EPPO Global Database

Globodera pallida(HETDPA)

EPPO Datasheet: Globodera pallida

Last updated: 2022-10-12

IDENTITY

Preferred name: Globodera pallida
Authority: (Stone) Behrens
Taxonomic position: Animalia: Nematoda: Chromadorea: Rhabditida: Heteroderidae
Other scientific names: Heterodera pallida Stone
Common names in English: pale potato cyst nematode, white potato cyst nematode
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Notes on taxonomy and nomenclature

In 1973, a new potato cyst nematode (PCN) species, Heterodera pallida, was described from potato in Lincolnshire, England (Stone, 1973a). Before then, most records and technical data refer to H. rostochiensis sensu lato, which included both species, so it is not always possible to determine which species was referred to in earlier publications. To accommodate the potato cyst nematodes and related species which have round cysts, Skarbilovich (1959) erected the subgenus Globodera which was later elevated to generic status by Behrens (1975) (see also Mulvey & Stone, 1976). 

Recently, distinct genetic differences among Globodera pallida populations spanning Europe and other regions, and those found in South America were revealed by Subbotin et al. (2020). Picard et al. (2007) also discovered that populations from South America have a greater genetic diversity. Two groups of South American G. pallida populations with large genetic diversity including the ‘pallida Chilean type’ were identified, suggesting this may be a cryptic species within a possible G. pallida complex. Further integrative taxonomical research, including high throughput sequencing (HTS), morphological and behavioral studies are required in order to clarify this (Thevenoux et al., 2019).

EPPO Categorization: A2 list
EU Categorization: A2 Quarantine pest (Annex II B)
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EPPO Code: HETDPA

HOSTS 2022-09-26

The host range of G. pallida is limited to plants of the Solanaceae family. Potato (Solanum tuberosum) is by far the most important host crop. On tomato (S. lycopersicum) and eggplant (S. melongena), no economic damage has been reported (EFSA, 2019). Over 130 Solanum spp., including their hybrids and weeds, can be potential host plants as well as a few other species of Datura, Hyoscyamus, Lycopersicon, Physalis, Physochlaina, Salpiglossis and Saracha, all belonging to the Solanaceae family (Sullivan et al., 2007).  

Both G. pallida and G. rostochiensis have several different pathotypes (Kort, 1974). The pathotypes are characterized by the ability of the population to multiply on certain tuberous Solanum clones and hybrids used in breeding, with a mixture of qualitative and quantitative resistances. Some of these pathotypes are recognized by their almost total inability to multiply on specific potato cultivars (single-gene resistance); for example, commonly grown resistant potato cultivars (based on gene H1 deriving from clones of S. tuberosum subsp. andigena) are resistant to pathotype Ro1 and Ro4 of G. rostochiensis only. Other pathotypes show different levels of ability to multiply on different cultivars; this method is discussed by Mugniéry et al. (1989). In Europe Kort et al. (1977) proposed a scheme with three G. pallida pathotypes (Pa1-Pa3) and with five G. rostochiensis pathotypes (Ro1- Ro5). In South America Canto Saenz & de Scurrah (1977) developed another scheme, recognizing more pathotypes. 

Despite general acceptance, both pathotype schemes are considered insufficient for testing potato varieties for resistance to potato cyst nematodes. Variation in virulence in many European G. pallida populations with respect to quantitative resistance derived from S. vernei and other selected sources of Solanum species cause problems. Due to the extensive heterogeneity of some populations and environmental influences these populations could not be reliably described as pathotypes (Phillips and Trudgill, 1998; Turner and Subbotin, 2013). In Europe, it is generally accepted that only Pa1 and Ro1 are clearly separable pathotypes and the others are seen as overlapping populations. Nevertheless, the ‘European’ scheme is still used in many countries as it is the only available tool for the selection and assessment of PCN resistant potato cultivars as for example in EPPO Standard PM 3/68 (3) Testing of potato varieties to assess resistance to Globodera rostochiensis and Globodera pallida (2021). In practice, field populations often contain mixtures of species which makes separation or characterization very difficult.

