Subfamily Heteroderinae

                                 08/03/2020

Classification:

      Tylenchida                                             
       Tylenchina
        Tylenchoidea
         Heteroderidae

          Heteroderinae Filip'ev & Schuurmans Stekhoven, 1941

Morphology and Anatomy:

Heteroderinae are cyst-forming nematodes

Female:

Taxonomic Background and Differentiation of Genera:

Genera:

    Synonyms:        
           Tylenchus (Heterodera) (Schmidt, 1871)
           Heterodera (Heterodera) (Schmidt, 1871)
           Heterobolbus (Railliet, 1896)
           Bidera (Krall' and Krall', 1978)
           Ephippiodera (Shagalina and Krall', 1978)

In 1871, Schmidt described sugarbeet cyst nematode and named it after Schacht who discovered it as the cause of "beet tiredness" in Germany in 1859.

Hetero = changing; Globo = spherical; Puncto = with punctations; Deros = skin.  So, genus name indicates characteristics, shape or marking of cyst.  

The cyst nematodes (subfamily Heteroderinae) are sedentary endoparasites of plant roots in three juvenile stages, and sedentary semiendoparasites in the adult female stage. Adult males do not feed. Within the subfamily Heteroderinae there are some 15 genera. Of these, the female body forms a hardened cyst in six genera (Luc et al., 1988).

Important taxonomic revisions were instituted by Behrens (1975) in establishing the genus Globodera and by Mulvey and Stone, 1976.
Three groups of cyst shapes were recognized and were used as basis for genera:
Round Cysts no vulval cone, no egg sac Globodera, 11+ spp., e.g.  
Pear-shaped Cysts 1.5x long as wide, excluding neck  Punctodera, 3 spp., e.g. 
Lemon-shaped Cysts posterior protruberance (vulval cone), vulva at apex, egg sac occurs Heterodera, 55+spp.

abullate group (without finger-like projections of cuticle intrenally aroumd vulval region)

bullate group (with finger-like projections of cuticle internally around vulval region, and thinner areas of cuticle, fenestra)

According to Baldwin & Mundo-Ocampo (1991) the differences among selected Heteroderidae of economic importance are

“Schachtii group" (H. schachtii, H. glycines, H. trifolii, H. zeae): Bullae and underbridge well developed; vulval slit more than 35 um, ambifenestrate. 

"Goettingiana group" (H. goettingiana, H. cruciferae, H. carotae): No Bullae, underbridge poorly developed or absent; vulval slit more than 30 um, ambifenestrate or bifenestrate.

"Avenae group" (H. avenae and others): Bullae and underbridge present or absent; short vulval slit less than 16 um”.

Tanha Maafi et al (2007) also distinguish a "Sacchari group" (H. sacchari, H. leuceilyma, H. goldeni) with finger-like projections (as distinct from bullae) on the well-developed underbridge in the vulval cone of the cysts.

 

Ref: Luc, Maggenti & Fortuner,  (1988)
Tanha Maafi et al (2007)
H. Ferris.
 

Cyst sizes and shapes:

Heterodera - lemon-shaped

Globodera - round

Cactodera - lemon-shaped

Punctodera - pear-shaped

 

In studies by Subbotin et al. (2001), the ITS1, ITS2, and 5.8S gene sequences of nuclear ribosomal DNA from 40 taxa of the family Heteroderidae were sequenced and analyzed. The acronym ITS means Internal Transcribed Spacer. ITS sequences are transcribed into messenger RNA but not translated into proteins.  ITS regions may be quite variable, which adds to their value in evolutionary studies, and the ITS regions within the Heteroderinae display high levels of sequence divergence.

From these studies, the cyst-forming nematodes separate into six main clades; the clades correspond to morphological characters and host specialization.  There appear to be close relationships between the Avenae and the Sacchari groups within Heteroderinae. The Goettingiana group occupies a basal position in the subfamily.

