Meloidogyne enterolobii (Pacara earpod tree root-knot nematode)
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IdentityTop of page
Preferred Scientific Name
- Meloidogyne enterolobii Yang & Eisenback, 1983
Preferred Common Name
- Pacara earpod tree root-knot nematode
Other Scientific Names
- Meloidogyne mayaguensis Rammah & Hirschmann, 1988
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Nematoda
- Family: Meloidogynidae
- Genus: Meloidogyne
- Species: Meloidogyne enterolobii
Notes on Taxonomy and NomenclatureTop of page
Meloidogyne enterolobii was described from roots of pacara earpod tree (Enterolobium contortisiliquum) on Hainan Island in China (Yang and Eisenback, 1983). On the basis of female perineal patterns, it was preliminary identified as Meloidogyne incognita, and further analysis indicated some resemblance with the latter species; however, from a morphological point of view, the population was very different from M. incognita and any other described root-knot nematode species (Yang and Eisenback, 1983). A few years later, a new species of root-knot nematode was described from specimens recovered from galled roots of aubergines (Solanum melongena) in Puerto Rico, and named Meloidogyne mayaguensis (Rammah and Hirschmann, 1988). The authors indicated that 'M. mayaguensis superficially resembles M. enterolobii but differs distinctly from it in (some) morphological features' (Rammah and Hirschmann, 1988). In addition, the esterase phenotype of M. mayaguensis (VS1-S1) was identical to that of M. enterolobii (Esbenshade and Triantaphyllou, 1985; Rammah and Hirschmann, 1988). In 2012, Karssen et al. (2012) compared holo- and paratypes of both species and confirmed that M. mayaguensis should be considered as a junior synonym of M. enterolobii.
DescriptionTop of page
The original description was made from a population that seriously damaged pacara earpod trees (Enterolobium contortisiliqum) on Hainan Island in China (Yang and Eisenback, 1983), following a preliminary (false) identification from perineal patterns of females that indicated the presence of Meloidogyne incognita. The morphological characters from female, male and second-stage juvenile stages, as published in the original description, are detailed below.
Body white, pear-shaped to globular, variable in size, with prominent neck variable in size, without posterior protuberance. Head region not distinctly set off from neck. Labial disc and medial lips fuse to form head cap. Hexaradiate cephalic framework distinct but weak; vestibule and vestibule extension prominent. Cephalids and hemizonids not observed. Position of excretory pore variable, often near metacorpus. Cuticular body annulations become progressively finer posteriorly. Stylet slender; conical portion slightly curved dorsally, tapering toward tip; cylindrical shaft, posterior end often enlarged. Knobs set off from shaft, distinct from each other, and divided longitudinally by groove so that each knob appears as two. Dorsal oesophageal gland orifice (DGO) 4-6 µm from base of stylet knobs; orifice branches into three channels; dorsal gland ampula large. Subventral gland orifices branched, located immediately posterior to enlarged lumen lining of metacorpus; subventral gland ampula small but distinct. Oesophageal gland comprised of one large uninucleate dorsal oesophageal gland lobe; two small, nucleated subventral oesophageal gland lobes usually posterior to dorsal gland lobe but variable in position, shape and size; all three lobes overlap intestine ventrally. Two small, rounded, singly nucleated oesophago-intestinal cells located between metacorpus and intestine. Perineal pattern usually oval, with coarse and smooth striae; dorsal arch moderately high to high, often rounded, nearly square in some specimens. Lateral lines not distinct. Perivulval region generally free of striae; striae may occur on lateral sides of vulva. Striae on ventral area of pattern generally finer and smoother. Tail tip visible; phasmidial ducts large.