Host list: Solanum lycopersicum, Solanum melongena, Solanum tuberosum

GEOGRAPHICAL DISTRIBUTION 2022-09-26

The area of origin of the two species G. pallida and G. rostochiensis is in the Andes Mountains in South America from where they were introduced to Europe with potatoes, probably in the mid-19th century. From there, they were spread with seed potatoes to other areas. 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. 

Research on mitochondrial sequences and microsatellite markers identified the more precise origin of western European G. pallida which is located in southern Peru, between Lake Titicaca and the city of Cusco (Plantard et al., 2008). Analysis of the mtDNA haplotype distribution of PCN populations from all over the world (Subbotin et al., 2020) confirmed this, and for each of the two species, G. pallida and G. rostochiensis, a different centre of origin was suggested in the Andes.

EPPO Region: Algeria, Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, Czech Republic, Denmark, Estonia, Finland, France (mainland), Germany, Greece (mainland, Kriti), Hungary, Ireland, Italy (mainland, Sicilia), Luxembourg, Malta, Morocco, Netherlands, Norway, Portugal (mainland, Madeira), Romania, Serbia, Slovakia, Slovenia, Spain (mainland, Islas Baleares, Islas Canárias), Sweden, Switzerland, Tunisia, Türkiye, United Kingdom (Channel Islands, England, Northern Ireland, Scotland, Wales)
Africa: Algeria, Kenya, Morocco, Tunisia
Asia: India (Himachal Pradesh, Jammu & Kashmir, Kerala, Tamil Nadu, Uttarakhand), Japan (Hokkaido), Pakistan
North America: Canada (Newfoundland), United States of America (Idaho)
Central America and Caribbean: Costa Rica, Panama
South America: Argentina, Bolivia, Chile, Colombia, Ecuador, Falkland Islands, Peru, Venezuela
Oceania: New Zealand

BIOLOGY 2022-09-26

G. pallida is a sedentary endoparasite. Second-stage juveniles (J2) hatch from eggs within cysts in the soil, under stimulus from root exudates of Solanaceae, and penetrate the root behind the growing root tip and move into the cortical region. Reaching the pericycle, the J2 penetrates a single cell and injects secretions which induce the formation of a large, multinucleate feeding structure, a syncytium, formed by dissolution of adjacent cell walls. The nematode remains here for the rest of its development, as it passes through two more juvenile stages to become either male or female. Females swell and break through the root surface but remain attached and white. The vermiform males leave the root and are attracted to females that exude sex pheromones. Many males may surround each female and multiple matings occur. Males live only a few days. After copulation the females remain on the roots while 200-500 eggs develop within them. When the females die and mature into cysts, their skin hardens and turns brown to become a protective cover around the eggs within. At this point they generally drop from the surface of the root into the soil. In temperate climate regions, G. pallida usually has one generation per year. The life cycle is completed in 40-60 days (Stelter, 1971; Stone, 1973b; Jones & Jones, 1974, Subbotin et al., 2010).

Soil temperature has an influence on the development of G. pallida. It is adapted to develop at colder temperatures than G. rostochiensis. Optimum hatching of the J2 from the eggs occurs between 13-25°C, hatching starts at 5°C (Kaczmarek et al., 2014). Above 17.5°C, however, reproduction, number of females per plant and their fecundity, decreases (Jones et al., 2017). G. pallida hatches more slowly than G. rostochiensis, over a longer period and has overall a higher number of eggs which hatch successfully compared to G. rostochiensis (Den Nijs and Lock, 1992; Kaczmarek et al., 2014). 

Cysts can remain dormant for many years (20 years or more) in the absence of solanaceous hosts, whereas second-stage juveniles have a much shorter survival time (weeks) when no hosts are present. For many years, a natural decline of 30-35% per year was assumed. Recently, it has become known that the type of soil affects this decrease: In sandy and peaty soils, the average decline in the first year after potato cultivation is much higher than in marine clay and loamy soils (69% vs 26%). In marine clay and loamy soils G. pallida populations also declined faster than G. rostochiensis populations (Been et al., 2019).

