H C

Fig. 3.2 The evolution of feeding among Tylenchomorpha super posed on a ribosomal DNA-based phylogenetic backbone. (Based on Bert et al. 2008; Holterman et al. 2009)

3.3.2 Evolution of Plant-Parasitism in Tylenchomorpha

The development of plant-parasitism in the Tylenchomorpha has traditionally been seen as a gradual evolution from fungal feeding to facultative parasitism of root hairs and epidermal cells into more complex forms of plant-parasitism, culminating in the development of sedentary endoparasitism (Luc et al. 1987). To investigate this hypothesis, ancestral feeding types were reconstructed among Tylenchomorpha using three different methods: unordered parsimony, parsimony using a stepmatrix, and likelihood (Bert et al. 2008; Holterman et al. 2009). Here we present only a schematic overview of these results (Fig. 3.2).

The feeding type analysis supported the classical hypothesis of the gradual evolution of simple forms of plant-parasitism, such as root hair and epidermal feeding and ectoparasitism towards more complex forms of endoparasitism. However, the ancestral feeding state of the Tylenchomorpha (without Aphelenchoididae) is still ambiguous; depending on the reconstruction method this is fungal-feeding, lower plant/root-hair feeding or bacteriovore feeding. Conclusions on this hypothesis await a better resolution in the basal part of the Tylenchomorpha tree and additional information on the feeding behavior of the basal Tylenchomorpha such as the Tylenchidae and Anguinidae. Within the tylenchid nematodes, migratory ectoparasitic feeding is ancestral for all major clades of nematodes that exclusively parasitize higher plants (Fig. 3.2). Migratory endoparasitism has evolved independently several times within Anguinidae and four times, always from migratory ectoparasitic ancestors, in the polyphyletic Pratylenchidae. Sedentary endoparasitism has also evolved three times independently; Nacobbus (false root-knot nematodes) and the cyst-forming nematodes most likely evolved from migratory ectoparasitic nematodes, while root-knot nematodes appear to have evolved from migratory endoparasitic nematodes. The number of independent developments is higher than expected mainly due to the polyphyly of the Pratylenchidae. Although the development of plant-parasitism is usually gradual, endoparasitism seems to have developed directly from several simple forms of plant-parasitism including ectoparasites (giving rise to Heteroderinae, Pratylenchidae, Pratylenchoides and Tylenchulus) and epidermal and root hair feeders (from which the Anguinidae evolved).

Although the parasitic biology of certain plant-parasitic Tylenchomorpha is now relatively well documented, we should achieve a broader understanding of the evolution of the mode and direction of plant-parasitism from intermediate groups, including economically less important plant-parasites. Within Clade 12 the family Aphelenchidae (fungivores) appears in a sister position to all "tylenchs" (Holterman et al. 2006; Bert et al. 2008). However, it should be noted that in a more recent, maximum likelihood analysis this positioning could not be robustly confirmed (van Megen et al. 2009). For the plant-parasitic Tylenchomorpha families positioned at the base of clade 12 such as the Tylenchidae, the Psilenchidae and the Belonolaimi-dae (the 'economically less important plant-parasites'), the number of (ribosomal)

DNA sequences available is very limited. It is expected that molecular characterisation of specimens from these families and improved insight in their feeding habits will give us more insight in the transition from fungivorous lifestyles, via facultative plant-parasitism towards obligatory plant-parasites.

