Vector Specificity

11 spp of Xiphinema transmit 13 NEPO viruses

11 spp of Longidorus transmit 10 NEPO viruses
14 spp of Trichodorus transmit various strains of two TOBRA viruses:
tobacco rattle and pea early browning.
Lamberti (1987) suggests that since several trichodorid spp transmit the
same virus, and that both viruses are transmitted by the same nematode,
vector specificity is less developed in trichodorids than in longidorids.

Transmission Characteristics

Trichodorids may retain the virus for up to a year.

Acquisition time may be less than an hour to several days, depending on the
feeding characteristics of the nematode.

Retention sites: Longidorus - odontostyle area

Xiphinema - odontophore and esophagus region
Trichodorus - onchiostyle and esophagus.
Selectively and specifically adsorbed at retention site - indicating a specific association between
protein coat of virus and cuticular surface.

Dissociation with cuticle probably occurs as glandular secretions pass forward into the plant cell.

 Virus does not pass through the egg stage.

 Virus does not replicate in the nematode.
 Virus is not retained through a molt.

In Xiphinema and Trichodorus, although the lining of the esophagus is not shed at a molt, it
undergoes structural changes and virus particles may pass into the intestine.
In Longidorus the stoma, odontostyle and guiding sheath are shed.

Nepoviruses

X. americanum (sensu lato) transmits tobacco ringspot and tomato ringspot.

The virus is acquired within 24 hours of the initiation of feeding.
Virus particles are transmitted by both adults and juveniles.
X. americanum transmits the tomato ringspot virus strains:
peach rosette mosaic virus
peach yellow bud mosaic virus
cherry rasp leaf virus
 grapevine yellowvein virus
Particles are carried in the esophagus lumen.

Lamberti et al. consider that X. americanum is not a vector of tomato ringspot virus, although
it is widely reported to be. They contend
that the reports represent a mis-identification especially in California where they feel that the
vector is X. californicum. However, Griesbach
and Maggenti (1989) found a wide range of vectoring capabilities of tomato ringspot viruses
with California populations of X. americanum sensu lato.
On the basis of considerable overlap of morphological and morphometric characters among
putative species, they synonymized X. americanum and
X. californicum (Griesbach and Maggenti (1990). That synonymy was later rejected (Robbins
and Brown, 1991). The situation is not yet clearly
resolved; studies on developmental biology and the application of molecular techniques are
providing further information on the diversity
within the whole X. americanum group (Halbrendt and Brown, 1993; Vrain,1993).
Lamberti suggests that the same mis-identification occurs with the vector of Cherry Rasp Leaf
virus in California.
There is a need for the application of molecular biology techniques in this problem of
diagnostics.

X. californicum transmits prune brown line and Prunus stem pitting strains of tomato ringspot
virus readily and the cherry leaf mottle strain rarely. (Hoy, Ph.D thesis, UC. Davis)
X. diversicaudatum transmits Arabis mosaic virus to variety of crops.
Adults retain the virus for at least 8 months.
X. index - grapevine fanleaf virus can be acquired in 5 to 15 minutes, persists up to 9 months
when nematode not feeding.
Longidorus elongatus transmits raspberry ringspot and tomato blackring
viruses.

Docking Disorder

Longidorus leptocephalus, L. attenuatus, L. elongatus, Trichodorus spp and viruses are

involved in Docking disorder of sugarbeets (named for Docking
region in south of England). Stunted growth in spring due to nematodes, virus symptoms in
foliage. Effects are most pronounced in spring, heavy
rainfall in May seems to increase the problem. In July the affected plants start to grow again
and may achieve almost normal foliage, but a much
reduced tap root. The severity of Docking disorder varies from year to year with the climate.
Management by rotation is difficult as several nematode species are involved, each with a
differing host range. Also host ranges of these
nematodes are not completely known.
1,3-D nematicide applied in the plant row prior to planting reduces the nematode populations
and increases yield, but only in well-drained alkaline
 soils. The treatment is not always effective at economically feasible rates.

Grapevine Fanleaf Virus

Grapevine Fanleaf Virus Degeneration is the oldest known disease of Vitis vinifera.

