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Root-knot nematode

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Root-knot nematode
Larva of root-knot nematode, Meloidogyne incognita, magnified 500×, shown here penetrating a tomato root
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Nematoda
Class: Secernentea
Order: Tylenchida
Family: Heteroderidae
Genus: Meloidogyne
Göldi, 1892
Species

See text

Root-knot nematodes are plant-parasitic nematodes from the genus Meloidogyne. They exist in soil in areas with hot climates or short winters. About 2000 species of plants worldwide are susceptible to infection by root-knot nematodes and they cause approximately 5% of global crop loss.[1] Root-knot nematode larvae infect plant roots, causing the development of root-knot galls that drain the plant's photosynthate and nutrients. Infection of young plants may be lethal, while infection of mature plants causes decreased yield.

Economic impact

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Root-knot nematodes (Meloidogyne spp.) are one of the three most economically damaging genera of plant-parasitic nematodes on horticultural and field crops. Root-knot nematodes are distributed worldwide, and are obligate parasites of the roots of thousands of plant species, including monocotyledonous and dicotyledonous, herbaceous and woody plants. The genus includes more than 90 species,[2] with some species having several races. Four Meloidogyne species (M. javanica, M. arenaria, M. incognita, and M. hapla) are major pests worldwide, with another seven being important on a local basis.[3] Meloidogyne occurs in 23 of 43 crops listed as having plant-parasitic nematodes of major importance, ranging from field crops, through pasture and grasses, to horticultural, ornamental and vegetable crops.[4] If root-knot nematodes become established in deep-rooted, perennial crops, control is difficult and options are limited.[citation needed]

Meloidogyne spp. were first reported in cassava by Neal in 1889.[5] Damage on cassava is variable depending on cultivar planted, and can range from negligible to serious.[6] Early-season infection leads to worse damage.[7] In most crops, nematode damage reduces plant health and growth; in cassava, though, nematode damage sometimes leads to increased aerial growth as the plants try to compensate. This possibly enables the plant to maintain a reasonable level of production. Therefore, aerial correlations to nematode density can be positive, negative or not at all.[8] Vegetable crops grown in warm climates can experience severe losses from root-knot nematodes, and are often routinely treated with a chemical nematicide. Root-knot nematode damage results in poor growth, a decline in quality and yield of the crop and reduced resistance to other stresses (e.g. drought, other diseases). A high level of damage can lead to total crop loss. Nematode-damaged roots do not use water and fertilisers as effectively, leading to additional losses for the grower. In cassava, it has been suggested that levels of Meloidogyne spp. that are sufficient to cause injury rarely occur naturally.[8] However, with changing farming systems, in a disease complex or weakened by other factors, nematode damage is likely to be associated with other problems.[9]

Root-knot galls

Control

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Root-knot nematodes can be controlled with biocontrol agents Paecilomyces lilacinus, Pasteuria penetrans[10] and Juglone.[11]

Life cycle

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All nematodes pass through an embryonic stage, four juvenile stages (J1–J4) and an adult stage. Juvenile Meloidogynes parasites hatch from eggs as vermiform, second-stage juveniles (J2), the first moult having occurred within the egg. Newly hatched juveniles have a short free-living stage in the soil, in the rhizosphere of the host plants. They may reinvade the host plants of their parent or migrate through the soil to find a new host root. J2 larvae do not feed during the free-living stage, but use lipids stored in the gut.[3]

An excellent model system for the study of the parasitic behaviour of plant-parasitic nematodes has been developed using Arabidopsis thaliana as a model host.[12] The Arabidopsis roots are initially small and transparent, enabling every detail to be seen. Invasion and migration in the root was studied using M. incognita.[13] Briefly, second stage juveniles invade in the root elongation region and migrate in the root until they became sedentary. Signals from the J2 promote parenchyma cells near the head of the J2 to become multinucleate[14] to form feeding cells, generally known as giant cells, from which the J2 and later the adults feed.[15] Concomitant with giant cell formation, the surrounding root tissue gives rise to a gall in which the developing juvenile is embedded. Juveniles first feed from the giant cells about 24 hours after becoming sedentary.[citation needed]

After further feeding, the J2s undergo morphological changes and become saccate. Without further feeding, they moult three times and eventually become adults. In females, which are close to spherical, feeding resumes and the reproductive system develops.[3] The life span of an adult female may extend to three months, and many hundreds of eggs can be produced. Females can continue egg laying after harvest of aerial parts of the plant and the survival stage between crops is generally within the egg.[citation needed]

