Meloidogyne  

 

Contents

 

Rev 11/19/2019

Root-knot nematodes Classification Hosts
Morphology and Anatomy Life Cycle

Return to Meloidogyne Menu

Economic Importance Damage
Distribution Management
Return to Heteroderidae Menu Feeding  References
    Go to Nemaplex Main Menu   Go to Dictionary of Terminology

Classification:

Tylenchida
       Tylenchina
        Tylenchoidea
          Heteroderidae
           Meloidogyninae

Meloidogyne Goeldi, 1892

Synonyms:

History:

Descriptions and taxonomic history important - name changes and taxonomic uncertainty negated much of the physiological and ecological early work.

The name Meloidogyne is derived from two Greek words meaning "apple-shaped" and "female".

Now host range test (J.N. Sasser), chromosome counts (Triantaphyllou), juvenile head structure (Eisenback), protein (gel electrophoresis patterns -Esbenshade) and DNA patterns are used to separate species. Many of these approaches came out of International Meloidogyne Project.

North Carolina (Sasser) Differential Hosts Test for four common species of Meloidogyne

Meloidogyne species and races Cotton (Deltapine 61) Tobacco (NC 95) Pepper (California Wonder) Watermelon (Charleston Gray) Peanut (Florunner) Tomato (Rutgers)
M. incognita            
Race 1 - - + + - +
Race 2 - + + + - +
Race 3 + - + + - +
Race 4 + + + + - +
M. arenaria            
Race 1 - + + + + +
Race 2 - + - + - +
M. javanica + + - + - +
M. hapla - + + - + +

Note that the current 75+ spp. probably include some that were lumped in the original 1 species and in Chitwood's 4 spp., hence compounding concern that some nematologists have with taxonomic revisions; e.g. McKenry and Lamberti - a dilemma.

 

Slide show on Meloidogyne spp.

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Morphology and Anatomy:

Female has 2 ovaries, prodelphic; adults swollen; eggs deposited in matrix secreted by six rectal glands, eggs not retained in female body.

Female body does not form cyst. Cuticular striations in posterior of female form a fingerprint-like perineal pattern.

 

 

 

 

 

 

Overlap of esophageal glands over intestine

Male has 1 testis, but sometimes two. Male does not have caudal alae; has characteristic half-twist of body. [Is it always same direction?]

Sedentary obligate parasites of roots, usually forming galls.

[Note predominance of parthenogenisis - is this associated with endoparasitism, in contrast to semi-endoparasites - is amphimixis more common in species with small galls; e.g., M. hapla)?; how about M. chitwoodi?]

International Meloidogyne Project focused on this single genus - J.N. Sasser, US-AID, from about 1975 to 1985.

Objectives of the project:

There are about 75 described species in the genus; 68 species listed by Luc, Maggenti, et al., 1988..

 

Body size range for the species of this genus in the database - Click:
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Distribution:

Genus has world-wide distribution, and is the most widely recognized plant-parasitic nematode because it causes characteristic galling symptoms.

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Economic Importance:

 All species are C-rated pest in California Nematode Pest Rating System, except M. naasi and M. chitwoodi which are B-rated.

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Feeding:

Host-Parasite Interactions: Nematode Responses

a. Attraction to Roots

J2 are attracted to the root tip in the zone of elongation. They are also attracted to areas of lateral root emergence.

They are attracted by CO2, and apparently by small molecules that are dialysable - perhaps amino acids.  Recent studies suggest that the attraction may not be to CO2 per se but to lower pH resulting from carbonic acid formed from the CO2 in solution.  When CO2 is injected on a surface of agar that is buffered to prevent pH shift, the CO2 appears less attractive (V.M. Williamson, pers comm).

b. Root Penetration and Migration to Feeding Site

Detailed studies have been conducted in the model plant system, Arabidopsis, by Wyss (Nematologica 38:98-111).