DETECTION AND IDENTIFICATION 2022-09-26

Symptoms

The symptoms caused by G. pallida are not specific. Patches of poor growth occur generally in the crop, sometimes with stunting, yellowing, wilting or death of the foliage. The tuber size of infested plants can be reduced, even with minor symptoms on the foliage. Roots display extensive branching, causing more adherence of the soil to the root system. In case of heavy infestation, the crop dies prematurely. 

Morphology 

Second-stage juveniles are vermiform and motile, 484 (440 – 525) µm long, having a well-developed stylet 23.8 (22-24) µm with robust and hooked knobs of 4-5 µm width with distinct forward projections and a pointed tail. Males are similar in general appearance, on average about 1200 µm long with a short and bluntly rounded tail terminus. Females are white or creamy coloured and spherical with a projecting neck, diameter approximately 450 µm (Stone, 1973a; 1973b, Brzeski, 1998). The cysts are smoothly rounded, no terminal cone, with a tanned skin. Vulval region consists of a single circumfenestration. The number of cuticular ridges between anus and vulva ranges from 8 - 20, generally lower than 14. Granek’s ratio is 1.2 - 3.5, generally lower than 3 (Baldwin & Mundo-Ocampo, 1991, Flemming and Powers, 1998).

Morphological identification of the three similar PCN species; G. pallida, G. rostochiensis and G. ellingtonae can only be done by well-trained persons, considering the high intraspecific variation and overlap between the species. Morphological as well as morphometric characteristics, including the number of cuticular ridges between anus and fenestra, Granek’s ratio, stylet length and shape of stylet knobs, need to be examined. G. pallida differs from G. rostochiensis as it has white rather than yellow-coloured females, a longer J2 stylet length (24 vs 22 µm) and a robust and square-hooked stylet knob (rather than small and rounded). 

Detection and inspection methods

Specific guidance on the sampling of soil and potato tubers is given in the EPPO Standards PM 9/26 National regulatory control system for Globodera pallida and Globodera rostochiensis (EPPO, 2018), PM 3/71 General crop inspection procedure for potatoes (EPPO, 2007) and PM 3/75 Globodera rostochiensis and Globodera pallida: sampling soil attached to ware potato tubers for detection prior to export and at import (EPPO, 2014). Detection of the young cysts by lifting potato plants is only possible for a short period when females mature into cysts. When inspected too late, cysts can easily fall off when lifting the plants. Females and young cysts are just visible to the naked eye and look like tiny white or brown pin-heads on the root surface. Low-level infestations in the field are very difficult to detect visually, they cause no patchy growth of the potato crop. Sufficient soil sampling in a systematic manner is necessary to ensure that no infestation is present in the field. In addition, for detection or surveys, sampling of tare soil or the soil brushed off from the potatoes can be done (Viaene et al., 2016). 

Nematode extraction (Southey, 1986) and identification should be carried out according to EPPO Standards PM 7/119 (EPPO, 2013) and PM 7/40 Diagnostic protocol for Globodera rostochiensis and G. pallida (EPPO, 2021b) providing all relevant morphological information and molecular methods for an accurate identification. Combining morphological and molecular methods is highly recommended, especially when new introductions are suspected. Molecular methods such as PCR, real-time PCR, HTS or Sanger sequencing must be used intelligently, taking into account the distinctive features of the test or method. For high-throughput diagnosis it is possible to use the real-time PCR method of Reid et al. (2015) based on detection and identification of floats from the extraction machine. DNA-based methods do not discriminate between dead or live eggs and juveniles. Molecular determination of the viability combined with identification can be done with the RNA-specific real-time PCR of Beniers et al. (2014).

PATHWAYS FOR MOVEMENT 2022-09-26

G. pallida has limited potential for natural movement; second-stage juveniles can move short distances in the soil when attracted towards roots, at most only 1 m per year and dry cysts can be dispersed to adjoining fields by wind or water. The main routes of spread are infested seed potatoes and movement of contaminated soil on non-host plants such as plants for planting, nursery stock and flower bulbs, farm machinery, ware potatoes or any other plant parts intended for consumption or processing. The latter are only important if there is a risk of these being planted or if care is not taken with disposal of waste soil. Soil as such and tare soil is also a pathway (EPPO, 2018).

