Globodera pallida
(white potato cyst nematode)

G. pallida originates from the Andes and is known to be present in 55 countries. It is found predominantly in temperate regions as is the related species, Globodera rostochiensis. It is possibly more difficult to manage than G. rostochiensis because there is currently less resistance available in commercially-grown potato cultivars.

Egg-laden cysts are the most environmentally resistant and easily transportable stage in the parasites life cycle, and are found in soil particles, on host roots, stolons or tubers. The microscopic size of the cyst makes it difficult to detect, and it can successfully establish new infestations when an appropriate climate and host plant are available.

Machinery used on infested land followed by use in otherwise uninfested areas is a common method of spread, for example, fumigation equipment that has not been cleaned before use in another area. Disinfection of farming tools, transport and clothing helps to keep uninfested land free from G. pallida. Wind, rain and flood water are also capable of redistributing viable cysts to create new infestations.

See also CABI/EPPO (1998, No. 161). The centre of origin of the species is in the Andes Mountains in South America, from where it has spread with the introduction of potatoes to other regions. The present distribution covers temperate zones down to sea level and in the tropics at higher altitudes. In these areas, distribution is linked with that of the potato crop.

Potato cyst nematodes are A2 quarantine pests for EPPO. They are also of quarantine significance for APPPC and NAPPO. Virtually all areas within the EPPO region that grow potatoes are already contaminated with potato cyst nematode. These areas are generally closely monitored. It is important to keep seed potato areas free of potato cyst nematode. Domestic measures and import controls are justified as they help to reduce spread and introduction of new pathotypes into already colonised areas. Globodera rostochiensis still seems to be the dominant species throughout Europe with the exception of England, UK, where G. pallida is common.

Phytosanitary measures

To prevent further spread of potato cyst nematode into uninfested areas, several methods are used. These include international and national legislation on the movement of seed potatoes, nursery stock, flower bulbs and soil (CEC, 1969).

The specific EPPO quarantine requirements (OEPP/EPPO, 1990) for these nematodes are that fields in which seed potatoes or rooted plants for export are grown are inspected by taking soil samples according to an EPPO-recommended method (OEPP/EPPO, 1991; EPPO, 2007) and must be found free from viable cysts of both species of potato cyst nematode. The sampling must be performed after harvest of the previous potato crop.

The major hosts of G. pallida are restricted to the Solanaceae, in particular potato, tomato and aubergine (Ellenby, 1945; 1954; Mai, 1951; 1952; Winslow, 1954; Stelter, 1957; 1959; 1987; Roberts and Stone, 1981; Sullivan et al., 2007). Oxalis tuberosa has been extensively tested in host range tests by Sullivan et al. (2007) with constant negative results and has been declared a non-host on this basis.

A cyst of G. pallida (PCN) contains as many as 500 eggs, which will form the next generation. The eggs can remain viable for many years before gradually deteriorating. Factors affecting hatching are very similar to those that affect Globodera rostochiensis. Soil moisture content has an important effect on both the movement of the second-stage juveniles and, consequently, their use of lipids; adequate soil moisture and lipid levels are both necessary for root infection. Various hatching stimuli are known, for example, root diffusate (Perry and Beane, 1988) and certain organic and inorganic chemical compounds (Clarke and Hennessy, 1987). G. pallida hatches at around 10°C or less and is adapted to develop at cool temperatures between 10 and 18°C, whereas G. rostochiensis seems to be adapted to a temperature range of 15 to 25°C (Franco, 1979). Day length also influences egg hatching, which is faster where the host has continuous light rather than prolonged hours of darkness (Hominick, 1986).

As with other cyst nematodes, the second-stage juvenile is the infective stage and, upon hatching, invades the host just behind the root tip. The juveniles move up or down the root until they receive a specific signal, which is likely to be of a chemical nature, to set up a feeding site in the form of a syncytium. The ultrastructure of the feeding site and nematode interaction with the syncytium have been studied intensively (Wyss and Zunke, 1986; Golinowski et al., 1997; Endo, 1998). The life cycle takes around 45 days to complete, during which time the second-stage juvenile develops into a male or a female whose survival depends on environmental factors such as available nutrients. Juveniles that penetrate the pericycle cells of the plant are more likely to become males, whereas those that penetrate the procambial cells tend to become females (Golinowski et al., 1997). Studies of G. rostochiensis juveniles have shown that, after a few hours of inactivity, the juvenile probes the selected cell and inserts its stylet into it while remaining motionless for several hours; the stylet is withdrawn and re-inserted into the same cell. A secretory product from the oesophageal glands is injected via the stylet into the selected cell. The initial syncytial cell is altered to provide large amounts of nutrients to the developing nematode. The syncytium undergoes major changes, for example lysis of inner cell walls, formation of cell wall ingrowths next to plant conductive tissue, formation of numerous lipid bodies and enlarged amoeboid nuclei are present. Some of these events are still not fully understood. In resistant plants, the juvenile may try to form a syncytial feeding site but the walls of cells involved usually thicken and cells may die. This prevents the ready movement of nutrients to the juvenile (Rice et al., 1986; Robinson et al., 1988).