Body translucent white, vermiform, tapering at both ends. Tail end more rounded than anterior end, twisting through 90° in heat-killed specimens. In lateral view, head cap high and rounded, head region only slightly set off from body. Hexaradiate cephalic framework moderately developed; vestibule and extension distinct. In SEM, stoma slit-like, prestoma hexagonal, surrounded by pit-like openings of six inner labial sensilla. Labial disc and medial lips fuse, forming elongate head cap and labial disc slightly elevated above medial lips. Four cephalic sensilla marked on medial lips by shallow cuticular depressions. Amphid openings slit-like; lateral lips absent; head region not annulated; body annules distinct. Lateral field begins near level of stylet knobs as two incisures; two additional incisures start near level of metacorpus; lateral field areolated, encircles tail. Stylet robust; cone straight, pointed; opening located several micrometres from tip. Shaft cylindrical; knobs large, rounded, distinctly set off from shaft; in some specimens each knob is divided longitudinally by groove so that each knob appears as two but not as pronounced as in female. Distance of GDO to stylet base long, orifice branched into three channels, ampulla poorly defined. Procorpus distinct; metacorpus elongate, oval with enlarged cuticular lumen lining; oesophago-intestinal junction indistinct, at leveI of nerve ring. Gland lobe variable in length, with two nuclei. Excretory pore far from anterior end, terminal duct long. Hemizonid 2-4 annules anterior to excretory pore. One or two testes, usually outstretched. Spicules arcuate, with rounded base, single tip. Gubernaculum short and simple. Tail short and rounded. Phasmids small, pore-like, at level of cloaca.
Second–Stage Juvenile (J2)
Body translucent white, vermiform, rather long, tapering at both ends with very long, narrow tail. Anterior end truncate; head region only slightly set off from body. Vestibule and extension more developed than remainder of hexaradiate cephalic framework. In SEM, stoma slit-like, located in oval prestoma, surrounded by six pore-like openings of inner labial sensilla. Medial lips and labial disc dumbbell-shaped in face view. Labial disc rounded, raised slightly above medial lips. Lateral lips large and triangular, lower than labial disc and medial lips. Posterior edge of one or both lateral lip may fuse with tile head region in some specimens. Elongate amphidial apertures located between labial disc and lateral lips. Head region not annulated; body annules distinct but fine. Lateral field beginning near level of procorpus as two lines; near metacorpus third line begins and shortly splits making four lines, running entire length of body before gradually decreasing to two lines which end near hyaline tail terminus, irregularly areolated. In LM, stylet delicate; cone straight, narrow, sharply pointed; shaft becomes slightly wider posteriorly; knobs large, rounded, separate from each other, set off from shaft. Distance from base of stylet to dorsal oesophageal gland orifice long; orifice branched into three channels; ampulla indistinct. Procorpus faintly outlined; metacorpus oval with enlarged lumen lining; isthmus not clearly defined oesophago-intestinal junction difficult to observe. Gland lobe variable in length, with three equal-sized nuclei; overlaps intestine ventrally. Excretory pore distinct; hemizonid 1-2 annules anterior to excretory pore, 3-5 annules long; cuticle slightly raised over hemizonid. Tail very thin; annulations increase in size, become more irregular posteriorly. Hyaline tail terminus clearly defined; tail tip broad, bluntly rounded. Rectum dilated. A few fat droplets may occur in hyaline tail terminus. Phasmids small, difficult to observe, located posterior to anus.
