Regulated Non-Quarantine Projects

Two EU funded projects for the benefit of the whole EPPO region

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Justification for qualification based on EPPO PM 4 Standards
Justification for disqualification
Additional or non-conclusive information
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NAME OF THE ORGANISM: Phytophthora rubi (1PHYTG)


GENERAL INFORMATION ON THE PEST

Name as submitted in the project specification (if different):
 
Phytophthora

Pest category:
 
Chromista


1- Identity of the pest/Level of taxonomic listing:

Is the organism clearly a single taxonomic entity and can it be adequately distinguished from other entities of the same rank?
 
Yes

Is the pest defined at the species level or lower?:
 
Yes

Can listing of the pest at a taxonomic level higher than species be supported by scientific reasons or can species be identified within the taxonomic rank which are the (main) pests of concern?
 
  • Not relevant: Fruits (including hops) sector
If necessary, please list the species:
 
-

Is it justified that the pest is listed at a taxonomic rank below species level?
 
Not relevant

Conclusion:
 
  • Candidate: Fruits (including hops) sector
Justification (if necessary):
 
In the last twenty years climatic changes, like flooding or temperature increase, favour the spread and the settlement of the Phytophthora species. All species are plant pathogens that attack various parts of the plant including roots, crowns, stems, buds, flowers, fruits and leaves. Phytophthora species have a high evolutionary potential for environment adaptability: among others it is becoming increasingly evident that natural interspecific hybridization is a casual event in heterothallic Phytophthora evolution which could lead to an increase of virulence.
Moreover, for the generic detection and identification of these oomycetes, different molecular techniques are available. Historically ITS region have been used but more recently methods based on the ras/related protein Ypt1 gene have been set up (Schena et al., 2006: Schena et al. 2008). In particular Schena et al. 2008 have developed a ‘molecular tool box’ for the identification of a number of Phytophthora species; the method is specific for the genus and sensitive enough to detect target species in infected leaves and infested soil and water samples.
In the responses to the questionnaire, ES, EUROSEEDS, FR, LT and SI considered that Phytophthora was a pest of concern on Rubus. EUROSEEDS and SI supported listing at genus since several species are considered important and causing similar damage. ES, FR and LT supported listing at species level.
For example, SI indicated that the following species are infecting Rubus: P. cactorum, P. citricola, P. fragariae var. rubi (preferred name: P. rubi), P. plurivora, P. syringae, P. idaei. EUROSEEDS added P. bisheria.

Although Phytophthora spp. are difficult to distinguish visually in the field/glasshouse from each other, the Fruit SEWG commented that some species were important for Rubus and others not. Phytophthora spp. may be present everywhere, and testing for absence of Phytophthora spp. would not be relevant. Moreover, as indicated by Wilcox & Cooke (2017), some of the Phytophthora’s mentioned are a problem in the field and are not introduced by propagation material (on the contrary, P. rubi has a narrow host range). Phytophthora spp. may differ per climate zone, etc. In the past various Phytophthora spp. were reported from raspberry, and nowadays more options are available to correctly identify the Phytophthora spp. Authors remark more than once that the species they identified was at that time a heterogenous species. Many identified Phytophthora spp. have been reclassified. Duncan et al. (1987), Duncan (1990) already indicated that P. megasperma was most pathogenic, different from the non-pathogenic P. megasperma var megasperma, and is in the ATCC collection as P. rubi. It is wondered whether all the outbreaks in the 1980’s in Europe related to P. rubi. The Fruit SEWG recommended that the RNQP regulation covers P. rubi, indirectly covering other species of importance for Rubus.