Males are relatively more abundant when environmental conditions are poor as they require less food than females and do not feed during the free-living stage (Evans, 1970). The vermiform male has a short life span of ten days or so and, during this time, it will mate with as many available females as possible. At this point in the life cycle, the white or cream females have become obese and broken through the root cortex, exposing their genitalia. The females secrete pheromones which attract males (Green and Miller, 1969; Green and Plumb, 1970; Mugniery, 1979; Mugniery et al., 1992).

Numerous studies on the biochemistry of both G. rostochiensis and G. pallida have been published since isoelectric focusing was first used to display different protein profiles for G. rostochiensis and G. pallida (Fleming and Marks, 1983). This is a quick, dependable and relatively inexpensive method of identification of the species of potato cyst nematodes. Other techniques are capable of greater discrimination, such as pathotypes within a population (Hinch et al., 1998). Monoclonal antibodies have also been used to develop diagnostic procedures based on ELISA (Curtis et al., 1998). DNA-based techniques are used routinely with a range of methods and species-specific primers (Mullholland et al., 1996; Fullaondo et al., 1999) now being used with diagnostics applications such as RAPD, RFLPS, AFLPS and multiplex PCR, which have become less expensive and more user friendly. With the many kits now designed to help with the methodology, even greater discrimination is possible. Sequencing of DNA is now undertaken in many laboratories not only to identify to species, but also in studying plant-nematode interactions with a view to developing better control methods (Perry and Jones, 1998).

Disruption of the nematode life cycle may be possible through the insertion of genetic constructs coding, for example, enzyme inhibitors into the plant by genetic engineering (Burrows, 1996; Burrows and De Waele, 1997). Studies have also been made of nematode secretions and their function and interaction within the host plant (Jones and Robertson, 1997; Jones and Harrower, 1998). The role of cuticular secretions in plant parasitic nematodes is not yet fully understood (Forrest et al., 1989; Jones et al., 1997). Changes occur in the cuticle of second-stage juveniles when they begin to feed: in addition to changes associated with natural growth patterns and the onset of moulting, changes occur that appear to be linked to interaction with the plant host (Jones and Robertson, 1997).

Molecular techniques have now advanced so far as to enable the functions of individual genes to be studied. Gp-FAR-1 has been identified from the surface of G. pallida and  is considered to be involved in eluding the defence system of the host plant (Prior et al., 2001). More recent studies on other genes identified from G. rostochiensis have highlighted the complexity of host penetration and the function of pectate lyases utilised by PCN for parasitism (Kudla et al., 2007). RNA interference (RNAi)  has been used in a range of studies and a recent review of progress in this area (Lilley et al., 2007) provides details of target genes in plant parasitic nematodes including PCN. Other biochemical studies have investigated the action of nematode proteinases and their possible involvement in extracellullar digestion (Koritsas and Atkinson, 1994; Lilley et al., 1996). Proteinase genes have been found in Caenorhabditis elegans (Sarkis et al., 1988) and Haemonchus contortus (Pratt et al., 1990). Proteinase inhibitors expressed in plants may have the potential to control nematodes (Hepher and Atkinson, 1992). There are marked differences in the secretions from the two species of potato cyst nematodes, namely G. pallida and G. rostochiensis (Duncan et al., 1997) and lectin blotting with WGA (wheat germ agglutinin) shows further differences: there were no differences between populations of G. rostochiensis, but there were between populations of G. pallida.

General

• Laboratory use
• Research model

Genetic importance

• Test organisms (for pests and diseases)

Detection based on host plant symptoms and identification by morphological and molecular methods are detailed in OEPP/EPPO (2009).