3.4 Tylenchomorpha—Top End Plant-Parasites

3.4.1 Root-Knot Nematodes—Towards the Origin(s) of This Highly Successful Genus

3.4.1.1 Introduction

Root-knot nematodes—members of the genus Meloidogyne—can be said without too much exaggeration to represent the ultimate success story among plant-parasitic nematodes. The more distal members of this genus have host ranges encompassing more than a thousand plant species, including numerous major crops, and are spread all over the temperate and (sub)tropical regions of the world. On the basis of SSU rDNA sequences Tandingan de Ley et al. (2002) defined three distal clades within the genus Meloidogyne. Clade I comprises a number of species often referred to as the tropical root-knot nematodes (e.g. M. incognita, M. javanica and M. arenaria), the most well known representative of Clade II is M. hapla, while Clade III harbors a number of species with EPPO A2 quarantine status such as M. chitwoodi and M. fallax (EPPO=European and Mediterranean Plant Protection Organisation) (Fig. 3.3). Analysis of a larger molecular data set and more Meloidogyne species resulted in a confirmation of these distal clades. Ribosomal DNA sequence data point at Meloidogyne artiellia—a polyphagous root-knot nematode typically inducing very small galls (host plant range includes both mono and dicotyledons)—as being sister to the distal Meloidogyne clades I, II and III (III being basal to Clades I and II) (Holterman et al. 2009).

One of the elements that could explain the success of this genus is the ability of these endoparasites to migrate between plant cells. Cell wall-degrading enzymes and expansins are likely to be widespread throughout Meloidogyne, although they have so far only been characterized for some of the more derived members of this genus. These enzymes and proteins make it possible for these plant-parasites to move towards the most nutritional part of the plant root, namely the vascular cylinder (stele). Migrating between cells, rather than through cells as is the case for cyst nematodes, may help the pre-parasitic second-stage juveniles to outpace and/ or avoid the host plant defense response. The question why lesion (Pratylenchus spp.) and cyst nematodes (Globodera spp. and Heterodera spp.) do not migrate intercellularly while infective life stages are producing and secreting various cell wall degrading enzymes and proteins remains to be answered.

Fig. 3.3 Schematic overview of the phylogeny of the Meloidogynidae derived from SSU rDNA sequence data. (Based on Holterman et al. 2009)

M. incognita M. javanica M. arenaria M. morocciens M. floridensis M. paranaensis M. arabicida M. ethiopica M. enterolobii

M. hapla M. microtyla M. ardenensis M. maritima M. spartinae M. duytsi

M. chitwoodi M. fallax M. minor M. naasi M. graminicola M. oryzae M. exigua

M. artiellia

Meloidogyne sp. M. ichinohei

3.4.1.2 Modes of Reproduction Among Root-Knot Nematodes

Another fascinating aspect of root-knot nematode biology is the wide range of modes of reproduction present with the group. Meloidogyne incognita multiplies by mitotic parthenogenesis. Mothers that produce genetically identical daughters could be considered as a dead end road in evolutionary terms—such a genetic constitution would make it impossible for an individual to cope with changing environmental conditions. Nevertheless, in terms of distribution and host plant range this is probably the most successful member of the genus Meloidogyne. M. incognita is one of the members of Clade I (as defined above). It is notable that Clade I is not homogenous in its mode of replication. Although mitotic parthenogenesis dominates this clade, one of its members (M. floridensis) multiplies by meiotic parthenogenesis. The same holds true for Clades II and III; although meiotic parthenogenesis is most frequently found there are a number of exceptions. Most remarkable is the case of Meloidogyne hapla for which two races are defined. Race A reproduces by facultative meiotic parthenogenesis, whereas the polyploid Race B multiplies by mitotic parthenogenesis. It would be useful to examine more basal root-knot nematode species when seeking further insight into the extreme diversity in modes of reproduction of root-knot nematodes.

According to McCarter (2008), most root-knot species are "sexually reproducing diploids, a status thought to reflect the root-knot nematode ancestral state". A careful examination of M. artiellia, which is sister to the distal Meloidogyne Clades I—III, suggests this could be correct; the frequent occurrence of males suggests this species could multiply sexually. However, based on the analysis of rDNA sequence data at least four Meloidogyne species are placed in more basal positions, viz. M. ulmi, M. mali, an undescribed Meloidogyne species found on Sansevieria, and M. ichinohei (Holterman et al. 2009).

