently, induction of a cytokinin-responsive ARR5 gene promoter::β-glucuronidase transgene has been observed in the early stages of both nodule and giant-cell formation in L. japonicus (Lohar et al., 2004). Although the direct or indirect effects of observed phytohormone accumulation associated with nematode feeding sites is still unclear, perturbation of local concentrations of cytokinin (Lohar et al., 2004) and auxin (Goverse et al., 2000) suppress successful root-knot and cyst nematode infection, respectively. Auxin accumulation around giant cells was suggested to trigger gall formation during root-knot infection of white clover (Trifolium repens; Hutangura et al., 1999) and, as with H. glycines infection of soybean roots (Kennedy et al., 1999), was associated with an increase in isoflavonoid expression. A similar accumulation of auxin and induction of the flavonoid pathway has been observed during the formation of Rhizobium nodules (Mathesius et al., 1998).

RESISTANCE VERSUS SUSCEPTIBILITY

How does a symbiont induce such dramatic modifications in plant cells and get away with it (without invoking host defense)? This is especially true for intimate parasites such as nematodes, where there is sustained irritation with no “return on investment” for the host. As intimated above and by others (Parniske, 2004), active suppression of host defense may be required of the invader to maintain the interaction. Although unclear at present, the potential manipulation of the host proteasome via nematode secretions may be targeted, in part, specifically toward suppression of the host defense response (Davis et al., 2004). Similar manipulation of host defense may occur at the level of synthesis of defense compounds, perhaps via augmentation of subcellular chorismate levels (Doyle and Lambert, 2003).

Conversely, the potential ability of nematodes to mimic signals in natural plant pathways may provide a measure of stealth that does not invoke host defense unless in the presence of an appropriate receptor. Evidence from many plant-microbe systems supports the model that (avirulence) variants of effector molecules from a microbe function as pathogenicity factors when not in the presence of an appropriate resistance gene (van't Slot and Knogge, 2002). Molecular comparisons of near-isogenic lines of the root-knot nematode that vary in virulence on tomato containing the Mi resistance gene have identified a number of secreted gene products that are differentially expressed between the avirulent and virulent strains (Neveu et al., 2003). Genes encoding peptides that contain conserved motifs of other pathogen avirulence products (Bos et al., 2003), including conserved Cys residues for potential three-dimensional architecture, are represented among the candidate parasitism genes of H. glycines (Gao et al., 2003). Most cloned plant resistance genes against nematode pathogens encode proteins containing nucleotide-binding site and LRR domains similar to those against other microbes (Williamson, 1999). Recently, candidate soybean genes at two loci, Rhg1 and Rhg4, which may condition resistance to H. glycines, were cloned (Lightfoot and Meksem, 2002). Both genes encode Xa21-like receptor kinases with an extracellular LRR domain, a transmembrane domain, and a protein kinase domain (Lightfoot and Meksem, 2002). The considerable variability in response to biotypes of H. glycines and the fact that genomic regions surrounding these loci in soybean are rich with nucleotide-binding site-LRR genes and other genes involved in plant-microbe interactions (Ghassemi and Gresshoff, 1998) suggests a mechanism for receptor variability among plant genotypes. It is tempting to consider the potential specificity of variants of effectors, such as a secreted CLE of H. glycines binding to variants of a CLV1-like or a Xa21-like receptor complex in the host either to promote parasitism or activate defense when in the appropriate combination.

THE FUTURE IS NOW

Will genomics play a major role in unraveling the differences and similarities among symbioses (mutualism and parasitism) in legumes? The host specificity observed in global plant gene expression to successful infection by Heterodera schachtii versus nonhost response to H. glycines has demonstrated the utility of Arabidopsis microarrays (Puthoff et al., 2003) to dissect plant-nematode interactions. Several microarray platforms are now available to the legume research community and may be combined with laser capture microdissection of nematode feeding sites (Ramsay et al., 2004) to greatly refine and expand analyses of nematode parasitism of legumes. Information on the organization and structure of legume genomes is keeping pace with expressed sequence discovery, and observed syntenic relationships among legume genomes (Young et al., 2003) should allow extrapolation to species of agronomic importance, such as soybean (until their genome sequences are generated).

Development of robust functional genomic analyses of legume-nematode interactions will be of primary importance in the post-genomics era as potential gene targets are discovered. As described above, the utility of mutants in model plants such as Arabidopsis, and the legumes Medicago and Lotus, is beginning to be realized for this purpose. Natural variation in Medicago and Lotus is also being explored to map resistance to root-knot nematodes and to identify a potential model legume-cyst nematode pathosystem (M. Dhandayham and C. Opperman, personal communication). Development of reverse genetic tools in legumes (Perry et al., 2003) provides great promise to understand the genetic basis of many traits, including molecular interactions with nematodes. Gene knockout technologies that incorporate expression of introduced double-stranded RNA to induce posttranscriptional gene silencing of plant genes or RNA interference of nematode genes offer the potential to specifically inhibit any target gene to assay its function (Tijsterman et al., 2002). The potential to feed double-stranded RNA to a target phytoparasitic nematode gene (Urwin et al., 2002) via a transgenic plant offers not only potential functional data, but also the exciting possibility of creating novel, target-specific resistance to nematodes in legumes and other important crops.

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