Review of the importance of Phytophthora spp. in Rubus based on Wilcox & Cooke (2017) and some other publications:
- Worldwide, P. rubi is the most important and aggressive Phytophthora sp. on red raspberry and has been reported from North and South America, Europe, and Australia. Its host range is confined primarily to red raspberry, although there are occasional reports of attack on other Rubus spp. and hybrids, particularly when they are subjected to prolonged waterlogged conditions (Wilcox & Cooke, 2017) (Phytophthora clade 7a).
- P. megasperma has been reported from the United States, the United Kingdom, and Chile. Isolates from raspberry belong to the subgroup variously characterized as P. megasperma var. megasperma, the ‘broad host range’ subgroup, and more recently, P. megasperma sensu stricto. As indicated, such isolates appear to have a very broad host range, but on raspberry, they typically are found only in plantations or portions thereof subjected to prolonged periods of saturated soil (Wilcox & Cooke, 2017). (Phytophthora clade 6b)
- P. cactorum has been reported only occasionally from the United States and the United Kingdom. The species attacks a broad range of primarily woody hosts but does not appear to be highly virulent on raspberry. P. idaei is a raspberry-specific species, morphologically similar and closely related to P. cactorum, that has, to date, been reported only from the United Kingdom. Current studies suggest its virulence is similar to that of P. cactorum (Wilcox & Cooke, 2017). In Poland, P. cactorum strains, isolated from a strawberry field with crown and leather rot, were also pathogenic to raspberry (Meszka & Michalecka, 2016). (both Phytophthora clade 1a)
- P. citricola has been reported from the United States, the United Kingdom, eastern Europe, and Chile. The species has a wide host range, largely on woody plants (Wilcox & Cooke, 2017). In Poland, one P. citricola strain, isolated from a strawberry field with crown and leather rot, were also pathogenic to raspberry (Meszka & Michalecka, 2016). (Phytophthora clade 2c)
- P. cryptogea has been reported from the western United States, Australia, and Chile. As presently (2017) defined, it is a heterogeneous taxon encompassing a range of morphologically related types. All require pairing with an isolate of the opposite mating type to form oospores. Isolates recovered from rosaceous fruit crops (e.g., apple, stone fruits, raspberry) and kiwifruit vines in California (United States) and Chile appear to be closely related, cross-pathogenic on hosts within this group (in limited testing), and highly virulent (Wilcox & Cooke, 2017). (Phytophthora clade 8a)
- P. gonapodyides has been reported from the United States (as P. cryptogea sensu lato) and Chile. Moderately to highly virulent isolates of the species also have been recovered from a variety of deciduous fruit crops in cooler regions of central and eastern North America, and other isolates have been recovered from woody plants in northwestern North America and northern Europe (Wilcox & Cooke, 2017). In 2018 it was isolated from symptomatic raspberry plants in Canada (Burlakoti et al., 2023). The species is reported to be the most widely distributed Phytophthora species in natural (aquatic) habitats. P. gonapodyides is thought to exhibit a primarily saprophytic lifestyle, maintaining their populations in natural ecosystems by colonizing plant litter or through pathogenesis of fine-roots, but is known to act as an opportunistic pathogen (McGowan et al., 2023). (Phytophthora clade 6b)
- P. citrophthora has been reported only from a limited number of locations in Bulgaria and Chile. Unlike most other Phytophthora spp. that attack raspberry, vegetative growth is as strong at 30°C as it is at 20°C (Wilcox & Cooke, 2017). (Phytophthora clade 2a)
- P. cambivora has been reported from the United Kingdom (Wilcox & Cooke, 2017). (Phytophthora clade 7a)
- Although P. drechsleri has been reported (only) from the United Kingdom, subsequent work indicated that these isolates are more accurately identified as P. cryptogea. Hence, P. drechsleri is no longer considered a pathogen of raspberry at this time (Wilcox & Cooke, 2017).
- An indeterminate number of unidentified Phytophthora spp. have also been isolated from raspberry roots in various countries, although pathogenicity has been reported only occasionally (Wilcox & Cooke, 2017):
• P. bishii (formerly Phytophthora bisheria) (see Abad et al., 2023) has been reported from raspberry in 2008 (Abad et al., 2008), but no report from Rubus spp. since (CAB abstract search, 26/Aug/2024). (Phytophthora clade 2e)
• P. plurivora has been detected in raspberry in the UK (Brown et al., 2023), however it was a co-infection with P. idaei, P. ilicis, Phytopythium vexans and Pp littorale. Phytophtora spp. could not be isolated in contrast to the Phytopythium spp.; Phytopythium spp were able to induce symptoms in raspberry. Chistova (2020) isolated P. plurivora from a small river, the isolates was able to infect blackberry leaves, but was not able to infect blackberry cutting (by artificially inoculation). (Phytophthora clade 2c)
• P. syringae has been isolated from raspberry roots of red raspberry plants affected by severe root and crown rot with associated cane death. P. syringae however did not cause areal symptoms on artificially inoculated raspberry plants, unlike other Phytophthora spp. isolated at the same time (Duncan et al., 1987). There are no recent reports on P. syringae involved in raspberry root rot (CAB abstract search, 26/Aug/2024). (Phytophthora clade 3)
• P. pseudocryptogea has been isolated from soil from a field with four and five years old wilting raspberry in Bulgaria, showing color and root rot. There are no specifics on circumstances, e.g. information on waterlogging etc. (Phytophthora clade 8a)
• Remark on Phytophthora ramorum: Cultivated Rubus is not on the list of host plants for P. ramorum, the only reference found relates to Rubus spectabilis (salmonberry, a wild species) found in the vicinity of an infected tanoak (Oregon, USA, 2005). The species could be artificially (re)infected with P. ramorum, but it did not seem to become systemic. No reports since 2005 (Meekes, pers. communication, 2024).