Meloidogyne ichinohei is an unusual root-knot nematode species both in its morphology and in its extreme host specificity. Unlike most RKN females, adult females of M. ichinohei show a prominent posterior protuberance, a laterally located neck and a perineal pattern showing remarkably faint and broken striae (Araki 1992). Previously the first two characters were considered to be rather atypical, and they had been the characteristics defining the genus Hypsoperine, a genus synonymized with Meloidogyne by Jepson (1987). M. ichinohei males are very rare according to the original description by Araki (1992). This observation has been confirmed by the Dutch National Plant Protection Organisation (NPPO); not a single male was found in M. ichinohei population C2312 (G. Karssen, unpublished data).

3.4.1.3 On the Former Genus Hypsoperine

Araki remarked that M. ichinohei would have been a typical member of the genus Hypsoperine if it still existed (Araki 1992). Sledge and Golden (1964) suggested that the genus Hypsoperine actually occupied a position in between Heterodera and Meloidogyne (though showing closer resemblance to the root-knot nematodes). This information prompted us to check a number of other Hypsoperine-like root-knot nematodes: (1) Hypsoperine acronea (now Meloidogyne acronea); (2) H. graminis (M. graminis); (3) H. mersa (M. mersa); (4) H. ottersoni (M. ottersoni); (5) H. propora (M. propora); (6) H. spartinae (M. spartinae) and (7) H. megriensis (M. megriensis). As very little is published about the members of this genus, information about host range and mode of reproduction (if known) is summarized here.

1. Meloidogyne acronea is a root-knot nematode-like parasite found on roots of sorghum (Sorghum vulgare) by Coetzee in 1956. The author reported that this particular isolate could also parasitize and multiply on beans and tomatoes. In the original description morphological characteristics of both males and females are given. M. acronea seems to have a very restricted geographical distribution as it has been reported from southern Africa only.

2. Meloidogyne graminis was found in 1964 by Sledge and Golden as a parasite on St. Augustine grass (Stenotaphrum secundatum). When few males were present, M. graminis reproduces by meiotic parthenogenesis. However, in the presence of males reproduction was by amphimixis (Triantaphyllou 1973). Based on cyto-logical data, Triantaphyllou (1973) suggested a close phylogenetic relationship of M. graminis, M. ottersoni, M. graminicola (Clade III) and M. naasi (Clade III).

3. Meloidogyne mersa is an unusual root-knot nematode found in a marine habitat (mangrove swamps in Brunei) parasitizing roots of the mangrove apple (Sonner-atia alba). The original paper describes both males (100 paratypes) and females (50 paratypes) and males are not rare (Siddiqi and Booth 1991). The morphology of M. mersa resembles that of M. spartinae, another root-knot nematode species living in marine or brackish habitats.

4. Thorne (1969) described Meloidogyne ottersoni as a parasite of canary grass (Phalaris arundinacea). As for M. graminis, M. ottersoni was reproduced by meiotic parthenogenesis when males are absent but in the presence of males reproduction was by amphimixis (Triantaphyllou 1973). Based on cytological data, Triantaphyllou suggested for a close phylogenetic relationship of M. otter-soni, M. graminis, M. graminicola (Clade III) and M. naasi (Clade III).

5. Meloidogyne propora was first described by Spaull (1977) as a parasite on the roots of Cyperus obtusiflorus and Solanum nigrum from an atoll in the Indian Ocean (Aldabra). Males were reported to be common in soil around infested roots and near ovigerous females.

6. Meloidogyne spartinae is a root root-knot nematode producing galls on cordgrass (Spartina alterniflora) which is found in intertidal wetlands, especially estuarine salt marshes. On the basis of SSU rDNA sequences Plantard et al. (2007) clearly showed this species to be related to M. maritima, and as such residing in Meloidogyne Clade II.

7. Meloidogyne megriensis—rather incomplete description published in Russian by Poghossian (1971)—was collected from roots of Mentha longifolia. Only known from the type locality, an orchard in Megri, and a nearby village named Vagravar, Armenia Karssen and van Hoenselaar 1998.

This overview, based on various data, indicates that members of the former genus Hypsoperine are scattered all over the Meloidogyne phylogenetic tree, and—other than the observation that their morphology is different from what is considered to be typical for root-knot nematodes—they have little in common.

