| Legend |
|---|
| Justification for qualification based on EPPO PM 4 Standards |
| Justification for disqualification |
| Additional or non-conclusive information |
| Standard text |
NAME OF THE ORGANISM: Agrobacterium & Rhizobium (Ti-plasmid) (1AGRBG & 1RIZBG)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Agrobacterium
Pest category:
Bacteria
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?:
No
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?
- Yes: 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):
All available information points to the fact that the pathogenic character of agrobacteria depends on the presence of the tumour-inducing plasmid (Ti-plasmid) (Weisberg et al., 2023), although some genes in the chromosome may also have some degree of involvement (Knauf et al, 1982). It seems clear that the pathogenic character is conferred by the plasmid. The Ti plasmid is not a sufficient but a necessary condition; as in any disease, there are other factors (host, environment) that influence whether or not the disease occurs. If the plasmid is present, the probability of disease is very high; if the plasmid is not present, there will be no disease. Therefore, since many agrobacteria are present in the environment, and most of them are not pathogenic, neither the listing at genus nor at species level will give a good indication about disease development. Consequently, the Fruit SEWG recommended to consider the presence (or not) of the Ti-plasmid, to know if the probability of disease development will be very high or not. This was also supported by EUROSEEDS in responses to the questionnaire, also indicating that several Agrobacterium isolates are not causing diseases. A. tumefaciens, A. rhizogenes, A. rubi, A. vitis and several other species can carry a Ti-Plasmid that is the actual cause of symptomatic galls causing the disease.
In Rubus, different species are involved e.g. Agrobacterium tumefaciens, A. rhizogenes (currently considered as Rhizobium rhizogenes; Flores-Félix et al., 2020) and A. rubi. New species have also been isolated e.g. Agrobacterium arsenijevicii and Rhizobium tumorigenes. In the responses to the questionnaire, DE, ES, EUROSEEDS, FR, LT, NL, SI and SK considered that Agrobacterium was a pest of concern on Rubus. DE supported listing at genus since several species are considered important and causing similar damage. ES, FR, LT, NL and SK supported listing at species level. The Fruit SEWG suggested to consider the listing of all Agrobacterium & Rhizobium harbouring the Ti-plasmid.
In Vitis, crown gall is caused by Agrobacterium (e.g. A. tumefaciens) as well as Allorhizobium vitis, both belonging to the family Rhizobiaceae. Indeed, based on the analysis of the rrs, recA, atpD and rpoB genes, Mousavi et al. (2015) proposed to transfer Rhizobium vitis (initially Agrobacterium vitis) to the genus Allorhizobium (Flores-Félix et al., 2020). This was later validated in the International Journal of Systematic and Evolutionary Microbiology (IJSEM, Oren & Garriti, 2016). In the responses to the questionnaire, BE, CY, ES, NL, SI and SK considered that Agrobacterium was a pest of concern on Vitis. DE and CY supported listing at genus since several species are considered important and causing similar damage. BE, ES, FR, LT, NL and SK supported listing at species level. The Fruit SEWG suggested to consider the listing of all Agrobacterium and Allorhizobium vitis harbouring the Ti-plasmid.
Remark: DE commented that a prerequisite for the categorisation of Agrobacterium / Allorhizobium vitis as RNQP for Vitis is the availability of a reliable test system that is also suitable for routine testing. Although PCR-based testing for latent bacterial infection directly from the wood is possible, it is still very unreliable without prior isolation of vital bacterial cells for multiplication on specific (semi-selective) media. The number of bacterial cells in the wood is usually so low that false negative results are frequent. Although tests with live isolation are significantly more reliable, they are time-consuming and labour-intensive and therefore expensive due to the high experimental effort involved. They are therefore only suitable or justified for certain scientific questions but not for general routine testing.
Therefore, DE did not recommend classification of Agrobacterium / Allorhizobium vitis as RNQP for Vitis.