Records in Europe date back 200 years and specimens in herbaria displaying symptoms predate
the introduction of American rootstocks (Martelli and Sovino, 1988). Grapevine Fanleaf
Virus Degeneration is the oldest known disease of V. vinifera.

The observation that X. index transmits grapevine fanleaf virus (GFLV) was the first
record of virus transmission by a nematode (Hewitt et al., 1958).

The virus is lost during the molt of the cuticle between life stages. The virus is not
passed through the egg stage. Consequently, the virus is re-acquired by feeding of
each vermiform life stage of the nematode. GFLV causes reduced vigor, lack of fruit
set, and reduced yield of grapevines. Of great importance in the design of control
programs for the X. index / GFLV problem is that portions of the grape root system
can remain alive and serve as a reservoir for virus and nematode for at least 5 years
after vine trunks have been removed (Raski et al., 1965).

The grapevine fanleaf virus is a Nepovirus with isometric particles of 30nm diameter. It is
transmitted by X. index and X. italiae, with X. index the more efficient vector (Argelis, 1987;
Martelli and Savino (1988).

The virus can be acquired in less than 15 minutes of feeding on an infected plant and is retained
up to eight months in the absence of feeding (Taylor and Robertson, 1975).).

The retention site for GFLV in X. index is the cuticular lining of the esophagus, including the
area surrounding the odontophore (Taylor and Robertson, 1975). As with other viruses
vectored by longidorid and trichodorid nematodes, it is selectively and specifically adsorbed at
the retention site, indicating a specific association between protein coat of virus and cuticular
surface. Dissociation with cuticle probably occurs as glandular secretions pass forward into the
plant cell (Taylor and Robertson, 1975).

The virus does not pass through the egg stage. It is not retained through a molt when the
esophageal lining and odontostyle are also shed. In Xiphinema, although the lining of the
esophagus is not shed at a molt, it undergoes structural changes and virus particles may pass into
the intestine (Taylor and Robertson, 1975).

The virus does not replicate in the nematode vector.

Detection:
 From a management standpoint, it is important to determine whether X. index is present in
a site intended for a vineyard, and whether the nematodes are viruliferous.

Virus particles can be detected in extracts from single nematodes by immunosorbent electron
microscopy (Roberts and Brown, 1980), however, as indicated by Esmenjaud et al (1993) the
procedure is complex and not readily adapted to routine assays.

Enzyme-linked immunosorbent assay (ELISA) methods are routinely used to determine GVFL
in plant tissue (Walker et al, 1994). When applied to nematodes, the techniques appear
sufficiently sensitive to detect the virus if more than ten viruliferous individuals are used, but are
unreliable for single individuals (Esmenjaud et al, 1993).

Symptoms:

Martelli and Savino (1988) describe three distinct syndromes of symptoms of

grapevine fanleaf degeneration:

1. Malformations: Leaves are variously distorted, asymmetrical, with

wide petiole sinuses and abnormal vein arrangement that results in the
appearance of an open fan. Leaf symptoms may also include chlorotic
mottling. Foliar symptoms are most evident in the spring and through the
vegetative growth period. Shoots show abnormal branching, with double
nodes and short internodes, while forming angles at internodes. Bunches
are small with poor fruit set and shot berries. They ripen irregularly.

2. Yellow mosaic: Bright yellow discoloration of leaves, shoots, tendrils

and inflorescences in the spring. Foliage and clusters are not malformed,
but clusters are small.

3. Veinbanding: Yellow flecking along main veins and associated

interveinal areas of mature leaves appearing mid to late summer. Leaves
are not malformed, but fruit set is poor and yield is low.
Martelli and Savino (1988) describe three distinct syndromes of symptoms of
grapevine fanleaf degeneration:

1. Malformations: Leaves are variously distorted, asymmetrical, with

wide petiole sinuses and abnormal vein arrangement that results in the
appearance of an open fan. Leaf symptoms may also include chlorotic
mottling. Foliar symptoms are most evident in the spring and through
the vegetative growth period. Shoots show abnormal branching, with
double nodes and short internodes, while forming angles at internodes.
Bunches are small with poor fruit set and shot berries. They ripen
irregularly.
Veinbanding Sym
2. Yellow mosaic: Bright yellow discoloration of leaves, shoots, tendrils
and inflorescences in the spring. Foliage and clusters are not malformed,
but clusters are small.

