Nematode Parasites of Higher Plants Nematode Parasites of Animals and Humans
   

                   Rev 12/21/2012

Taxonomic classification of plant parasites:

      Plant parasites occur in the orders:
                         Rhabditida (Chromadorea)
                         Dorylaimida (Enoplea)
                         Triplonchida (Enoplea)

Plant parasitism evolved independently in three traditional nematode orders, Dorylaimida Pearse 1942, Triplonchida Cobb 1920 (both Enoplea), and Rhabditida (Tylenchina Thorne 1949) (Chromadorea). In the Tylenchina, ribosomal RNA analysis suggests that plant parasites have evolved within clades that include many free-living nematodes (Baldwin et al, 2004). Insight from molecular phylogenies based on the nuclear small subunit ribosomal RNA indicate that the enoplean Dorylaimida and Triplonchida lack a common ancestor.  Tylenchina shares a most recent common ancestor with Cephalobina (primarily bacteriovore Cephaloboidea).  Triplonchida appears to be the sister clade to the Enoplida Filipjev, 1929 (primarily marine omnivores and bacteriovores), and Dorylaimida are embedded within a clade that includes insect parasites (Mermithida), vertebrate parasites (Trichinellida), and predators (Mononchida, and other Dorylaimida).  It cannot be assumed that plant parasitism arose only once in each order (Baldwin et al, 2004).

Within the Dorylaimida, the evolutionary origin of the Longidoridae is currently uncertain, however the genus Longidorella (Nordiidae) appears to have evolved from an omnivore ancestor while the evolutionary history of Pungentus is uncertain (Holterman et al. 2008).

Plant-feeding Nematodes of the Phylum Nematoda

Class Chromadorea

Class Enoplea

Rhabditida

  Dorylaimida

Triplonchida

Tylenchina
  Classification by Functional Guild
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     Rhabditida
         Suborder:
Tylenchina - dorsal esophageal gland opening (DEGO) in procorpus
                         
           Three superfamilies:

                Criconematoidea

Tylenchoidea

                    Aphelenchoidea

     Dorylaimida
         Sub-order: Dorylaimina

     Triplonchida
         Sub-order: Diphtherophorina
           Superfamily: Diphtherophoroidea


Anatomy of Plant-feeding Nematodes (Order Rhabditida)

Drawings by Charles S. Papp, CDFA

 

Classification of plant parasites by feeding habit:

1.  Ectoparasites of plant roots
     a.  Migratory
     b.  Sedentary
2. Semi-endoparasites of plant roots
    a.  Migratory
    b.  Sedentary
3.  Endoparasites of plant roots
    a.  Migratory
    b.  Sedentary
4. Endoparasites of bulbs and stems

5. Endoparasites of leaves

6. Endoparasites of seeds

Definitions:

  • Migratory ectoparasites:  Remain outside the root or other feeding area throughout the life cycle and feed on epidermal cells or on cells deeper in the root.  Retain the ability to move to new feeding sites.
  • Sedentary ectoparasites:  Remain outside the root or other feeding area throughout the life cycle but feed from a modified nurse cell or group of nurse cells for an extended period.
  • Migratory endoparasites:  Enter the root system or other feeding area and feed from cells as they migrate.
  • Sedentary endoparasites Enter the root system or other feeding area and feed from highly modified cells.  Lose the ability to move and must maintain an active feeding site.
  • Migratory and sedentary semi-endoparasites:  Subcategories of the above with only the anterior portion of the body within the root and the remainder on the root surface.
  • Feeding Habits of Nematodes on Plant Roots Sedentary Forms of Root-feeding Nematodes
    Drawings by Charles S. Papp, CDFA

     

    Commonalities

    • Plant-parasitic nematodes with postcorpus (digestive glands) bounded by a  membrane are all ectoparasites; 
    • All genera that feed or that can feed endoparasitically have overlapping esophageal glands with dorsal gland usually more developed.
    • Nematodes with long stylets are ectoparasites; those with short stylets may be ectoparasites or endoparasites.
    • Nematodes with long stylets feed several cell layers deep and do not move  frequently to new feeding sites; hence they are relatively sedentary.
    • Nematodes with long stylets and those that use the stylet actively to penetrate cells have a well-developed headframe.
    • Metacorpus size and feeding habit or feeding rate??
    • No apparent relationship between number of gonads and feeding habit.
    • No apparent relationship between mode of reproduction and feeding habit, although parthenogenesis is common.
    • Caudal alae and feeding habit??
    • Tail length (c') and number of ovaries??
    • Tail length and feeding habit??

    Ref:  Bongers (1988), Ferris and Bongers (communication), Luc et al.

    Generalizations

    Plant-feeding nematodes that have long bodies (>2mm):

    • are ectoparasites (or feed in natural channels in the root).
    • have long stylets and feed in deeper root tissues.
    • are sedentary ectoparasites and stimulate nurse cells.
    • have low ovary to body volume ratios and partition more assimilates to maintenance of somatic tissues
    • have lower fecundity than short-bodied nematodes.
    • are susceptible to mechanical soil disturbance.
    • inhabit coarse-textured soils or structured soils with high aggregate stability.
    • are components of structured and mature food webs.

    Community Structure of Nematodes Parasites of Higher Plants:

    Generalizations

    • A diversity of plant-feeding nematodes with different feeding habits and morphotypes occurs in nutrient-enriched agricultural systems.
    • In nutrient-enriched systems, plant-feeding nematodes are often in great abundance.
    • In natural, non-enriched systems, abundance of plant-feeding nematodes is usually much lower than in agricultural systems. 
    • In natural, non-enriched systems, plant-feeding nematodes with small bodies and high ovary:body ratios predominate.
    • In natural, non-enriched systems, plant-feeding nematodes with long stylets, sedentary lifestyles, nurse cells and other features that increase the access to limited resources, predominate.
    • In natural, non-enriched systems, narrow host-range specialists rather than wide host range generalists, predominate.

    Conversations among Ferris, Tom Bongers, Bart Verschoor, Ron de Goede.

    References

    Baldwin, J.G., S.A. Nadler and B.J. Adams. 2004. Evolution of plant parasitism among nematodes. Ann. Rev. Phytopathol, 42:83-105.

    Holterman et al. 2008. A ribosomal DNA-based framework for the detection and quantification of stress-sensitive nematode families in terrestrial habitats. Molecular Ecology Resources 8:23-34.

     

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