Phytophthora clades:
Abad ZG, Burgess TI, Bourret T, Bensch K, Cacciola SO, Scanu B, Mathew R, Kasiborski B, Srivastava S, Kageyama K, Bienapfl JC, Verkleij G, Broders K, Schena L & Redford AJ (2023). Phytophthora: taxonomic and phylogenetic revision of the genus. Studies in Mycology 106(1), 259-348.

2 – Status in the EU:
 
Is this pest already a quarantine pest for the whole EU?
 
No

Presence in the EU:
 
Yes

List of countries (EPPO Global Database):
 
-

Conclusion:
 

Justification (if necessary):
 
Various Phytophthora spp. are present in Europe.

HOST PLANT N°1: Rubus (1RUBG) for the Fruits (including hops) sector.


Origin of the listing:
 
Commission Implementing Directive (EU) 2014/98/EU and Commission Implementing Regulation (EU) 2019/2072

Plants for planting:
 
Plants intended for planting


3 - Is the pest already listed in a PM4 standard on the concerned host plant?
 
Yes
 
Conclusion:
 
Qualified

 
Justification (if necessary):
 
EPPO Standard PM 4-10 Certification scheme for Rubus recommends testing for Phytophthora rubi and all other Phytophthora spp. infecting Rubus. The Standard indicates that it may be necessary to eliminate Phytophthora rubi or other Phytophthora spp., especially in cool and moist climates by micropropagation culture or using stem cuttings planted in soil-less or sterilized growing medium with testing.

4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
 
 
Conclusion:
 

 
Justification:
 