Experts from the Fruit SEWG agreed that detection can be difficult because these bacteria may only be present in low concentration or unevenly distributed. Detection in asymptomatic material is obviously less reliable than detection from symptomatic material when the number of bacteria is much higher (Anonymous, 2024). Testing grapevine roots only allows to detect less than 40% of infected grapevine material (Riedle-Bauer et al., 2012). Several factors, apart from the pathogen concentration in nursery stock, such as site characteristics, management practices and environmental conditions, should be taken into account (Voegel and Nelson, 2018). In any case, efforts have been made to develop PCR tests to circumvent these handicaps, and detection limits are comparable to those obtained in other bacterial models (Nguyen-Huu et al., 2021; Turgut and Basim, 2021; Voegel et al., 2023). Sawada et al. (1995) demonstrated that PCR analysis utilizing the primer set (VCF/VCR) can amplify the expected 730-bp products from most (75 of 77) pathogenic agrobacteria harboring Ti or Ri plasmids. With the universal primer set (VCF/VCR), this method, rapid and easy, can be considered convenient for routine detection of Ti and Ri plasmids from pure cultures, and will extend the capability for studying the molecular epidemiology and etiology of Agrobacterium species.
Although the disease is not caused by a clear single taxonomic entity (if considering the bacteria), this criteria can be considered as fulfilled when considering the Ti-plasmid.
In Rubus, different species are involved e.g. Agrobacterium tumefaciens, A. rhizogenes (currently considered as Rhizobium rhizogenes; Flores-Félix et al., 2020) and A. rubi. New species have also been isolated e.g. Agrobacterium arsenijevicii and Rhizobium tumorigenes. In the responses to the questionnaire, DE, ES, EUROSEEDS, FR, LT, NL, SI and SK considered that Agrobacterium was a pest of concern on Rubus. DE supported listing at genus since several species are considered important and causing similar damage. ES, FR, LT, NL and SK supported listing at species level. The Fruit SEWG suggested to consider the listing of all Agrobacterium & Rhizobium harbouring the Ti-plasmid.
In Vitis, crown gall is caused by Agrobacterium (e.g. A. tumefaciens) as well as Allorhizobium vitis, both belonging to the family Rhizobiaceae. Indeed, based on the analysis of the rrs, recA, atpD and rpoB genes, Mousavi et al. (2015) proposed to transfer Rhizobium vitis (initially Agrobacterium vitis) to the genus Allorhizobium (Flores-Félix et al., 2020). This was later validated in the International Journal of Systematic and Evolutionary Microbiology (IJSEM, Oren & Garriti, 2016). In the responses to the questionnaire, BE, CY, ES, NL, SI and SK considered that Agrobacterium was a pest of concern on Vitis. DE and CY supported listing at genus since several species are considered important and causing similar damage. BE, ES, FR, LT, NL and SK supported listing at species level. The Fruit SEWG suggested to consider the listing of all Agrobacterium and Allorhizobium vitis harbouring the Ti-plasmid.
Remark: DE commented that a prerequisite for the categorisation of Agrobacterium / Allorhizobium vitis as RNQP for Vitis is the availability of a reliable test system that is also suitable for routine testing. Although PCR-based testing for latent bacterial infection directly from the wood is possible, it is still very unreliable without prior isolation of vital bacterial cells for multiplication on specific (semi-selective) media. The number of bacterial cells in the wood is usually so low that false negative results are frequent. Although tests with live isolation are significantly more reliable, they are time-consuming and labour-intensive and therefore expensive due to the high experimental effort involved. They are therefore only suitable or justified for certain scientific questions but not for general routine testing.
Therefore, DE did not recommend classification of Agrobacterium / Allorhizobium vitis as RNQP for Vitis.
Experts from the Fruit SEWG agreed that detection can be difficult because these bacteria may only be present in low concentration or unevenly distributed. Detection in asymptomatic material is obviously less reliable than detection from symptomatic material when the number of bacteria is much higher (Anonymous, 2024). Testing grapevine roots only allows to detect less than 40% of infected grapevine material (Riedle-Bauer et al., 2012). Several factors, apart from the pathogen concentration in nursery stock, such as site characteristics, management practices and environmental conditions, should be taken into account (Voegel and Nelson, 2018). In any case, efforts have been made to develop PCR tests to circumvent these handicaps, and detection limits are comparable to those obtained in other bacterial models (Nguyen-Huu et al., 2021; Turgut and Basim, 2021; Voegel et al., 2023). Sawada et al. (1995) demonstrated that PCR analysis utilizing the primer set (VCF/VCR) can amplify the expected 730-bp products from most (75 of 77) pathogenic agrobacteria harboring Ti or Ri plasmids. With the universal primer set (VCF/VCR), this method, rapid and easy, can be considered convenient for routine detection of Ti and Ri plasmids from pure cultures, and will extend the capability for studying the molecular epidemiology and etiology of Agrobacterium species.