The length of the life cycle is temperature-dependent.[16][17] The relationship between rate of development and temperature is linear over much of the root-knot nematode life cycle, though it is possible the component stages of the life cycle, e.g. egg development, host root invasion or growth, have slightly different optima. Species within the genus Meloidogyne also have different temperature optima. In M. javanica, development occurs between 13 and 34 °C, with optimal development at about 29 °C.[18]

Gelatinous matrix

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Root-knot nematode females lay eggs into a gelatinous matrix produced by six rectal glands and secreted before and during egg laying.[19] The matrix initially forms a canal through the outer layers of root tissue and later surrounds the eggs, providing a barrier to water loss by maintaining a high moisture level around the eggs.[20] As the gelatinous matrix ages, it becomes tanned, turning from a sticky, colourless jelly to an orange-brown substance which appears layered.[21]

Egg formation and development

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Egg formation in M. javanica has been studied in detail,[22] and is similar to egg formation in the well studied, free-living nematode Caenorhabditis elegans.[23] Embryogenesis has also been studied, and the stages of development are easily identifiable with a phase contrast microscope following preparation of an egg mass squash. The egg is formed as one cell, with two-cell, four-cell and eight-cell stages recognisable. Further cell division leads to the tadpole stage, with further elongation resulting in the first stage juvenile, which is roughly four times as long as the egg. The J1 stage of C. elegans has 558 cells, and the J1 of M. javanica likely has a similar number, since all nematodes are morphologically and anatomically similar.[23] The egg shell has three layers, with the vitelline layer outermost, then a chitinous layer and a lipid layer innermost.

Egg hatching

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Preceded by induced changes in eggshell permeability, hatching may involve physical and/or enzymatic processes in plant-parasitic nematodes.[24] Cyst nematodes, such as Globodera rostochiensis, may require a specific signal from the root exudates of the host to trigger hatching. Root-knot nematodes are generally unaffected by the presence of a host, but hatch freely at the appropriate temperature when water is available. However, in an egg mass or cyst, not all eggs will hatch when the conditions are optimal for their particular species, leaving some eggs to hatch at a later date. Ammonium ions have been shown to inhibit hatching and to reduce the plant-penetration ability of M. incognita juveniles that do hatch.[25]

Reproduction

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Root-knot nematodes exhibit a range of reproductive modes, including sexuality (amphimixis), facultative sexuality, meiotic parthenogenesis (automixis) and mitotic parthenogenesis (apomixis).