Surveys

Field samples are taken to check if potato cyst nematode is present or not, and to determine which species is present and in what quantities. This information is required in order to plan the management of any infestation. In the past, nematodes were thought to have a random distribution throughout a field, whereas it now seems likely that distribution is aggregated. Statistical models have been used to assess the existing and potential distribution of potato cyst nematode in fields, but geostatisical models and techniques may provide more definitive information on spatial distribution. See Been and Schomaker (2006).

G. pallida, a sibling species of G. rostochiensis, can be distinguished by the colour of the mature female: most other species of the genus have yellow to golden females, whereas G. pallida has white or cream females, depending on the pathotype. In general, the second-stage juveniles of G. pallida are longer, have a more robust-looking stylet with forward pointing basal knobs, and have longer true tail lengths than other species in the genus.

G. pallida, G. rostochiensis and the G. tabacum complex, which includes G. tabacum (Lownsbery and Lownsbery, 1954), G. solanacearum (Miller and Gray, 1972) and G. virginiae (Miller and Gray, 1968) plus the subspecies G. 'mexicana', incompletely described by Campos-Vela (1967), share an extensive host range mainly composed of solanaceous species, with the G. tabacum complex more commonly found on the spiny species whereas potato cyst nematodes have a preference for tuber-forming species. The G. tabacum complex is mainly confined to North, South and Central America. G. 'mexicana' appears to have greatest affinity with G. pallida and these species are able to interbreed (Mugniery, 1978).

Other Globodera species, such as G. artemisia (Eroshenko and Kazachenko, 1972), are found only on Compositae hosts. G. artemisia can be distinguished morphologically, having a very small Granek's ratio and second-stage juveniles with backward sloping stylet knobs. Globodera leptonepia (Cobb and Taylor, 1953), a species found just once in soil with a consignment of potatoes, has seven folds in the second-stage juvenile within the egg, whereas G. pallida has only four.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

SPS Measures

Legislation provides a definitive set of rules (MAFF, 2000) designed to prevent the spread of potato cyst nematodes. The movement of soil is a common factor in the spread of potato cyst nematode, whether this is between countries, between farms or between sites in one field. Potato cyst nematodes probably spread to Europe through trade and the movement of potato tubers and soil adhering to them from other continents. Most countries have quarantine organizations that inspect potato shipments to protect their own countries from inadvertent importation of pests and diseases.

Physical barriers also tend to isolate pests in local areas, for example, deserts and rivers may isolate pests. Trade is the most common probable simple cause of new infestations of plant parasitic nematodes (Parker, 2000). Farmers are made are made aware of the risk of moving contaminated matter from one site to another on machinery, and of the need for preventive measures such as not sharing machinery between farms without thorough washing, cleaning and disinfestation first. Some natural movement cannot be controlled, for instance topsoil blown by strong winds from field to field, or infected topsoil moved by flood water onto clean sites. Animal manure has also been shown to contain viable cysts; the ingestion of the cyst appears not to impair its reproductive ability so can provide the means for new infestations to arise.

The following prevention methods can be used:

1. Check that machinery is thoroughly clean and free from plant debris.
2. Do not return soil that may contain potato cyst nematode to fields.
3. Clean the soil from potato tubers and have the soil tested to be sure that potato cyst nematodes are not transferred.
4. Make sure that the agency that tests the soil is competent and tests 500 g of soil per sample.
5. Grow susceptible and resistant potato cultivars alternately, thus reducing the possibility of selecting a highly virulent or new pathotype.

Crop Rotation

Crop rotation is frequently used to reduce population densities of potato cyst nematode. The major commercial hosts of the two potato cyst nematode species are in the plant family Solanaceae, namely potato, tomato and aubergine, all important cash crops. Where these crops are grown in monoculture for several seasons in infested soil, nematode densities increase to extremely high levels and crop yields become uneconomic. To reduce nematode population densities, non-host crops such as barley are grown between host crops (Whitehead, 1995). The length of the rotation and the crops used can have variable effects on the yield and the potato cyst nematode density. In South American countries, slightly different regimes are used and may include fallow, with intervening crops of lima beans, maize, barley or wheat. The annual decline rate in soil of G. pallida is, in general, slower than that of Globodera rostochiensis. When the reduction of potato cyst nematode is too slow by rotation alone, other additional methods can be used; for example, trap cropping can hasten the reduction of population densities.