Although the disease is not caused by a clear single taxonomic entity (if considering the bacteria), this criteria can be considered as fulfilled when considering the Ti-plasmid.
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:
Candidate
Justification (if necessary):
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, except seeds
3 - Is the pest already listed in a PM4 standard on the concerned host plant?
No
Conclusion:
Evaluation continues
Justification (if necessary):
Remark: only Agrobacterium tumefaciens listed in the Standard PM 4/10 Standard for Rubus (measures are recommended for the production of nuclear stock). Assessment continues.
4 - Are the listed plants for planting the main* pathway for the "pest/host/intended use" combination? (*: significant compared to others):
Yes
Conclusion:
Candidate
Justification:
In the case of Rubus spp., several agrobacteria play a role in crown and cane gall disease. The agrobacterium most commonly recovered from crown gall on Rubus spp. is Rhizobium rhizogenes (Agrobacterium tumefaciens biovar 2) (Weller et al., 2004; Putnam, 2017), this bacterium has a wide host range. A second agrobacterium from Rubus spp. is Rhizobium rubi (Agrobacterium rubi), it has only a few isolates, a more restricted host range and is particularly associated with galls on floricanes (Putnam, 2017). More recently various other agrobacteria were isolated from Rubus sp. plants with crown gall disease in Serbia: Agrobacterium tumefaciens (biovar 1) (Kuzmanović et al., 2015a) and new species, Agrobacterium arsenijevicii (Kuzmanović et al., 2015b) and Rhizobium tumorigenes (Kuzmanović et al., 2018). All these agrobacteria carried a tumour-inducing (Ti) plasmid, which makes them capable of inducing symptoms under the right circumstances. Agrobacteria were also isolated from wild blackberries (Moore et al., 1997).
Crown gall development is initiated when the pathogen enters a wound, attaches to a susceptible plant cell, and inserts a segment of DNA (called T-DNA) from the Ti plasmid (carried by the pathogen) into a chromosome of the healthy raspberry or blackberry cell. Expression of T-DNA results in the overproduction of plant hormones. The uncontrolled synthesis of growth hormones stimulates the plant cells to divide and enlarge abnormally, forming a gall, which typically carries the pathogen. Bacteria without this plasmid are non pathogenic (Putnam, 2017).
Considering host-plant range: Bradbury (1986, cited in CABI 2021) listed 391 susceptible plant genera which have been reported with crown gall symptoms, many of which have multiple susceptible species within the genus. Crown gall disease, however, has been reported on only a few of these plant species in their natural habitat. Reference strains from relatively few host plant species are held in public collections (CABI 2021). Typically, isolates from nature exhibit some degree of host specificity (limited host range) (Anderson & Moore, 1979; Moore & Cooksey, 1981, cited in CABI, 2021). The concept of a limited host range for Rhizobium strains contrasts with the widely published idea of a wide host range (de Cleene & de Ley, 1976). A reason for this seeming discrepancy is that most research on host range is based on “artificial” laboratory inoculations, resulting in a wide host range. There is strong evidence from molecular studies that host range is controlled by genes on the Ti plasmid and the bacterial chromosome (Loper & Kado, 1979; Close et al., 1985; Huang et al., 1990; D’Souza et al., 1993, cited in CABI, 2021).
Plants for planting (excluding seeds): plant material can be a pathway for agrobacteria (Garret, 1978) and the frequent occurrence of this disease may result from transmission by contaminated propagation materials (Sawada et al., 1995). Long-distance dispersal to other geographic areas is readily accomplished through sale and shipment of diseased and infested planting materials, especially as many of the susceptible hosts are propagated vegetatively like Rubus spp. (CABI, 2021). The presence of multiple galls up and down the stems of blackberry suggests the bacterium may be systemic in Rubus spp. (Putnam, 2017). Also, according to the available literature (see 'feasible and effective measures'), the main measure to reduce the incidence of this disease is based on limiting its spread through the planting material (use of pathogen-free material).
