Meloidogyne		Contents		Rev 05/05/2006
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 Home Page

Classification:

Tylenchida
       Tylenchina
        Tylenchoidea
          Heteroderidae
           Meloidogyninae

Meloidogyne (Goeldi, 1892)

Synonyms:

• Caconema (Cobb, 1924)
• Hypsoperine (Sledge and Golden, 1964)
• Hypsoperine (Spartonema) (Siddiqi, 1986)

History:

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

• 1855- Reverend Miles Joseph Berkeley (clergyman) noted galls on cucumbers in greenhouse in England - first official report. Must have been seen and recognized symptoms before that, however, therefore official means that he wrote about it so that the information could be retrieved.
• 1871- Schmidt described Heterodera schachtii, sugarbeet cyst nematode.
• 1872- Greeff described Anguillula radicicola - galls on cereals and grasses - actually Ditylenchus.
• 1879 - Cornu -  described a root-knot nematode as Anguillula marioni.
• 1884 - Muller decided root-knot nematode was the same as Greeff's root-galling nematode and that both should be Heterodera - Heterodera radicicola.
• 1887 - Goeldi - Brazil - described a root knot on coffee - Meloidogyne exigua.
• 1932 - Goodey - decided that use of H. radicicola was incorrect according to International Rules of Zoological Nomenclature as original H. radicicola was not a root-knot nematode.  He renamed it Heterodera marioni.
• 1949 - Chitwood removed them from Heterodera on the basis that they differed from cyst nematodes. Since the oldest name for the genus was Goeldi's Meloidogyne, that name had precedence. Chitwood described five species based on perineal patterns.

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

Note that the current 75+ spp. probably include some that were lumped in the original 1 species and in Chitwood's 5 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.             Dorsal overlap of esophageal glands. 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:

• Identify species and biotypes of root-knot nematodes within each of 6 geographical regions.
• Determine resistance/susceptibility of food crops in each region.
• Identify sources of resistant germplasm.
• Evaluate crop response in each region.
• Study variability within each species, including host reaction, morphology, cytogenetics, etc.
• Evaluate environmental factors influencing distribution in each area.
• Develop effective integrated crop protection systems for control of root-knot nematodes in each region.

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

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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 pests in California, except M. chitwoodi which is 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.

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 and syncytia (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.  However, syncytia undergo repeated S-phase endoreduplication without mitosis or nuclear division. 

The eukaryotic cell cycle has four stages. Nuclear DNA is replicated during synthesis phase (S-phase) and the nucleus divides (mitosis) in the M-phase. The interval between the completion of mitosis and the beginning of DNA synthesis is called the G1-phase (G = gap), and the interval between the end of DNA synthesis and the beginning of mitosis is the G2 phase. In normal cell division, the cell divides (cytokinesis) after the mitosis phase. In the root-knot nematode 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 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.

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 applied to 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.

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Life Cycle:

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

Orion discovery of cellulases in matrix - hole bored to surface by developing egg-mass.

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.

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Damage:

See mechanistic details in Feeding section.

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Management:

Host Plant Resistance

Number of vegetable cultivars with resistance to common species (Fassuliotis, 1976).

These numbers are now higher, but the proportions are similar.

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References:

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.

Wyss, U.  (Nematologica 38:98-111).

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Copyright © 1999 by Howard Ferris.
Revised: May 05, 2006 .