Host Range

Most species of cyst nematodes have a narrow host range, which creates some unique possibilities for management through crop rotation. However, the adaptive disadvantage of a narrow host range is often offset by long survival in the absence of a food source, adding complexity to the design of management strategies. While a few species are well-known for their devastating effect on crops, approximately 50% of known species are exclusively parasites of grasses and sedges (Schmitt and Ferris, 1998).

Table 1. Database search of host range of cyst nematodes (NEMABASE - Ferris et al., 1995).

Nematode

Plant Hosts

Cyst Type

Genus

Species

Primary Family

Other Host Families

Lemon-shaped Heterodera mediterranea Anacardiaceae

*

Lemon-shaped Heterodera carotae Apiaceae

0

Lemon-shaped Heterodera achilleae Asteraceae

0

Lemon-shaped Heterodera cruciferae Brassicaceae

*

Lemon-shaped Heterodera cacti Cactaceae

0

Lemon-shaped Heterodera schachtii Chenopodiaceae

****

Lemon-shaped Heterodera betulae Corylaceae

*

Lemon-shaped Heterodera mothi Cyperaceae

***

Lemon-shaped Heterodera canadensis Cyperaceae

0

Lemon-shaped Heterodera cyperi Cyperaceae

0

Lemon-shaped Heterodera raskii Cyperaceae

0

Lemon-shaped Heterodera cajani Fabaceae

*

Lemon-shaped Heterodera glycines Fabaceae

*

Lemon-shaped Heterodera ciceri Fabaceae

0

Lemon-shaped Heterodera daverti Fabaceae

0

Lemon-shaped Heterodera goettingiana Fabaceae

0

Lemon-shaped Heterodera lespedezae Fabaceae

0

Lemon-shaped Heterodera medicagensis Fabaceae

0

Lemon-shaped Heterodera trifolii Fabiaceae

****

Lemon-shaped Heterodera galeopsidis Lamiaceae

****

Lemon-shaped Heterodera humuli Moraceae

*

Lemon-shaped Heterodera fici Moraceae

0

Lemon-shaped Heterodera bifenestra Poaceae

0

Lemon-shaped Heterodera delvii Poaceae  
Lemon-shaped Heterodera oryzae Poaceae

*

Punctated Punctodera punctata Poaceae

0

Punctated Punctodera chiloensis Poaceae

0

Lemon-shaped Heterodera avenae Poaceae

0

Lemon-shaped Heterodera graminis Poaceae

0

Lemon-shaped Heterodera graminiophila Poaceae

0

Lemon-shaped Heterodera hordecalis Poaceae

0

Lemon-shaped Heterodera iri Poaceae

0

Lemon-shaped Heterodera latipons Poaceae

0

Lemon-shaped Heterodera leuceilyma Poaceae

0

Lemon-shaped Heterodera longicolla Poaceae

0

Lemon-shaped Heterodera mani Poaceae

0

Lemon-shaped Heterodera oryzicola Poaceae

0

Lemon-shaped Heterodera pakistanensis Poaceae

0

Lemon-shaped Heterodera sacchari Poaceae

0

Lemon-shaped Heterodera zeae Poaceae

0

Lemon-shaped Heterodera rumicis Polygonaceae

0

Lemon-shaped Heterodera weissi Polygonaceae

0

Lemon-shaped Heterodera thornei Portulacaceae

0

Round Globodera pallida Solanaceae

*

Round Globodera tabacum Solanaceae

*

Round Globodera rostochiensis Solanaceae

**

Lemon-shaped Heterodera urticae Urticaceae

0

? Cactodera eremica Chenopodiaceae

0

? Dolichodera ? ?

?

? Afenestrata ? ?

?