3. Veinbanding: Yellow flecking along main veins and associated

interveinal areas of mature leaves appearing mid to late summer. Leaves
are not malformed, but fruit set is poor and yield is low.

Asymmetric leaf formations Abnormal

Several closely related nepoviruses found in grapevines are apparently related to

GFLV but are serologically different. They are sap-transmissible, and where vectors
have been definitively established they are species of Xiphinema and Longidorus.
They include arabis mosaic virus, raspberry ringspot virus, tomato blackring virus,
grapevine chrome mosaic virus, Strawberry latent ringspot virus, artichoke Italian
latent virus, and grapevine Bulgarian latent virus (Argelis, 1987; Stellmach and
Goheen, 1988).

One or more of ten species of Xiphinema are present in all major grape-growing
regions of the world. They
are X. algeriense, X. americanum, X.brevicolle, X. diversicaudatum, X. index, X. italia
e, X. mediterraneum, X. pachtaicum, X. turcicum, and X. vuittenezi (Raski, 1988).
With X. index a notable exception, most species of Xiphinema have a wide host range
and are adapted to a wide range of soil textures.

Xiphinema americanum is actually considered a group of some 39 species, which

include X. brevicolle and X. pachtaicum. Molecular techniques (Vrain, 1993),
biological evaluations (Halbrendt and Brown, 1993) and virus transmission studies
(Brown et al., 1993) are continuing to underscore the variability and similarities
within the X. americanum group. These studies are adding to the body of knowledge
that will be required for an eventual taxonomic revision. The group also
includes X. californicum Lamberti and Bleve-Zacheo, which is probably associated
with grape in California (Lamberti and Ciancio, 1993).

Tomato Ringspot Virus in Grapevines

Tomato Ringspot Virus Degeneration is also called grape yellow vein disease, tomato
ringspot disease, and little berry disease. It is endemic in the northeastern U.S. and
Canada, and occurs less frequently in California (Gonsalves, 1988). The nepovirus is
transmitted by X. americanum, X. californicum, and X. rivesi. Particles are carried in
the esophagus lumen adhering to the cuticular lining. Since there is considerable
variability in the species complex that is loosely-termed X. americanum, Lamberti and
Bleve-Zacheo (1979) contend that reports of X. americanum as a vector of TRSV
represent a misidentification, or predate taxonomic revisions. They consider
that X. californicum is the vector of TRSV in California. However, Griesbach and
Maggenti (1989) found a wide range of vectoring capabilities of TRSV strains with
California populations of X. americanum sensu lato.

Symptoms of Tomato Ringspot Virus Degeneration differ geographically, with the

disease more severe in colder regions. Leaves are mottled, with oak leaf patterns, new
growth is weak and buds are susceptible to cold damage. Internodes are shortened,
leaf area is reduced, and clusters are small. The grape yellow vein symptom, common
in infections with this virus in California, consists of yellow flecking along the veins
and associated lamina. There is reduced fruit set and slow decline of the vine
(Gonsalves, 1988).

Peach Rosette Mosaic Virus in Grapevines

Peach Rosette Mosaic Virus Decline is a disease of V. labrusca L. grapevines that

occurs only in Michigan in the U.S. The virus also causes a disease in peach, as
indicated by the name (Ramsdell, 1988). This nepovirus is a strain of TRSV
transmitted by X. americanum and Longidorus diadecturus with the characteristics of
other nepoviruses transmitted by these genera. The virus may be endemic in vineyard
weeds, which complicates exclusionary measures. Symptoms of Peach Rosette
Mosaic Virus Decline include puckered leaves with flattened basal sinuses, sparse
clusters, and crooked shoots. The vines are susceptible to winter injury (Ramsdell,
1988).

Tobraviruses
Trichodorus viruliferous - transmits tobacco rattle and pea early browning virus. It is sometomes
involved in Docking disorder in sugarbeets in England. Trichodorus similis - transmits tobacco
rattle virus. At least 14 species of Trichodoridae have been demonstrated to vector Tobra viruses.