Trap Cropping

Trap cropping is a simple method that has been used successfully for the reduction of cyst nematode populations (Halford et al., 1999). Sufficient crop growth time is allowed for the nematodes to penetrate the roots and develop into young adults (5-6 weeks), but not enough time for them to form new eggs. Potato cyst nematode populations can be reduced very quickly as long as the grower removes and destroys the crop, including the nematodes in the roots. If left too late, the nematode density will increase but, if the crop is removed in time, the nematode density is reduced and there will be a significant yield benefit for any subsequent potato crop. G. pallida can be reduced by as much as 80% per annum and even greater reductions were found when ethopropos was used in the soil before the first of two potato trap crops; almost 100% control was achieved (Mugniery and Balandras, 1984). The use of other non-tuberous solanaceous plant species to stimulate hatching has proved very efficient in Dutch studies. Non-hosts that are well adapted to temperate conditions, in this case Solanum sisymbrifolium, proved capable of inducing large hatches of potato cyst nematode juveniles. Solanum sisymbrifolium is fully resistant to potato cyst nematode, therefore eliminating the risk of increasing potato cyst nematode density (Scholte, 2000). 

The use of 10 potato clones as trap crops has been tested in field trials in Northern Ireland (Turner et al., 2006) and their potential for the organic market has also been shown. Non-hosts that are well adapted to temperate conditions, in this case S. sisymbriifolium, proved capable of inducing large hatches of potato cyst nematode juveniles. S. sisymbriifolium is fully resistant to potato cyst nematodes, thus eliminating the risk of increasing potato cyst nematode density (Scholte, 2000). A note of caution: it is important to use the correct seed accession number as Stelter (1987) recorded lines no.72 and 121 as poor hosts, although producing fewer than 5 cysts per pot.

Soil Solarization

Solarization is a good method of killing nematodes in hot climates. The soil is covered with two layers of polyethylene sheeting, allowing the soil underneath to heat up to temperatures of 60°C or more. In cooler climates solarization is much less effective.

Resistant Cultivars

Certain European cultivars of potato have resistance (often only partial) to European pathotypes of potato cyst nematode but some South American populations are more virulent than European populations and are able to overcome the resistance in European cultivars (Kort and Jaspers, 1973; Turner et al., 1995). Thus, strict quarantine measures remain essential. Studies at the International Potato Centre (CIP) in Lima, Peru, on 3000 accessions of potato, have focused on the two locally predominant pathotypes of G. pallida: P4A and P5A. A more virulent pathotype (P6A) has emerged and been selected in some areas. Variety of cultivars (tolerant, resistant and partially resistant) has an important part to play in maintaining an acceptable balance of pathotypes. For example, Maris Piper is a popular potato cultivar in the UK and has full resistance to UK populations of G. rostochiensis but no resistance to G. pallida. Its widespread cultivation has selected G. pallida and it is now recognized that other types of cultivars (e.g. tolerant ones) should be included in the rotation to avoid this problem. Some potato cultivars with high resistance to G. pallida are grown in Europe and others are currently being developed. For example, Karaka (Anderson et al., 1993) and Gladiator (Genet et al., 1995) both have high resistance to both species of potato cyst nematode. Other cultivars with desirable qualities are listed in Whitehead (1998). UK populations of G. pallida are genetically more diverse than UK populations of G. rostochiensis. Resistance to G. pallida is usually polygenic and only partial, as in the cultivars Santé and Morag. Another problem in introducing new cultivars of potato is persuading retailers and consumers of the value and desirability of those cultivars.

Biological Control

Biological control agents active against potato cyst nematode are currently the subject of intense study. Although several parasites of eggs and females have been identified, none has given consistent control (Crump, 1987). Soils suppressive to potato cyst nematode have been identified (Roessner, 1986; Crump, 1998) and the fungal causal agents isolated. Selected isolates of Verticillium chlamydosporium, Paecilomyces lilacinus and Acremonium sp. show considerable potential and methods for their production, formulation and application are being evaluated. Natural parasites and biological control are being studied in order to identify natural agents for potato cyst nematode control, without needing to use the toxic chemicals currently in use. These methods will integrate with a variety of strategies such as trap cropping and rotation in sustainable management systems. This work began in the late 1930s (Linford et al., 1938) and still continues (Crump and Flynn, 1995; Segers et al., 1996).

The majority of studies in the late 1990s have concentrated on the fungal control agents Verticillium, Hirsutella and Arthrobotrys, and the bacterium Pasteuria. Several workers (e.g. Roessner, 1986) have studied biological control of G. rostochiensis in pots and in vitro. This work is difficult to transfer to the field for several reasons. For example, the form and volume in which to apply the control agent must be decided, and how the inoculum reacts to the microbial population already present in the field must be determined. Verticillium chlamydosporium will infect young females in pots but is less effective when potatoes are grown in the presence of low nematode population densities.