Phytophthora root rot of Rubus spp. appears to primarily affect red raspberry and some of its hybrids, but black raspberry (R. occidentalis) cultivars may also be infected by some species of the pathogen, although typically not so severely. Phytophthora root rot has not been documented on other Rubus spp. or their hybrids (Wilcox & Cooke, 2017); in generally, Phytophthora does not cause economic damage to blackberries (UC PMG, 2014).
Phytophthora species vary in their general levels of virulence to raspberry and the details of their symptomology, their levels of virulence to specific raspberry cultivars, host ranges and adaptation to specific environmental conditions. For example Phytophthora rubi and P. megasperma predominate in the cool and wet regions of Chile, whereas they are supplanted by P. cryptogea and P. citricola in production regions 1,000 km to the north, where conditions are hotter and drier (Wilcox & Latorre, 2002; Wilcox & Cooke, 2017). Although in Huelva in Spain P. rubi was also found in the complex of Phytophhora spp. causing raspberry root rot (Borrero et al., 2024).
There are several potential sources of primary inoculum, but their relative importance varies among species. For instance, some species (such as P. megasperma and P. cactorum) have wide host ranges, are virtually cosmopolitan in their distribution, and are likely to be present in many soils prior to the establishment of a new raspberry planting (Wilcox & Cooke, 2017). P. gonapodyides is reported to be the most widely distributed Phytophthora species in natural (aquatic) habitats and is thought to exhibit a primarily saprophytic lifestyle, maintaining their populations in natural ecosystems by colonizing plant litter or through pathogenesis of fine-roots, but is known to act as opportunistic pathogen (McGowan et al., 2023).
P. rubi has an extremely narrow host range. It is a potentially deadly pathogen and the most important Phytophthora sp. on raspberry worldwide. P. rubi is probably not present in soils where raspberry has not been grown previously (or those subject to contamination from raspberry sites), and therefore, seemingly must be introduced into new planting sites. Common means of introducing this and other Phytophthora spp. include the use of infected planting material or infested soil clinging to it, the movement of infested soil or runoff water from nearby contaminated sites, and the use of infested surface water for irrigation (Wilcox & Cooke, 2017). For P. rubi, Tabima et al. (2018) showed that populations of P. rubi from western USA were the likely source of pathogen migration to Europe.
Phytophthora is a soilborne pathogen that survives in the soil as a resting spore (oospore). When soils become saturated with water for prolonged periods, infectious motile spores (zoospores) are released into the soil and can infect raspberry roots or crowns. Phytophthora species other than P. rubi may be involved in root rot of raspberry. Not all root rots are due to Phytophthora. Raspberry roots are very sensitive to excessive moisture in the soil for long periods of time. Root death from lack of air can also occur and result in similar foliar and root decay symptoms (UC PMG, 2014).

5 - Economic impact:

Are there documented reports of any economic impact on the host?
 

Justification:
 
Phytophthora rubi is the most serious pathogen of raspberry worldwide, and it can result in complete crop losses, as large areas are completely killed (Wilcox and Cooke 2017). To establish raspberry plantations requires considerable capital investment, which is recovered over the life of the plantation, usually 10-15 years. This investment is lost if severe outbreaks occur within 2-3 years of planting. The disease is of great importance in France, Germany, Norway, Switzerland and the United Kingdom. In 2013, P. rubi was found in 90% of the surveyed raspberry fields in Washington state, with the potential of causing millions of dollars in losses to the industry annually (Gigot et al., 2013; Stewart et al., 2014) (cited from EPPO, 2022).

What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
 

Is the economic impact due to the presence of the pest on the named host plant for planting, acceptable to the propagation and end user sectors concerned?
 

Is there unacceptable economic impact caused to other hosts (or the same host with a different intended use) produced at the same place of production due to the transfer of the pest from the named host plant for planting?
 

Conclusion:
 

Justification:
 

6 - Are there feasible and effective measures available to prevent the presence of the pest on the plants for planting at an incidence above a certain threshold (including zero) to avoid an unacceptable economic impact as regards the relevant host plants?
 
 
Conclusion:
 

Justification:
 
Control programs should include the following components (Wilcox & Cooke, 2017):
- Exclusion: pathogen free plant material in healthy potting soil. This is especially important for P. rubi, a potentially deadly pathogen and the most important Phytophthora sp. on raspberry worldwide.
- Soil drainage and site modification
- Rubus species and cultivar selection: susceptibility to Phytophthora root rot varies widely among raspberry cultivars.

7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
 
 
Conclusion:
 

Justification:
 

CONCLUSION ON THE STATUS:
 
Recommended for listing as an RNQP, based on EPPO PM 4 Standards.


8 - Tolerance level:

Is there a need to change the Tolerance level:
 
No

Proposed Tolerance levels:
 

9 - Risk management measures:

Is there a need to change the Risk management measure:
 
Yes

Proposed Risk management measure:
 
the Fruit SEWG commented that, in addition to the rogueing out of the plants showing symptoms of Phytophthora spp. at the production site, the plants surrounding infected/symptomatic plants at the site of production should also be rogued out when production occurs in the fields (not when produced in containers e.g. pots). The area (radius) of neighbouring plants to be removed in the site of production should depend on the growing conditions/cropping system. As is already the case, sampling and testing in the field should only be performed in case of doubts.