Seeds: no.
Soil: Agrobacterium tumefaciens naturally resides on the rhizoplane of woody and herbaceous weeds. Its presence in soils originates from galls that were broken or sloughed off from infected plants during cultivation practices or disseminated as infected plant material (Kado, 2002). Crown gall occurs worldwide in nurseries, orchards and landscapes (cultivated and natural), but it is especially troublesome in nurseries (CABI, 2021). In the presence of nematodes (Pratylenchus penetrans), the incidence of crown gall was significantly increased on root systems of cultivars Skeena and Willamette, which are known to be highly resistant (but not immune) to agrobacteria (Putnam, 2017).
Contaminated tools (and water): tools may become contaminated with the pathogen upon contact with infested soil or by cutting through infested plant material (Fichtner, 2018).
The Fruit SEWG considered that plants for planting is a significant pathway.
Crown gall development is initiated when the pathogen enters a wound, attaches to a susceptible plant cell, and inserts a segment of DNA (called T-DNA) from the Ti plasmid (carried by the pathogen) into a chromosome of the healthy raspberry or blackberry cell. Expression of T-DNA results in the overproduction of plant hormones. The uncontrolled synthesis of growth hormones stimulates the plant cells to divide and enlarge abnormally, forming a gall, which typically carries the pathogen. Bacteria without this plasmid are non pathogenic (Putnam, 2017).
Considering host-plant range: Bradbury (1986, cited in CABI 2021) listed 391 susceptible plant genera which have been reported with crown gall symptoms, many of which have multiple susceptible species within the genus. Crown gall disease, however, has been reported on only a few of these plant species in their natural habitat. Reference strains from relatively few host plant species are held in public collections (CABI 2021). Typically, isolates from nature exhibit some degree of host specificity (limited host range) (Anderson & Moore, 1979; Moore & Cooksey, 1981, cited in CABI, 2021). The concept of a limited host range for Rhizobium strains contrasts with the widely published idea of a wide host range (de Cleene & de Ley, 1976). A reason for this seeming discrepancy is that most research on host range is based on “artificial” laboratory inoculations, resulting in a wide host range. There is strong evidence from molecular studies that host range is controlled by genes on the Ti plasmid and the bacterial chromosome (Loper & Kado, 1979; Close et al., 1985; Huang et al., 1990; D’Souza et al., 1993, cited in CABI, 2021).
Plants for planting (excluding seeds): plant material can be a pathway for agrobacteria (Garret, 1978) and the frequent occurrence of this disease may result from transmission by contaminated propagation materials (Sawada et al., 1995). Long-distance dispersal to other geographic areas is readily accomplished through sale and shipment of diseased and infested planting materials, especially as many of the susceptible hosts are propagated vegetatively like Rubus spp. (CABI, 2021). The presence of multiple galls up and down the stems of blackberry suggests the bacterium may be systemic in Rubus spp. (Putnam, 2017). Also, according to the available literature (see 'feasible and effective measures'), the main measure to reduce the incidence of this disease is based on limiting its spread through the planting material (use of pathogen-free material).
Seeds: no.
Soil: Agrobacterium tumefaciens naturally resides on the rhizoplane of woody and herbaceous weeds. Its presence in soils originates from galls that were broken or sloughed off from infected plants during cultivation practices or disseminated as infected plant material (Kado, 2002). Crown gall occurs worldwide in nurseries, orchards and landscapes (cultivated and natural), but it is especially troublesome in nurseries (CABI, 2021). In the presence of nematodes (Pratylenchus penetrans), the incidence of crown gall was significantly increased on root systems of cultivars Skeena and Willamette, which are known to be highly resistant (but not immune) to agrobacteria (Putnam, 2017).
Contaminated tools (and water): tools may become contaminated with the pathogen upon contact with infested soil or by cutting through infested plant material (Fichtner, 2018).