J2 penetrates zone of elongation by mechanical (stylet thrusts) and probably chemical (cellulase and pectinase) means. It moves between, rather than through, cortical cells towards root apex, turns at the meristem, and migrates back to the vascular cylinder in the zone of cell differentiation. (Heterodera J2 moves through cells directly to vascular tissue).

c. Feeding Site Initiation

The J2 penetrates cells with the stylet and initiates the giant cell from potential vascular tissue. Subventral glands become prominent 2 days after penetrating root. The subventral glands are most visible and active in J2;  they shrink and atrophy as nematode becomes an adult - so what is their role? There is strong evidence that they produce enzymes responsible for giant cell initiation even though their structure suggests that their secretions would pass back into intestine.

As nematode grows and molts, the dorsal esophageal gland (DEG) becomes more prominent and secretions are thought to stimulate multinucleate giant cell. Secretions are packed in secretory granules, 800nm diameter. The DEG canal is a cytoplasmic extension of the single-cell DEG and opens into the lumen of the esophagus just behind the stylet. The secretions of the DEG are injected into the cell. If the nematode is removed, the giant cell atrophies.

There are ongoing attempts at chemical analysis of secretory granules; also the ability of the nematode to initiate giant cells following laser surgery of the glands has been investigated. Monoclonal antibodies have been used to identify sources of nematode secretions.

Host-Parasite Interactions: Plant Responses

a. Development of the "Giant Cell"

  1. Nuclear proliferation occurs; two nuclei are observed within 24 hours of stylet penetration and more than eight within the next 24 hours. The nuclei become polyploid. Consequently, each cell has many copies of the genome which provides a large quantity of DNA to make proteins in these highly active nutrient sink cells.

Note the issue of definition -  a syncytium is formed by the breakdown of neighboring cell walls to form a multinucleate cell. However, the Meloidogyne spp. feeding sites are giant cells induced by synchronous mitosis without cell wall deposition (Endo in Vistas on Nematology) - following initial findings of karyokinesis without cytokinesis by Huang and Maggenti.  Karyokinesis without cytokinesis, also known as acytokinetic mitosis,  might be regarded as a specific form of endoreduplication, the process of an interupted and repeated cell cycle that results in increase in the number of chromosomes and consequently the amount of DNA in a cell.

More than 50 genes are upregulated to some extent in the development of giant cells (Meloidogyne) and syncytia (Heterodera/Globodera) (Gheysen and Fenoll, 2002). Both types of feeding cells have the genome amplified as a result of multiple shortened cell cycles; but the processes differ. Giant-cells go through repeated (acytokinetic) mitosis.  Syncytia undergo repeated S-phase endoreduplication without mitosis or nuclear division. 

The eukaryotic cell cycle has four stages.:
1. Nuclear DNA is replicated during synthesis phase (S-phase).
2. DNA synthesis is followed by an interval called the G2 phase (G=gap).
3.  Mitosis occurs, the nucleus divides (M-phase).
4.  The interval between the completion of mitosis and the beginning of DNA synthesis is the G1-phase,

 In normal cell division, the cell divides (cytokinesis) after the mitosis phase.

In the root-knot nematode (Meloidogyne) feeding site there is repeated nuclear division (S and M phases of the cell cycle) but no cell division; this is called acytokinetic mitosis or karyokinesis without cytokinesis.

In the cyst nematode (Heterodera, Globodera) feeding site, the S phase of the cell cycle is activated but not the M phase.   Instead, the cells repeatedly go through the S-phase (endoreduplication) and probably through parts of the  G1 and G2 phases, but bypass mitosis.

The Cell Cycle:  modified from Gheysen and Fenell, 2002.
  1. Cell differentiation is altered.
  2. The cell cycle is altered.
  3. Cell growth - hypertrophy - the cell enlargement results in surrounding cell compression.
  4. Cell wall synthesis - transfer cell characteristics. Giant cell walls thickened, protrusions result in increased surface for nutrient flow - a transfer cell. McClure showed that plants exposed to C14O2 - after 5 days, small amounts in uninfected areas, some in giant cell, most in eggs.
  5. In the giant cell there is an organelle-free zone around the stylet aperture. A feeding tube forms in the cell from stylet secretions.