Additional measures for Pre-basic, Basic and Certified material could include:
o Recording of cropping and soil borne disease history of fields;
o Rest period from host plants between findings of the pest and next planting.


REFERENCES:
  • Abad ZG, Abad JA, Coffey MD, Oudemans PV, Man in ’t Veld WA, de Gruyter H, Cunnington J & & Louws FJ (2008) Phytophthora bisheria sp. nov., a new species identified in isolates from the Rosaceous raspberry, rose and strawberry in three continents. Mycologia 100(1), 99-110.
  • Abad ZG, Burgess TI, Bourret T, Bensch K, Cacciola SO, Scanu B, Mathew R, Kasiborski B, Srivastava S, Kageyama K, Bienapfl JC, Verkleij G, Broders K, Schena L & Redford AJ (2023) Phytophthora: taxonomic and phylogenetic revision of the genus. Studies in Mycology 106(1), 259-348.
  • Borrero C, Pastrana AM, Ordóñez J, Paez JI, Orta MS & Avilés M (2024) Host range of Phytophthora spp. from berry crops in Huelva, Spain. Plant Disease [online abstract].
  • Burlakoti RR, Sapkota S, Lubberts M, Lamour K (2023) First report of Phytophthora gonapodyides causing root rot on raspberry in Canada. Plant Disease 107, 784. doi: 10.1094/PDIS-08-22-1940-PDN..
  • Christova PK (2022) Detection of Phytophthora gallica in Bulgaria and co-existence with other Phytophthora species in a small river. Journal of Plant Diseases and Protection 129(6), 1377-1387
  • Duncan JM, Kennedy DM & Seemüller E (1987) Identities and pathogenicities of Phytophthora spp. causing root rot of red raspberry. Plant Pathology 36(3), 276-289.
  • EPPO (2022) EPPO Datasheet: Phytophthora rubi. https://gd.eppo.int/taxon/PHYTFU/datasheet
  • Gigot J, Walters TW & Zasada IA (2013) Impact and occurrence of Phytophthora rubi and Pratylenchus penetrans in commercial red raspberry (Rubus idaeus) fields in northwestern Washington. International Journal of Fruit Science 13, 357-372.
  • McGowan J, O’Hanlon R, Owens RA & Fitzpatrick DA (2020) Comparative genomic and proteomic analyses of three widespread Phytophthora species: Phytophthora chlamydospora, Phytophthora gonapodyides and Phytophthora pseudosyringae. Microorganisms 8(5), 653.
  • Meszka B & Michalecka M (2016) Identification of Phytophthora spp. isolated from plants and soil samples on strawberry plantations in Poland. Journal of Plant Diseases and Protection 123, 29-36.
  • Stewart JE, Kroese D, Tabima JF, Larsen MM, Fieland VJ, Press CM, Zasada IA & Grünwald NJ (2014) Pathogenicity, fungicide resistance, and genetic variability of Phytophthora rubi isolates from raspberry (Rubus idaeus) in the western United States. Plant Disease 98(12), 1702-1708.
  • Tabima JF, Coffey MD, Zazada IA & Grunwald NJ (2018). Populations of Phytophthora rubi show little differentiation and high rates of migration among states in the western United States. Molecular Plant-Microbe Interactions 31(6), 614-622.
  • Wilcox WF & Cooke DEL (2017) Phytophthora root rot. In Compendium of Raspberry and Blackberry Diseases and Pests (eds Martin RR, Ellis MA, Williamson B & Williams RN). American Phytopathological Society, St Paul, MN, USA. pages 52-56.
  • Wilcox WF & Latorre BA (2002) Identities and geographic distributions of Phytophthora spp. causing root rot of red raspberry in Chile. Plant Disease 86, 1357-1362