Tobacco rattle virus (genus Tobravirus) is a multi-component virus with rod-shaped long (RNA-
1) and short (RNA-2).particles (Mojtahedi et al., 2000).

 M-type (normal) viral isolates contain both RNA-1 and RNA-2; they code for
coat protein synthesis and are readily transmitted mechanically and by
trichodorid nematodes (Stevenson et al., 2001)..
 NM-type viral isolates have only contain RNA-1. They can be sap-transmitted
and move through the plant systemically. Since they do not code for coat
protein synthesis are not transmitted by trichodorid nematodes (Dale et al.,
2004).
 The multi-component nature of the particles results in considerable variation
among isolates (Brown et al., 2000; Mojtahedi et al., 2001).

Corky Ringspot of Potato (Spraing)

Corky ringspot is caused by tobacco rattle virus (Tobravirus), which is vectored by

stubby-root nematodes (Paratrichodorus spp. and Trichodorus spp.). The condition is
sometimes referred to as Spraing, a Scottish word meaning a bright streak or stripe (de
Bokx, 1972).

Corky ringspot symptoms vary depending on virus strain, potato cultivar, and time of
infection. Symptoms often include of brown necrotic rings, arcs, and diffuse spots
which are considered quality defects and may result in after-harvest devaluation or
rejection of either table or processed potatoes.

External Symptoms of Corky Ringspot Virus on a Potato Tuber Internal Symptoms of Corky

Corky ringspot symptoms in potato include necrotic rings and pits on the tuber surface
and range from diffuse brown spots to concentric rings or arcs of brown, necrotic
tissue to dark-brown necrotic tissue which extends through tuber flesh (Mojtahedi et
al., 2001). The virus is usually detectable when symptoms are seen but may also be
present in asymptomatic tissue (Charlton, 2006).

Tubers from soil with a history of tobacco rattle virus serve as a reservoir. The virus
may spread to daughter tubers when infected tubers are used as seed (Crosslin et al.,
1999). Newly formed potato tubers are quite vulnerable to tobacco rattle
virus infection and tubers as small as 3-cm in diameter had corky ringspot blemishes
in tobacco-rattle infested fields in Florida (Weingartner et al. (1975).

Tobacco Rattle Virus is reported in many areas of the world and more than 400 plant
species in 50 plant families are susceptible to infection (Brunt et al., 1996; Dallwitz,
1980; Dallwitz et al., 1993; Hooker, 1981; Ploeg et al., 1989).

Several species of Trichodorus and Paratrichodorus transmit M-type isolates of

Tobacco Rattle Virus (Harrison and Robinson, 1986). Stubby-root nematodes are
migratory ectoparasites that are mobile during each stage of their life cycle (Stark and
Love, 2003) and feed primarily on meristematic cells or root tips which hinders root
elongation (Crow, 2005). Damaged root tips may swell and lateral roots may emerge
behind them, resulting in root proliferation.

The life cycle of stubby-root nematodes is not well studied. Eggs

of Paratrichodorus minor, hatch 53.3 ± 7.3 degree-days using a basal threshold of
10 C (DD10C) after egg deposition. Second stage population peaks occurred at 28
º

DD10C , third stage at 67 DD10C , fourth stage at 109 DD10C and adults at 143 DD10C for
adults. Population densities increased in the presence of a suitable host but declined to
33% of the initial level after 300 DD10C in the absence of a host (Schneider and Ferris,
1987). The optimum temperature range for development and reproduction
of Paratrichodorus allius is 21 to 24 C (Ayala et al., 1970).
º

In general, Trichodoridae nematodes prefer coarser textured soils and avoid

desiccation stress by migrating vertically to moister soil layers. Vertical movement of
Trichodoridae nematodes appears greatest when soil pores are half-full of water and
least in waterlogged or dry soil conditions (Decraemer, 1995). Since soil moisture is
often maintained below field capacity for optimum yield and quality in potato
production, vertical migration may explain the difficulty of consistently finding
stubby-root nematodes during routine soil sampling procedures to 30-cm depth in
Washington and Oregon (Charlton, 2006).

Stubby-root feeding injury is not important economically and is rarely visible in

potato, however, corky ringspot virus can be transmitted at very low population
densities of the nematode (Charlton, 2006).