Since nematodes in the Heteroderidae become sedentary from the late second stage onwards (except for the metamorphosis to males), the feeding site in the plant must be maintained in a condition favorable for perhaps five or six weeks to allow the nematode to fulfill its reproductive potential.  Besides stimulation of the cell cycle events, pathogen-triggered immunity (PTI) responses, including activation of the salicylic acid pathway, must be suppressed. The salicylic acid pathway leads to production of active oxygen molecules and hypersensitive cell death.  In the Meloidogyninae, a possible candidate for effector-triggered suppression of PTI is chorismate mutase, produced in the nematode esophageal glands.  In PTI responses, chorismate is converted to salicylic acid to iniate the defense events.  Chorismate mutase from the nematode reduces chorismate, and thus salicylic acid (Smant and Jones, 2011).

b. Hyperplasia

Increase in tissue size varies with both plant and nematode species - M. hapla and M. incognita cause different sized galls on tomato. Mundo and Baldwin showed that, in the Heteroderinae, syncytium formation and number varies with nematode species and genus in the same plant (note they were not working with Meloidogyninae).

Plant growth regulators occur at higher levels in galled tissue. Both auxins (promoters of cell growth) and cytokinins (promoters of cell division) have been implicated - roots of susceptible tomato cultivars contain higher levels of cytokinin than resistant roots. Cytokinins are also reported from eggs, juveniles and adults; however, this may not be a source, but a result of feeding. When cytokinins are applied to nematode-resistant plant roots, resistance may be partially or completely reversed; e.g., Nemaguard rootstocks in peach.

Symptoms:

Yellowing; mid-day wilting; symptoms of water and nutrient stress; sometimes death, especially if interacting with other organisms; gall formation (note convenience of bioassay - ease of study but cautionary implications in screening for resistance); root branching; J2 and eggs in soil.

Galls on grape roots.

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Hosts:

As a genus, they are reported as parasites of over 3000 host plants, and individual species often have a wide host range. Jensen et al. (1977) listed some 874 crop species as hosts of the 7 or 8 species commonly occurring in the western U.S.

Extreme differences in host range occur within the genus.   Meloidogyne incognita is extremely polyphagous, with a host range of up to 3,000 plant species, while M. megatyla and M. pini are restricted to Pinus spp. (Castagnone-Sereno, 2002; Jepson, 1987).

For an extensive host range list for this genus, click
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Life Cycle:

Root-knot nematodes feed as endoparasites and they depend on the induction of a permanent feeding site to complete their life cycle.

Second-stage juveniles (J2) penetrate the roots, migrate through the intercellular space to enter the vascular cylinder and induce the formation of feeding sites.

Upon feeding-site development, the J2 become sedentary, followed by molts to third- (J3) and fourth-stage juveniles (J4).

Under favourable conditions and sufficient nutrients, J4 molt to become females and commence  produciong eggs which are deposited in a gelatinous matrix, developing to the egg-laying stage. By this time, these egg-laying females have adopted a typical globose shape and begin to lay eggs into a gelatinous matrix attached to the posterior end of the female (Escobar et al., 2015). The plant response to RKN infection usually involves the formation of galls or knots in the root system of susceptible plants. The parasitic interaction between nema- ∗ Present address: Rijk Zwaan Ib�rica, 04120 La Ca�ada, Almer�a, Spain. ∗∗ Corresponding author, e-mail: soledad.verdejo@juntadeandalucia.es todes and plants is defined by the plant competence to support nematode reproduction (host suitability) and ability of the nematode to reproduce in a specific host plant (reproductive fitness) (Taylor & Sasser, 1978). The reproductive fitness of a pathogen is a major component of pathogenicity and an important driver for disease development (Shaner et al., 1992). Three possible basic interactions may occur between nematodes and plants: i) neutral (immune), with no infection; ii) compatible (suitable host), with nematode reproduction; and iii) incompatible (unsuitable host), with reduced nematode reproduction (resistance response) (Barker, 1993). Several types of plant resistance may interfere with nematode development at different stages during its life cycle. Pre-infection resistance would prevent nematodes from entering the roots (Proite et al., 2008). Post-infection resistance would prevent nematodes reaching the egg-laying stage and reproducing within the roots. The mechanisms of this resis-

For Ecophysiological Parameters for this genus, click 
 

 

Life stages of Meloidogyne spp.  Infective J2 on left, young female on right.  Most of the growth occurs during the second stage.