DistributionTop of page
M. enterolobii is largely distributed in regions with typical tropical climatic conditions, including Asia, Africa, South and Central America and the Caribbean. It has also been reported from areas of North America exhibiting a warmer climate, e.g., Florida and North Carolina (Kaur et al., 2006; Ye et al., 2013). Because of its thermal requirements, M. enterolobii will probably not survive in colder regions. However, it might be able to establish in Mediterranean climates or in greenhouses (e.g., the nematode was detected on vegetables in greenhouses in Switzerland; Kiewnick et al., 2008). M. enterolobii has been intercepted on several occasions in a few European countries in plant materials imported from tropical areas.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
Risk of IntroductionTop of page
As a root-knot nematode species, M. enterolobii can easily be transmitted with soil and plant material. Infested soil and growing media, plants for planting, bulbs and tubers from countries where M. enterolobii occurs are the most probable pathways of introduction into different regions. Soil attached to machinery, tools, footwear or plant products is also another possible pathway. The recent interception of this pest in several countries in Europe and the Mediterranean region (Germany, The Netherlands, UK) illustrates that it has the potential to enter different regions. In addition, M. enterolobii could survive under glasshouse conditions across regions with a sub-Mediterranean or a continental climate. Once root-knot nematodes have been introduced, it is generally difficult to control or eradicate them. Only in the EPPO region has this nematode been listed as a quarantine pest (EPPO A2 list No.361).
Hosts/Species AffectedTop of page
M. enterolobii is considered to be a highly polyphagous species, with a host range similar to that of Meloidogyne incognita (Yang and Eisenback, 1983). The most frequently recorded hosts include many vegetables, e.g., tomato, pepper and watermelon (Yang and Eisenback, 1983; Rammah and Hirschmann, 1988) but also guava (Gomes et al., 2011), ornamental plants (Brito et al., 2010) and weeds (Rich et al., 2009). Of particular concern is the ability of M. enterolobii to develop on crop genotypes carrying resistance to the major Meloidogyne species, among which are resistant cotton, sweet potato, tomatoes (Mi-1 gene), potato (Mh gene), soyabean (Mir1 gene), bell pepper (N gene), sweet pepper (Tabasco gene) and cowpea (Rkgene) (Yang and Eisenback, 1983; Fargette and Braaksma, 1990; Berthou et al., 2003; Brito et al., 2007; Cetintas et al., 2008). Very few crop species have been recorded as non-hosts for M. enterolobii, including grapefruit, sour orange, garlic and peanut (Rodriguez et al., 2003; Brito et al., 2004).
Biology and EcologyTop of page
M. enterolobii is a sedentary endoparasite. Its life-cycle is very similar to other root-knot nematodes, and can be summarized briefly as follows. The worms hatch in the soil as second-stage, infective juveniles (J2s) and migrate towards the root of their host plant, which they invade in the zone of elongation. There, they migrate intercellularly, first to the root apex and then to the vascular cylinder, where permanent feeding sites (i.e., giant cells) are established. Now sedentary, J2s further undergo three successive moults to develop into adults. The saccate (pyriform) females remain sedentary, producing large egg masses that are extruded in a gelatinous matrix out of the root, while males (if any) migrate out of the plant tissues (Abad et al., 2003). The life-cycle of M. enterolobii takes 4-5 weeks under favourable conditions and females produce around 400-600 eggs.
The reproduction of M. enterolobii is by mitotic parthenogenesis and the somatic chromosome number is 2n = 44-46. Most oocytes advance to metaphase and telophase soon after they have entered the uterus and show no extended prophase stage (Yang and Eisenback, 1983).
Impact SummaryTop of page
Economic ImpactTop of page
M. enterolobii is considered as a very damaging pest because of its wide host range, high reproduction rate and the induction of large galls (Castagnone-Sereno, 2012). Although few detailed studies are available, M. enterolobii is referred to as a highly aggressive species (i.e., a very successful parasitic species with high infestation rate on the roots of host plants) and induces more severe root galling than other root-knot nematode species. In a microplot experiment, tomato yield losses of up to 65% have been observed (Cetintas et al., 2007). In two greenhouses in Switzerland, yield losses of up to 50% and severe stunting of tomato rootstocks and cucumber were observed (Kiewnick et al., 2008). In heavily infested areas, cultivation may become unviable, as exemplified for guava in Brazil (Carneiro et al., 2007).
DiagnosisTop of page
A species-specific esterase phenotype (VS1-S1) with two major bands has been described for M. enterolobii, while occasionally, one of these bands could resolve into two minor bands (Esbenshade and Triantaphyllou, 1985; Carneiro et al., 2000). However, the limitation of this technique is that J2s cannot be reliably diagnosed, which hinders its use in e.g., routine examination of soil samples.