PEST SIGNIFICANCE 2022-09-26

Economic impact 

Potato cyst nematodes are major pests of the potato crop in cool and temperate areas, losses have been estimated within Europe at 9% of total potato production; and in other potato growing areas where less or no control strategies are used, almost total losses can occur (Turner and Subbotin, 2013). This is particularly the case when, because of the pathotypes present, only a few resistant cultivars are commercially available for planting. Most popular cultivars have no resistance against G. pallida. 

The amount of damage, particularly in relation to the weight of tubers produced, is closely related to the number of nematode eggs per unit of soil. It has been estimated that approximately 2 tonnes/ha of potatoes are lost for every 20 eggs/g soil (Brown, 1969). Up to 80% of the crop can be lost when nematode populations increase to very high levels due to repeated cultivation of potatoes. The damage threshold can be as low as 1-2 eggs/g soil, depending on environmental conditions and level of tolerance of the grown cultivar. In addition to yield loss, there is also an indirect impact due to costs for control and phytosanitary measures. Online decision tools as ‘Nemadecide’ were developed to help growers to keep PCN at low, economically acceptable density levels (Been et al., 2006). 

Control 

Control is traditionally by crop rotation, as it is recognized that after several years in the absence of potato cultivation the population of nematodes will be reduced to below the damage and detection thresholds; 6-7 years without potatoes is a common recommendation. Other more recent field management practices for limiting the population are; use of resistant potato crops and trap crops as sticky nightshade (S. sisymbriifolium), biofumigation techniques, inundation or early destruction of susceptible potato crops before the life cycle has completed. In addition, good farm hygiene, including cleaning equipment and machinery, and reduction of growth of volunteer potato plants in the field is necessary (EPPO, 2020), in combination with regular testing for the presence of PCN and the use of suitable potato cultivars for effective deployment of the resistance (Molendijk and de Jongh, 2018).

In the last decade great progress had been made in the breeding of resistant potato varieties despite the fact that identification of a single major resistance gene is very difficult due to the high genetic diversity of the European G. pallida populations. No single gene offers complete resistance, (unlike the H1 for G. rostochiensis). A small number of partially or high resistant potato cultivars such as Innovator, Arsenal and Ivetta are currently on the market. However, Innovator is intolerant, not growing well when higher populations densities are present. Innovator and Arsenal are limited to the processing market, but Ivetta is also suitable for cooking.

Control in tomato crops is chiefly by soil fumigants.

Phytosanitary risk 

In the EPPO region G. pallida is already established in most areas that are important for the cultivation of ware and starch potatoes; and regular attention to control is needed in such areas. G. pallida is still absent from some areas or EPPO countries; in particular in some seed potato production areas, which should be kept as free as possible from this nematode. New introductions would have a high probability of establishing a viable population in areas where potatoes are grown (EFSA, 2012). 

Additionally, the introduction of new virulent populations by import of non-European populations, particularly South American populations, would pose a threat to the use of resistant cultivars as major tool in controlling G. pallida. The inability to precisely link genetic variability to the virulence characteristics of a specific nematode population, and quickly identify the virulence status of intercepted populations for inspection purposes, strengthens the need to prevent their introduction (Hockland et al., 2012). New virulent populations can also arise from selection pressure as effect of intensive cropping presents risks, as recently occurred in Germany and the Netherlands (EFSA, 2020). The German population ‘Oberlangen’ showed a higher reproduction and fitness than ‘Chavornay’, the standard Pa3 reference population. The resistance response of potato cultivar ‘Seresta’, restricting the development of a syncytium, only imposed a partial effect on the Oberlangen population, evident by the number of juveniles developing into females (Mwangi et al., 2019).

In contrast to plants for planting, soil associated with potatoes, as tare soil, and root crops for packing or processing is mostly not regulated or only rarely regulated. Combined with the increasing use of the same machinery on multiple farms e.g. between sugar beet and potato farms and the renting of land that belongs to different farms increases the risk of the spread of G. pallida. Recommendations are available in EPPO Standard PM 3/92 Management of phytosanitary risks for potato crops resulting from movement of soil associated with root crops and potatoes (EPPO, 2021) to better address the risk associated with this pathway.