Mature Meloidogyne female (on head of pin for size perspective).

Meloidogyne male still coiled within the J4 cuticle.

Third and 4th stage within 2nd stage cuticle, passed fairly rapidly, no stylet, do not feed. Usually 4-500 eggs per egg-mass, Tyler reported a high count of 2,800.

Mass invasion of second-stage juveniles in a grape root.  Only a few will establish a feeding site at this location.
Mature female at feeding site with egg mass on root surface.
Enlarged metacorpus of adult female.

Photo by Hussey


Life cycle diagram by J.D. Eisenback, International Meloidogyne Project


Life cycle diagram by Charles Papp, CDFA

Orion discovery of cellulases in egg-mass matrix - suggests that a hole is enzymatically digested to the root surface by the developing egg-mass.  Nematodes are thought to have acquired cellulases via horizontal gene transfer from bacteria.

Sexual differentiation starts in late 2nd stage, heart shaped gonad. Sex reversal can occur under adverse conditions resulting in males with two testes (Triantaphyllou et al.).

Nematode exhibits a high reproductive rate.

Melakerberhan and Ferris - increase in body weight 250 fold, from 0.11µg for J2 to  300µg for total weight of female and egg mass. Total energy demand = 1 calorie, but consider repair costs, increased root metabolism, leakage, control of partitioning - effects which outweigh that of feeding.

Characteristic Heteroderinae Meloidogyninae
Feeding site Multinucleate syncytium Multinucleate giant cell
Host range Narrow Wide
Reproductive strategies Sexual Mainly parthenogenic
Eggs Mainly retained in female body Deposited in egg mass
Female body Becomes hardened cyst Does not form cyst
Hatching factors From host root exudates Favorable environmental conds.
Cell cycle Endoreduplication Acytokinetic mitosis andendoreduplication
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Damage:

See mechanistic details in Feeding section.

Meloidogyne spp. damage in grape vineyards in California

 

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Management:

Host Plant Resistance

Three  interactions may occur between nematodes and plants: i) neutral (immune), with no infection occurring; ii) compatible (suitable host), with nematode reproduction; and iii) incompatible (unsuitable host), with reduced nematode reproduction (resistance). Resistance may be expressed as pre-infection resistance in which nematodes are prevented from entering, or post-infection resistance in which nematodes do not reach the egg-laying stage and do not reproduce (or reproduction is delayed or reduced) (Talavera-Rubia et al., 2018). 

Mechanisms include:

  1.  hypersensitive reaction response, common in plants with dominant resistance genes such as the Mi gene in tomato

  2.  failure of the nematode to reach the egg-laying stage  or reduction in the rate of egg production or the number of eggs produced

The Mi gene is a single dominant gene that confers resistance to M. incognita, M. javanica, and M. arenaria.  It is located near the centromere of chromosome 6.  Bailey (1940) provided an early report of the wild tomato species Solanum peruvianum as a source of resistance to root-knot nematodes. Due to reproductive incompatibilities between the Solanum lycopersicum and S. peruvianum, embryos resulting from crosses do not reach maturity.  Consequently, techniques for embryo rescue techniques were developed in which immature embryos are dissected from seed and cultured axenically.  The technique appears to have been first used to transfer the Mi gene from wild tomato into commercial cultivars by Smith (1944) in crossing Solanum lycopersicum var. Michigan State with S. peruvianum PI128.657.

Dr. Charles Rick and colleagues at UC Davis discovered that an isozyme, acid phosphatase, is coded by the gene Aps-1 which is located on chromosome 6 of tomato close to, and tightly linked with, Mi (Rick and Fobes, 1974).  The isozyme provides a tool for tomato breeders to determine whether they have successfully transferred Mi into commercial varieties and has facilitated the development of processing varieties with root-knot nematode resistance.