The Fruit SEWG considered that plants for planting is a significant pathway.
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
Crown gall is one of the main problems in many Rubus spp. growing areas (Finn, 2008; France y Morales, 2017).The impact of the disease on plant growth and production can range from no apparent effect to death of the plant. Damage is greatest when young plants become infected during the year in which they are planted. Severely galled plants are weakened, stunted, and unproductive. The abnormal proliferation of plant tissues that results in gall formation disrupts water and nutrient uptake and transport in the plant (Putnam, 2017; Weller et al., 2004). Crown gall reduces stand productivity; once a field is infected, it could stay infected for many years (Andersen & Crocker, 2001).
What is the likely economic impact of the pest irrespective of its infestation source in the absence of phytosanitary measures? (= official measures)
Medium
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?
No
Conclusion:
Justification:
Evidence of its economic impact is available in the literature and was rated here for young plants only (Medium for young plants. No impact for old plants when they survived).
Symptom expression highly depends on environmental conditions during the first years, at the time the plant builds its main vascular system: Cold winter followed by a warm spring will cause tumor formation if infected. It also depends on stress factors.
Lower impact is observed in warmer countries. Less impact is expected in the future in Europe with global warming.
Symptom expression highly depends on environmental conditions during the first years, at the time the plant builds its main vascular system: Cold winter followed by a warm spring will cause tumor formation if infected. It also depends on stress factors.
Lower impact is observed in warmer countries. Less impact is expected in the future in Europe with global warming.
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?
No
Conclusion:
Not candidate
Justification:
Producing pest-free planting material is the basis of effective control. Once established in crops the control of these pathogens is difficult (Sawada et al., 1995; Fance y Morales, 2017; PlantwisePlus Knowledge Bank, 2021).
Sanitation and the use of good cultural practices, such as careful inspection of all nursery stock and uprooting and burning all plants with crown gall symptoms, are important in disease control.
The adoption of any management practice that eliminates or minimizes the wounding of plant tissues is beneficial in control. It has been reported that wounds left after cutting out old blackberry canes remained susceptible for at least several days. These wounds were most readily infected during the growing season. Avoiding planting sites with heavy infestations of root-attacking insects and nematodes and controlling these root attacking insects and nematodes reduce the wounding of the roots.
Crown gall is worse in low areas where water tends to accumulate and in wet, heavy soils. It is recommended to avoid planting in such areas.
Choosing where possible a rootstock that is less susceptible.
Avoiding planting sites where galled plants were grown within the last 4-5 years.
(PlantwisePlus Knowledge Bank, 2021; Putnam, 2017).
However, the Fruit SEWG considered that since symptom expression was highly dependant on environmental conditions, and that testing was probably not a reliable enough measures.
Sanitation and the use of good cultural practices, such as careful inspection of all nursery stock and uprooting and burning all plants with crown gall symptoms, are important in disease control.
The adoption of any management practice that eliminates or minimizes the wounding of plant tissues is beneficial in control. It has been reported that wounds left after cutting out old blackberry canes remained susceptible for at least several days. These wounds were most readily infected during the growing season. Avoiding planting sites with heavy infestations of root-attacking insects and nematodes and controlling these root attacking insects and nematodes reduce the wounding of the roots.
Crown gall is worse in low areas where water tends to accumulate and in wet, heavy soils. It is recommended to avoid planting in such areas.
Choosing where possible a rootstock that is less susceptible.
Avoiding planting sites where galled plants were grown within the last 4-5 years.
(PlantwisePlus Knowledge Bank, 2021; Putnam, 2017).
However, the Fruit SEWG considered that since symptom expression was highly dependant on environmental conditions, and that testing was probably not a reliable enough measures.
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
No
Conclusion:
Justification:
CONCLUSION ON THE STATUS:
Disqualified: uncertainty whether economic impact should be considered as unacceptable. No effective and feasible measures available. Several other uncertainties.
8 - Tolerance level:
Is there a need to change the Tolerance level:
Yes
Proposed Tolerance levels:
Delisting
9 - Risk management measures:
Is there a need to change the Risk management measure:
Yes
Proposed Risk management measure:
Delisting
REFERENCES:
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