Another Meloidogyne species sharing a number of morphological characteristics with M. ichinohei (but never classified as member of the genus Hypsoperine) is Meloidogyne kralli. M. kralli was first found in 1968 by Dr. E. Krall on the roots of sedge (Carex acuta) (Jepson 1983). Adult females share a number of characteristics with M. ichinohei; they have a distinct neck (contrary to M. ichinohei, the neck was not set off) and the vulva was positioned on a posterior protuberance. Although males have been described for M. kralli (Jepson 1983), they are seldom found under natural conditions (Karssen 2002). Meloidogyne kralli seems to have a relatively small host range as it is found only on four Carex species, namely C. acuta, C. vesi-caria, C. riparia and C. pseudocyperus, and on Scirpus sylvaticus. Under laboratory conditions M. kralli populations were reported to reproduce well on barley (Jepson 1983). It is noted that both M. ichinohei and M. kralli exclusively parasitize a small number of monocotyledons. However, SSU rDNA sequence analysis revealed that

M. ichinohei and M. kralli are rather distinct, with M. kralli robustly positioned in Meloidogyne Clade III close to M. oryzae (Helder and Karssen, unpublished results).

Based on the information discussed above, M. acronea would be worthwhile investigating in more detail, as it resembles M. ichinohei. Cytological and scattered molecular data place most of the former members of the genus Hypsoperine in the distal Meloidogyne Clades II or III, except for M. acronea and M. propora. It is concluded that molecular data from particularly these two species could possibly contribute to a better understanding of the origin of the genus Meloidogyne. However, both species seem to have a restricted distribution (southern Africa, and an atoll in the Indian Ocean) and this complicates the collection of DNA from these highly interesting root-knot nematode species. Currently, M. ichinohei—together with a so far non-described Meloidogyne species from Kenya found on Sansevieria (Holter-man et al. 2009)—seem to reside genuinely at the very base of the Meloidogyne tree of life. Both species have a very limited host range, and for both species males are very rare. In our eyes, this justifies a hypothesis stating that (at least facultative) asexual reproduction is the root-knot nematode ancestral state.

3.4.2 Lesion Nematodes—A Stenomorphic Genus Closely Related to Root-Knot Nematodes

Lesion nematodes—members of the genus Pratylenchus—can be recognized easily. Lesion nematodes are relatively small (usually around 500 |im), have a short and stout stylet (11-22 |im) with strong basal knobs, a low lip region with a well-developed sclerotized framework, and glands forming a rather short lobe which ventrally overlaps the intestine (see e.g. Castillo and Vovlas 2007). However, recognizing individual species is difficult as the number of diagnostic characters at this particular taxonomic level is small. The identification of lesion nematodes is further complicated by intra-specific variation in some of these characters. Pratylenchus identification to species level is usually done on the basis of the morphology of adult females. They have more informative characters than males, and—at least equally important—for a number of species males are extremely rare or even non-existent. Despite these difficulties (or possibly as a consequence of them), this genus comprises approximately 70 nominal species (Castillo and Vovlas 2007).

Using the labial region as a distinguishing character, Corbett and Clark (1983) distinguished three groups of Pratylenchus species. Group I includes (among others) P. brachyurus, P. coffeae, P. crenatus, P. loofi, and P. zeae; group 2 includes P. neglectus and P. thornei; and P. penetrans, P. pratensis, P. scribneri and P. vul-nus belong to group 3. Combined analysis of D2-D3 of 28S (= LSU rDNA) and partial 18S (= SSU rDNA) alignments revealed a subdivision of the genus Pratylenchus into six groups (Subbotin et al. 2008). Members of group 1 sensu Corbett and Clarke (1983) are scattered over major clades a, b and d. Group 2 (Corbett and Clarke 1983) corresponds to group c (Subbotin et al. 2008), and Group 3 (Corbett and Clarke 1983) members all reside in group a according to Subbotin et al.