The Mi gene has been cloned and sequenced in the laboratory of Dr. Valerie Williamson at UC Davis.  Using Agrobacterium as a carrier, the resistance gene has been transferred to a susceptible tomato cultivar, which expresses the resistance.  Plants grown from seeds of the transgenic plant are also resistant to M. incognita.  However, after the second generation of plant offspring, the expression of resistance is progressively reduced in seed batches from some plants but not from others.  In both cases,  the gene is still present and is still coding for RNA (Goggin et al, 2004).

The resistance conferred by the Mi gene breaks down at soil temperatures >28C.

With repeated use of the single source of resistance in California tomato production, aggressive strains of the nematode are being selected (Kaloshian et al. 1996).

In the early 1990s, farm advisors and entomologist Dr. Harry Lange noticed that tomatoes with the Mi gene appeared to be also resistant to the potato aphid, Macrosiphum euphorbiae.  Initial determination was that a gene tightly linked to Mi and designated Meu1 was responsible for the potato aphid resistance.  Current research indicates, however, that the two genes are identical and that Mi confers resistance to both root-knot nematodes and the potato aphid.  A more recent development is the discovery that the Mi gene also confers resistance against the white fly Bemisia tabaci (Nombela et al., 2003). The gene is located near the centromere of tomato chromosome #6.

As with the resistance to M. incognita, the resistance to the potato aphid is also progressively reduced after the the second generation of plant progeny (Goggin et al, 2004).

 

Number of vegetable cultivars with resistance to common species (Fassuliotis, 1976). (The numbers of cultivars in each category are now higher, but the proportions are similar).

  M. arenaria M. hapla M. incognita M. javanica
Beans 0 0 12 0
Pepper 7 0 3 6
Soybeans 0 0 4 0
Cowpeas 4 1 30 4
Sweetpotato 7 1 17 3
Tomato 2 1 43 7
Totals 20 3 109 20
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References:

Bailey, D.M. 1940. The seedling test method for root-knot nematode resistance. Proc. Amer. Soc Hort. Sci. 38:573-575.

Castagnone-Sereno, P. 2002.  Genetic variability of nematodes: a threat to the durability of plant resistance genes?  Euphytica 124:193-199.

Endo, B. 1976. In Vistas on Nematology

Gheyson, G. and C. Fenoll.  2002. Gene expression in nematode feeding sites.  Ann. Rev. Phytopathol. 40: 191-219.

Goggin FL, Shah G, Williamson VM, Ullman DE. 2004.  Instability of Mi-mediated nematode resistance in transgenic tomato plants. Molecular Breeding 13:357-364.

Kaloshian, I., V.M. Williamson, G. Miyao, D.A. Lawn and B.B. Westerdahl. 1996.  "Resistance-breaking" nematodes identified in California tomatoes.  California Agriculture 50(6):18-19.

Nombela, G., V. M. Williamson, and M. Muniz. 2003. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant Microbe Int. 16:645-649.

Rick, C.M. and Fobes, J.F. 1974. Association of an allozyme with nematode resistance. Rep. Tomato Genet. Coop 24:25.

Smant, G., Jones, J. 2011.  Suppression of plant defences by nematodes.  Chapter 13, pp 273-286. In Jones, J., Gheysen, G., Fenoll, C. (eds).  Genomics and Molecular Genetics of Plant-Nematode Interactions.  Springer, NY.

Smith, P.G. 1944. Embryo culture of a tomato species hybrid. Proc. Amer. Soc Hort. Sci. 44:413-416.

Talavera-Rubia, M., A. P�rez De Luque, M. L�pez-G�mez and Ss. Verdejo-Lucas. 2018. Differential feeding site development and reproductive fitness of Meloidogyne incognita and M. javanica on zucchini, a source of resistance to M. incognita. Nematology 20:187-199.

Wyss, U.  (Nematologica 38:98-111).

 

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Copyright © 1999 by Howard Ferris.
Revised: November 19, 2019 .