Very few data are available on the effectiveness of biological control in the field. This is due in part to the logistics of such operations, such as producing sufficent inoculum. It is also known that some tests do not produce the expected results for reasons as yet undefined, but they are probably related in some way to the physiology and ecology of the host parasite relationship. Progress in the area of biological control requires a better understanding of the population dynamics of potato cyst nematode and their parasites (Davies, 1998; Davies et al., 1991). A number of factors interact, such as plant host, the action of root exudates, soil type and the mode of parasitism of the control micro-organism at any one point in time. Also, potato cyst nematode may be more susceptible to infection by any one fungus at different points in its life- cycle. For example, the three major fungal parasites V. chlamydosporium, Fusarium oxysporum and Cylindrocarpon destructans, have all been detected at different times in the nematode life cycle but the most active of the three depends on the life-stage present (Crump, 1987). 

The fungi, Paecilomyces lilacinis, Pochonia chlamydosporia and Monographella cucumerina may be used to aid control in PCN infested areas, but not used as the only method of control as field data suggests that the reduction in PCN populations is only around 60%. M. cucumaria is available commercially (MeloCon WG and BioAct WG - approved in the USA).

Some isolates of the bacteria Pasteuria penetrans can reduce populations of PCN. Applications are made during rotation of non-potato crops or before sowing potato to trigger a reduction in population density. Pasteuria penetrans is commercially available for root-knot nematodes. (Nematech Ltd., Tokyo).

Integrated pest management schemes benefit from the inclusion of a biocontrol agent, but, to date, no biocontrol agent can offer full protection on its own. Mutualistic bacteria and fungal endophytes are probably common in the agroecosystem (Sikora, 2007) but, to exploit potential candidates, a necessary objective for the future, is to understand the complicated manner in which they interact. The need to identify the mechanisms of control, how they function and then to scale up the technology for use commercial use in the field will take time.

A novel biological nematicide DiTera®, produced by Valent Biosciences Corp., USA, which has already been shown to control other plant parasitic nematodes in the field such as Xiphinema spp. and Radopholus spp., seems to have the capability to prevent hatching of potato cyst nematode in a specific manner. The specificity is linked to the permeability of the eggshell membrane. After testing DiTera® in solutions of 1 to 10 %, all were found to inhibit the hatching of the eggs. Meloidogyne incognita was used as a control and hatching of its eggs was not inhibited by DiTera® (Twomey et al., 2000).

Chemical Control

Kuhn first used chemicals as a nematode control method in 1881, but chemicals were not used extensively for this purpose until 1943 (Carter, 1943). The first attempts used D-D (1,2-dichloropropane - 1,3-dichloropropene mixtures). This led to other chemical control agents, such as chloropicrin.

The oximecarbamates are more effective in the early stages of plant growth, as the nematodes must hatch first. G. pallida is more difficult to manage than G. rostochiensis because it hatches over a longer period of time and can therefore escape as nematicidal activity is gradually lost (Whitehead,1975).

In 1991, Mazin suggested that chemical control is more effective where resistant cultivars are used. Nematicides do not prevent PCN build up, merely avoid yield loss (Tiilikkala, 1991). Fumigant nematicides are toxic and expensive, but their use is sometimes essential to keep PCN population densities low or beneath the damage threshold (ca 2 eggs/g of soil). Soil fumigants can kill large numbers of nematodes, especially in moist sandy soils under polythene sheeting. Soil fumigants are injected into the soil, usually in the autumn. The excessive use of all pesticides is currently discouraged on environmental grounds. It may be better to concentrate chemical applications on hot spots in a field in combination with other methods which, when combined, will lead to a lower population density of potato cyst nematode in the field (Been and Shomaker, 1998).

Non-fumigant nematicides are used in smaller amounts then fumigants but usually persist in the soil as long as fumigants. They are applied as granules in broadcast, row or narrow band treatments at the time of planting. In some cases a second application may be made at mid-season.

For further information, see Whitehead (1998) and Haydock et al. (2006).

 

18/03/2008 Updated by:

Janet Rowe, IACR-Rothamsted, Rothamsted Experimental Station, Harpenden, Hertfordshire, AL5 2JQ, UK