PHYTOSANITARY MEASURES 2022-09-26

Measures to prevent the introduction of G. pallida to areas where it is not already established include soil sampling surveys and regulations concerning movement of seed potatoes, nursery stock, flower bulbs and soil. These apply nationally as well as internationally. 

Specific requirements are recommended in EPPO Standard PM 8/1 Commodity-specific phytosanitary measures for Potato (EPPO, 2017) for seed potatoes (except micropropagative material and minitubers) and ware potatoes to be imported from third countries. In this Standard, seed potatoes should come from fields free from viable cysts of G. rostochiensis and G. pallida according to PM 9/26. Ware potatoes from non-EPPO countries where G. pallida or G. rostochiensis occur should come, under transitional arrangements, from a pest free area and origin from a pest-free potato production and distribution system for the respective pests according to EPPO Standard PM 3/61 (EPPO, 2019), and confirmation by inspection or testing of tubers on import that the respective pest(s) does not occur. 

For several EPPO countries, seed potatoes, the major pathway for entry, is already closed. For example, in the EU, the implementation regulation 2019/2072 prohibits import of seed potatoes and plants for planting of stolon- or tuber-forming species of Solanum L. or their hybrids. 

Additional safeguards during transit of consignments could be washing of tubers and flower bulbs to remove soil, although it should be noted that cysts can remain embedded in tubers, especially in the eyes.

Measures to contain or eradicate G. pallida are described in the national regulatory control system PM 9/26 (EPPO, 2017). The regulatory control system was developed for potato but can be applied to other crops as well, with possible slight modifications depending on the crops.

REFERENCES 2022-09-26

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Been TH, Schomaker CH & Molendijk LPG (2006) NemaDecide, a decision support system for the management of potato cyst nematodes. In Proceedings of the 28th International Symposium of the European Society of Nematologists, 5-9 June, Blagoevgrad (BG). 

Been T, Schomaker C & Molendijk L (2019) Natural decline of potato cyst nematodes in the Netherlands. Aspects of Applied Biology 142, 55-58.

Behrens E (1975) [Globodera Skarbilovich, 1959 an independent genus in the subfamily Heteroderinae Skarbilovich, 1949 (Nematoda: Heteroderidae)]. Vortragstagung zu Aktuellen Problemen der Phytonematologie No. 1, pp. 12-26. 

Beniers JE, Been TH, Mendes O, van Gent-Pelzer MPE & van der Lee TAJ (2014) Quantification of viable eggs of the potato cyst nematodes (Globodera spp.) using either trehalose or RNA-specific Real-time PCR. Nematology 16, 1219-1232.

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EFSA (2020) Grenier E, Kiewnick S, Smant G, Fournet S, Montarry J, Holterman M, Helder J & Goverse A. Monitoring and tackling genetic selection in the potato cyst nematode Globodera pallida. EFSA supporting publication 2020:EN-1874. 25 pp. https://doi.org/10.2903/sp.efsa.2020.EN-1874 

EPPO (2007) EPPO Standard PM 3/71(1) General crop inspection procedure for potatoes + corrigendum. EPPO Bulletin 37, 592-597. 

EPPO (2013) EPPO Standard PM 7/119 (1) Nematode extraction. EPPO Bulletin 43, 471-495.

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EPPO (2017) EPPO Standard PM 8/1 (2) Commodity-specific phytosanitary measures for potato. EPPO Bulletin 47, 487-503.

EPPO (2018) EPPO Standard PM 9/26 (1) National regulatory control system for Globodera pallida and Globodera rostochiensis. EPPO Bulletin 48, 516-532.

EPPO (2019) EPPO Standard PM 3/61 (2) Pest-free areas and pest-free production and distribution systems for quarantine pests of potato. EPPO Bulletin 49, 480-481.

EPPO (2020) EPPO Standard PM 3/89 (1) Control of volunteer potato plants. EPPO Bulletin 50(3), 372-382. 