Species

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References

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  1. ^ Sasser JN, Carter CC: Overview of the International Meloidogyne Project 1975–1984. In An Advanced Treatise on Meloidogyne. Edited by: Sasser JN, Carter CC. Raleigh: North Carolina State University Graphics; 1985:19–24.
  2. ^ Moens, Maurice, Roland N Perry, and James L Starr. 2009. "Meloidogyne Species: a Diverse Group of Novel and Important Plant Parasites." In Root-knot Nematodes, ed. Roland N Perry, Maurice Moens, and James L Starr, 1–17. Wallingford, UK: CABI Publishing.
  3. ^ a b c Eisenback, J. D. & Triantaphyllou, H. H. 1991 Root-knot Nematodes: Meloidogyne species and races. In: Manual of Agricultural Nematology, W. R. Nickle. (Ed). Marcel Dekker, New York. pp 281–286.
  4. ^ Stirling, G. R.; Stanton, J. M.; Marshall, J. W. (1992). "The importance of plant-parasitic nematodes to Australian and New Zealand agriculture". Australasian Plant Pathology. 21 (3): 104–115. doi:10.1071/app9920104. S2CID 30012090.
  5. ^ Neal, J. C. 1889. The root-knot disease of the peach, orange and other plants in Florida due to the work of Anguillula Bull. I.S. Bur. Ent.20.31pp.
  6. ^ Jatala, P., bridge, J. 1990. Nematode parasites of root and tuber crops. In Plant parasitic nematodes in sub-tropical and tropical agriculture., pp 137-180. Luc, M., Sikora, R.A., Bridge, J., CABI Publishing, Wallingford, UK.
  7. ^ Makumbi-kidza, N. N., Speijer and Sikora R. A. 2000. Effects of Meloidogyne incognita on growth and storage-root formation of cassava (Manihot esculenta). J Nematol.; 32(4S): 475–477.
  8. ^ a b Gapasin, R.M. 1980. Reaction of golden yellow cassava to Meloidogyne spp. Inoculation. Annals of Tropical Research 2:49–53.
  9. ^ Theberge, R. L. (eds). 1985. Common African Pests and Diseases of cassava, Yam, Sweet Potato and Cocoyam. International Institute of Tropical Agriculture (IITA). Ibadan, Nigeria 107 p.
  10. ^ Charles, Lauren; Carbone, Ignazio; Davies, Keith G.; Bird, David; Burke, Mark; Kerry, Brian R.; Opperman, Charles H. (2005). "Phylogenetic analysis of Pasteuria penetrans by use of multiple genetic loci". Journal of Bacteriology. 187 (August 2005): 5700–5708. doi:10.1128/JB.187.16.5700-5708.2005. PMC 1196054. PMID 16077116.
  11. ^ Dama, L.B.; Poul, B.N.; Jadhav, B.V.; Hafeez, M.D. (1999). "Effect of Herbal "Juglone" on Development of the plant parasitic nematode (Meloidogyne spp.) on Arachis hypogaea". Journal of Ecotoxicology and Environmental Monitoring. 9: 73–76.
  12. ^ Sijmons, P. C.; Grundler, F. M. W.; von Mende, N.; Burrows, P. R.; Wyss, U. (1991). "Arabidopsis thalliana as a new model host for plant-parasitic nematodes". The Plant Journal. 1 (2): 245–254. doi:10.1111/j.1365-313x.1991.00245.x.
  13. ^ Wyss, U., Grundler, F.M.W. & Munch, A. 1992 The parasitic behaviour of second stage juveniles of Meloidogyne incognita in roots of Arabidopsis thaliana. Nematologica, 38, 98–111.
  14. ^ Hussey, R. S. & Grundler, F. M. W. 1998 Nematode parasitism of plants. In: The Physiology and Biochemistry of free-living and plant-parasitic nematodes. Perry, R. N. & Wright, D. J. (Eds), CABI Publishing, UK. pp 213 – 243.
  15. ^ Sijmons, P. C.; Atkinson, H. J.; Wyss, U. (1994). "Parasitic strategies of root nematodes and associated host cell responses". Annual Review of Phytopathology. 32: 235–259. doi:10.1146/annurev.phyto.32.1.235.
  16. ^ Madulu, J. & Trudgill, D. L. 1994 Influence of temperature on Meloidogyne javanica. Nematologica, 40, 230–243.
  17. ^ Trudgill, D. L. 1995 An assessment of the relevance of thermal time relationships to nematology. Fundamental and Applied Nematology, 18, 407–417.
  18. ^ Bird, A. F.; Wallace, H.R. (1965). "The Influence of Temperature On Meloidogyne Hapla and M. Javanica". Nematologica. 11 (4): 581–589. doi:10.1163/187529265X00726.
  19. ^ Maggenti, A. R. & Allen, M. W. 1960 The origin of the gelatinous matrix in Meloidogyne. Proceedings of the Helminthological Society of Washington, 27, 4–10.
  20. ^ Wallace, H. R. 1968 The influence of soil moisture on survival and hatch of Meloidogyne javanica. Nematologica, 14, 231–242.
  21. ^ Bird, A. F. 1958 The adult female cuticle and egg sac of the genus Meloidogyne Goeldi, 1887. Nematologica, 3, 205–212.
  22. ^ McClure, M. A.; Bird, A. F. (1976). "The tylenchid (Nematoda) egg shell: formation of the egg shell in Meloidogyne javanica". Parasitology. 72: 29–39. doi:10.1017/s003118200004316x. S2CID 84455043.
  23. ^ a b Wood, W. B. 1988 Introduction to C.elegans. In::The Nematode Caenorhabditis elegans, W. B. Wood (Ed), Cold Spring Harbour Laboratory, New York. pp 1–16.
  24. ^ Norton, D. C. & Niblack, T. L. 1991 Biology and ecology of nematodes. In: Manual of Agricultural Nematology, Nickle, W. R. (Ed), Marcel Dekker, New York. pp 47–68.
  25. ^ Surdiman; Webster, J. M. (1995). "Effect of ammonium ions on egg hatching and second-stage juveniles of Meloidogyne incognita in axenic tomato root culture". Journal of Nematology. 27 (3): 346–352. PMC 2619617. PMID 19277298.
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