In recent years, a number of molecular protocols have been developed that proved to be efficient in differentiating M. enterolobii from the most common root-knot nematode species, based on the presence/absence and/or size of the amplicons in PCR reactions. Conversely to isoenzyme electrophoresis, the interest of such PCR methods is that they can be applied to all developmental stages of nematodes. The molecular targets chosen in the various protocols available mainly include mitochondrial DNA (Block et al., 2002; Brito et al., 2004; Xu et al., 2004), ribosomal DNA (Adam et al., 2007), satellite DNA (Randig et al., 2009) and an anonymous SCAR marker (Tigano et al., 2010).
Detection and InspectionTop of page
Similar to other root-knot nematode species, M. enterolobii induces typical galls on the roots of infested plants. In case of severe attacks, extremely large and numerous galls can be found (Cetintas et al., 2007). Above-ground symptoms include stunted growth, wilting, leaf yellowing and deformation of plant organs. Overall, crop yield is reduced both qualitatively and quantitatively. In addition, M. enterolobii infestation may favour attacks of roots by secondary plant pathogens.
The presence of M. enterolobii in infested soil and plant material can de determined after extraction of the nematodes using conventional methods and microscopic examination. However, as morphological characters often overlap in root-knot nematode species, misidentification of species using morphology as the only criteria may occur. Alternatively, the use of biochemical and molecular tools, such as esterase profiling and DNA-based markers, has proven to be a good complement to provide reliable diagnostics in most cases.
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
As is the case for other root-knot nematodes, general management strategies against M. enterolobii rely on a combination of prevention and control practices to achieve effective reduction of the nematode population density below a damage threshold enabling sustainable crop production. Reviews describing such general practices are available in recent literature (e.g., Coyne et al., 2009; Nyczepir and Thomas, 2009).
Basically, taking into account the banning of most chemical nematicides, growing resistant crops or non-host plants currently represents the best method for reducing M. enterolobii populations. However, the list of non-host plants for this species is very limited. In addition, resistance genes active against the major tropical root-knot nematode species (i.e., M. incognita, M. javanica and M. arenaria) do not control M. enterolobii, for example, in the case the Mi-1, N and Rk genes from tomato, pepper and cowpea, respectively. Therefore, some efforts have been devoted in recent years to the identification of new sources of resistance to M. enterolobii, with some success in perennial crops. A decade ago, a screening experiment using high and durable inoculum pressure indicated that Ma genes in Myrobolan plum, known to control the main tropical root-knot nematode species, also control resistance to M. enterolobii (Rubio-Cabetas et al., 1999). In peach, commercial rootstocks carrying the RMia resistance gene were shown resistant to the nematode in greenhouse evaluation tests (Nyczepir et al., 2008; Daniel Esmenjaud, pers. comm.). In guava trees, whose cultivation may suffer high damage in cases of heavy infestations, resistance has recently been identified in Psidium spp. accessions (de Almeida et al., 2009; Freitas et al., 2014). Clearly, search for new sources of resistance to M. enterolobii, especially in vegetables and annual crops, and their introgression into cultivars of agronomic interest, currently represent a major challenge to plant breeders worldwide.
Another alternative to chemical nematicides is based on the use of biocontrol agents, and several organisms have been investigated for their antagonistic effects against M. enterolobii. However, although some show promise, the results of all these studies require validation in various field conditions before a biological agent active against M. enterolobii may be commercially released.
ReferencesTop of page
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ContributorsTop of page
30/10/14 Original text by:
Philippe Castagnone-Sereno, INRA, Institut Sophia Agrobiotech, UMR INRA1355/UNS/CNRS7254, 400 route des Chappes, BP167 – 06903 Sophia Antipolis Cedex, France.
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