EPPO (2021) EPPO Standard PM3/68 (2) Testing of potato varieties to assess resistance to Globodera rostochiensis and Globodera pallida. EPPO Bulletin, 51, 404-405

EPPO (2022) Diagnostic protocol PM 7/40 (5) Globodera rostochiensis and G. pallida. EPPO Bulletin, 52, 286-313.

EU (2007) Council Directive 2007/33/EC of 11 June 2007 on the control of potato cyst nematodes and repealing Directive 69/465/EEC. Official Journal of the European Union L 156, p. 12-22. Available at https://eur-lex.europa.eu/legal-content/EN/ALL/?uri=CELEX:32007L0033

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Jones LM, Koehler A-K, Trnka M, Balek J, Challinor AJ, Atkinson HJ & Urwin P (2017) Climate change is predicted to alter the current pest status of Globodera pallida and Globodera rostochiensis in the United Kingdom. Global Change Biology 23, 4497-4507. 

Kaczmarek A, MacKenzie K, Kettle H & Blok V (2014) Influence of soil temperature on Globodera rostochiensis and Globodera pallida. Phytopathologia Mediterranea 53, 396-405.

Kort J (1974) Identification of pathotypes of the potato cyst nematode. EPPO Bulletin 4, 511-518. 

Kort J, Ross H, Rumpenhorst HJ & Stone AR (1977) An international scheme for the identification of pathotypes of potato cyst nematodes Globodera rostochiensis and G. pallida. Nematologica 23, 333-339.

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Stone AR (1973a) Heterodera pallida n. sp. (Nematoda: Heteroderidae), a second species of potato cyst nematode. Nematologica 18, 591-606. 

Stone AR (1973b) Heterodera pallida and Heterodera rostochiensis. CIH Descriptions of Plant parasitic Nematodes. 16 and 17. CAB International, Wallingford (UK). 

Subbotin SA, Franco J, Knoetze R, Roubtsova TV, Bostock RM & Prado Vera IC del (2020) DNA barcoding, phylogeny and phylogeography of the cyst nematode species from the genus Globodera (Tylenchida: Heteroderidae). Nematology 22, 269-297.

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Sullivan MJ, Inserra RN, Franco J, Moreno-Leheudé I & Greco N (2007) Potato cyst nematodes: Plant host status and their regulatory impact. Nematropica 37, 193-201.

Thevenoux R, Folcher L, Esquibet M, Fouville D, Montarry J & Grenier E (2020) The hidden diversity of the potato cyst nematode Globodera pallida in the south of Peru. Evolutionary Applications 13, 727-737. 

Turner SJ & Subbotin SA (2013) Cyst nematodes, pp 109-143. In Plant Nematology, 2nd edn. (eds Perry RN & Moens M), CAB International, Wallingford (UK). 

Viaene N, Deeren A-M, Goeminne M, Dupont P, Demeulemeester K, Lanterbecq D & De Proft M (2016) An alternative way of soil sampling for detection of field infestations with Globodera spp. In Abstract Book of the 32nd Symposium of the European Society of Nematologists, p 155 Braga (PT).

Viaene N, Ajmal B, Bighiu A, Damme N & De Sutter N (2019) Exploring heating of potato cysts as a method to disinfest soil. 5th Symposium of Potato Cyst Nematode Management. Aspects of Applied Biology 142, 95–102.

ACKNOWLEDGEMENTS 2022-09-26

This datasheet was extensively revised in 2022 by Evelyn van Heese (NVWA, NL). Her valuable contribution is gratefully acknowledged.

How to cite this datasheet?

EPPO (2022) Globodera pallida. EPPO datasheets on pests recommended for regulation. Available online. https://gd.eppo.int

Datasheet history 2022-09-26

This datasheet was first published in the EPPO Bulletin in 1978 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2022. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1st and 2nd edition). CABI, Wallingford (GB).

EPPO (1978) EPPO Data Sheet on Quarantine Organisms no 124: Globodera pallida. EPPO Bulletin 8(2), 131-133. https://doi.org/10.1111/j.1365-2338.1978.tb02785.x