(2008) except for P. scribneri which resides in clade b. No representatives of the genus Meloidogyne were included in this analysis. Holterman et al. (2009) presented a phylogenetic tree based on a full length SSU rDNA data set including nine Pratylenchus species. However, poor backbone support in this particular part of the tree did not allow for the identification of a Pratylenchus (or at least Pratylenchidae) candidate that could be a likely living representative close to the common ancestor of all root-knot nematodes.

3.4.3 Phylogenetic Relationship Between the Genera Meloidogyne and Pratylenchus

On the basis of shared morphological characteristics of the labial region and pha-ryngeal structures Ryss (1988) and Geraert (1997) proposed a common ancestry between the genera Pratylenchus and Meloidogyne. Analysis of SSU and LSU rDNA sequences from a considerable range of lesion and root-knot nematodes supports a close phylogenetic relationship between the two genera. Subbotin et al. (2006) found "evidence for a Pratylenchus, Hirschmanniella and Meloidogyne clade" (based on D2-D3 sequence data). Two years later Bert et al. (2008) concluded "... root-knot nematodes are most closely related to Pratylenchus spp. and appear to have evolved from migratory endoparasitic nematodes" (based on SSU rDNA data). In 2009 Holterman et al. concluded "our data suggest that root-knot nema-todes have evolved from an ancestral member of the genus Pratylenchus, but it remains unclear which species is closest to this branching point" (based on more extensive SSU rDNA data). All in all the following can be concluded:

1. Ribosomal DNA sequences suggest that the genus Pratylenchus is paraphyletic as all Meloidogyne species are nested in it.

2. If this (1.) is correct, the ultimate consequence would be the abolishment of the genus Pratylenchus (Meloidogyne has priority following the rules of the International Commission on Zoological Nomenclature). This could be undesirable for numerous practical reasons, but in scientific research and especially in our thinking about root-knot nematode evolution this could be useful.

3. The discussion about ancient (a)sexuality as the ancestral state of root-knot nematodes should be replaced by a discussion about the ancestral mode of reproduction of a clade encompassing (at least) all members of the genera Pratylenchus and Meloidogyne.

3.5 Concluding Remarks

The steep increase in the amount of molecular data over the last decade has allowed for the establishment of more and more robust and versatile phylogenetic frameworks for the phylum Nematoda (Blaxter et al. 1998; Holterman et al. 2006, Van

Megen et al. 2009). It is noted that current frameworks are based on a single cistron (SSU and/or LSU ribosomal DNA sequences), and marine taxa (including numerous plant-parasites) are strongly underrepresented. Current data suggest at least three independent lineages of plant-parasites. This number will probably increase over time; analysis of a 5' region of LSU rDNA pointed at multiple plant-parasite lineages among the Dorylaimida (Holterman et al. 2008b).

The infraorder Tylenchomorpha (equivalent to Clade 12 (Fig. 3.1) with the addition of the family Aphelenchoididae) comprises the largest group of plant-parasitic nematodes. Analysis of rDNA sequences resulted in a good resolution in the more distal parts of this clade only. Basal Tylenchomorpha—mostly plant-parasites with virtually no economic importance—are currently underrepresented, and this might co-explain why the relationships within this group are poorly resolved (Subbotin et al. 2006; Bert et al. 2008; Holterman et al. 2009). Additional sequencing of basal Tylenchomorpha probably will improve our understanding of the evolution of the more advanced (and successful) members of this infraorder. The relationships between and within distal taxa in Clade 12 including cyst, lesion and root-knot nematodes are far better resolved. Within this chapter the relatedness of the two latter genera—Pratylenchus and Meloidogyne—was discussed in more detail, and current data suggest that root-knot nematode are in fact nested in (and derived from) the Pratylenchus branch.

At this moment, several, so-called next generation DNA sequencing technologies are becoming widely available. This will make it possible to generate sequence data from hundreds if not thousands of genes from individual nematodes at a reasonable cost price. Given that we still have nematode taxonomists around to ensure the link between classical systematics and multigene phylogenetics, we foresee that within a few years from now the notoriously volatile nematode systematics will be turned into a single, more or less robust and widely accepted framework.

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