0 = hosts not known in other plant families

* = hosts occur in very few other plant families

** = hosts occur in few other plant families

*** = hosts occur in several other plant families

**** = hosts occur in many other plant families

Recognition of the damaging effects of cyst nematodes to crops is originally documented in Schacht’s (1859) descriptions of "beet tiredness" in German sugarbeet fields. Qualitative surveys and conventional wisdom indicate that cyst nematodes rank prominently in importance among the plant-parasitic nematodes of agricultural crops. In some areas of the world, due to the nature of crops grown, direct damage potential, and costs associated with regulatory programs, they are considered the most important genera (e.g., Sasser and Freckman, 1987). Those rankings provide cause for reflection. Other genera at the top of the importance list are damaging to a wide range of crops (e.g., Meloidogyne, Pratylenchus). The cyst nematodes achieve their prominence, not only because they cause direct damage to host crops, but also because of the long-term disruption of cropping patterns necessary for their management and the disruption of marketing opportunities associated with regulatory programs.

Host Range and Responsiveness to Hatching Factors

In many Heteroderinae, host range is narrow and specialized.  Fitness of these nematodes and success in agricultural systems can be attributed to high survival ability - up to 15 years for the round-cyst nematode, Globodera rostochiensis.

In general, Heteroderinae with a narrow host range are most sensitive to hatching factors originating for host roots; those with wider host ranges are less sensitive.

Host-mediated hatch in response to host root exudates.  Vary in degree of response to hatching factors:
         a) Very sensitive - hatch in water only 5% of that in host root diffusate.
            G. rostochiensis, H. carotae, H. cruciferae, H. humuli
         b) Intermediate - hatch in water 10-50% of that in diffusate.
            H. schachtii, H. trifolii, H. galeopsidis.
         c) Insensitive - apparently not stimulated by diffusate.
            H. goettingiana, H. avenae, H. glycinesH. avenae requires a chill period to break diapause.
Artificial hatching agents include Aminoacridine (Rivanol) and ZnCl for H. schachtii.
Ecological factors also influence hatch: temperature, moisture, aeration, osmotic potential, pH, etc.   

Also, several forms of delayed hatch and diapause are exhibited within the Heteroderinae.  

References

Behrens, E. (1975) Globodera Skarbilovic, 1959, eine selbstindige Gattung in der Unterfamilie Heteroderinae Skarbilovic, 1947 (Nematoda: Heteroderidae). Vortragstagung zu
aktuellen Problemen der Phytonematologie am 29/5/1975 in Rostock. Manuskriptdruck der Vortrage. Rostock, 1975, pp.12-26.

Ferris, H., E. P. Caswell-Chen, and R. L. Sloan. 1995. Synopsis of a developing database of the host status of plants to nematodes. Journal of Nematology 27:499-500.

Luc, M., A. R. Maggenti, and R. Fortuner. 1988. A reappraisal of Tylenchina (Nemata). 9. The family Heteroderidae Filip’ev and Schuurmans Stekhoven, 1941. Revue de Nématologie 11:159-176.

Sasser, J. N., and D. W. Freckman. 1987. A world perspecive on Nematology: the role of the society. Pp. 7-14 in J. A. Veech and D. W. Dickson (eds). Vistas on Nematology. Society of Nematologists, Hyattsville, MD.

Schacht, H. 1859. Über einige Feinde der Rübenfelder. Zeit. Ver. Rubenzuckerindustrie Zolluer. 9:175-179.

Schmitt, D. P. and H. Ferris. 1998. Pathogenicity and damage levels. Pp 239-265 in S. B. Sharma (Ed.). The Cyst Nematodes. Kluwer Academic Publishers, Dordrecht. 452p.

Subbotin, S.A., A. Vierstraete, P. De Ley, J. Rowe, L. Waeyenberge, M. Moens and J.R. Vanfleteren. 2001. Phylogenetic Relationships within the Cyst-Forming Nematodes (Nematoda, Heteroderidae) Based on Analysis of Sequences from the ITS Regions of Ribosomal DNA .  Molecular Phylogenetics and Evolution, 21:1-16.

Tanha Maafi, Z., Sturhan, D., Handoo, Z., Mor, M., Moens, M., Subbotin, S.A. 2007. Morphological and molecular studies on Heterodera sacchari, H. goldeni and H. leuceilyma (Nematoda: Heteroderidae). Nematology 9: 483-497.

 

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