| 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 (Ti-plasmid) {Agrobacterium tumefaciens} (AGRBTU)
GENERAL INFORMATION ON THE PEST
Name as submitted in the project specification (if different):
Agrobacterium tumefaciens
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?:
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):
The genus Agrobacterium (= Rhizobium) can carry plasmids which, in the case of a Ti-plasmid (tumour-inducing plasmid) can induce galls or tumors (crown gall) in many different host plants.
Crown gall infections result following transfer of a part of the Ti-plasmid (T-DNA) into the host plant. T-DNA expression induces an overproduction of plant hormones which stimulate plant cell division and enlargement, i.e. gall formation. Bacteria without this plasmid are non pathogenic (Moore, revised by Burr, 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).
In walnut both species/biovars are reported:
1) Agrobacterium tumefaciens biovar 1 = Agrobacterium radiobacter = Rhizobium radiobacter (note: with Ti-plasmid: Agrobacterium tumefaciens, without Ti-plasmid Agrobacterium radiobacter - taxonomic discussion on whether presence/absence of a plasmid could determine the name), this datasheet is on bacterium 1) not 2)
2) Agrobacterium tumefaciens biovar 2 = Rhizobium rhizogenes
Both bacteria can have a tumour-inducing plasmid (Ti-plasmid), both can infect walnut. Bacteria without plasmid do not cause disease.
Remark: Both bacteria can also have a rhizome-inducing plasmid (Ri-plasmid), causing hairy roots or crazy roots.
In walnut, the EWG considered that 'Agrobacterium with Ti-plasmid' was the pest of concern. Since the Ti-plasmid may be exchanged with other Agrobacterium species, the Fruit SEWG recommended to replace 'Agrobacterium tumefasciens' by 'Agrobacterium'.
For similar reasons, 'Agrobacterium with Ti-plasmid' is also the pest of concern for all the other concerned host plants.
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.
Crown gall infections result following transfer of a part of the Ti-plasmid (T-DNA) into the host plant. T-DNA expression induces an overproduction of plant hormones which stimulate plant cell division and enlargement, i.e. gall formation. Bacteria without this plasmid are non pathogenic (Moore, revised by Burr, 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).
In walnut both species/biovars are reported:
1) Agrobacterium tumefaciens biovar 1 = Agrobacterium radiobacter = Rhizobium radiobacter (note: with Ti-plasmid: Agrobacterium tumefaciens, without Ti-plasmid Agrobacterium radiobacter - taxonomic discussion on whether presence/absence of a plasmid could determine the name), this datasheet is on bacterium 1) not 2)
2) Agrobacterium tumefaciens biovar 2 = Rhizobium rhizogenes
Both bacteria can have a tumour-inducing plasmid (Ti-plasmid), both can infect walnut. Bacteria without plasmid do not cause disease.
Remark: Both bacteria can also have a rhizome-inducing plasmid (Ri-plasmid), causing hairy roots or crazy roots.
In walnut, the EWG considered that 'Agrobacterium with Ti-plasmid' was the pest of concern. Since the Ti-plasmid may be exchanged with other Agrobacterium species, the Fruit SEWG recommended to replace 'Agrobacterium tumefasciens' by 'Agrobacterium'.
For similar reasons, 'Agrobacterium with Ti-plasmid' is also the pest of concern for all the other concerned host plants.
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):
Austria (1993); Belgium (1992); Bulgaria (1993); Cyprus (2011); Czech Republic (2011); Denmark (1993); Estonia (1992); Finland (1992); France (1993); Germany (1993); Greece (1992); Hungary (1992); Italy (1992); Netherlands (1992); Poland (2015); Romania (1992); Slovakia (2003); Spain (1992); Sweden (1992)
Conclusion:
Candidate
Justification (if necessary):
Data of the presence of this pest on the EU territory are available in EPPO Global Database (https://gd.eppo.int/).
HOST PLANT N°1: Vaccinium (1VACG) 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?
Yes
Conclusion:
Evaluation continues
Justification (if necessary):
Listed in PM 4 Standard for the concerned pest/host combination. However, when responding to the questionnaire, FR considered that effective and feasible measures were not available. Evaluation continues on economic impact and measures, together with all other assessments for A. tumefaciens.
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:
Crown gall, Agrobacterium tumefaciens, has been reported in Malus and Pyrus (Moore, revised by Burr, 2017), Cydonia (CABI, 2021), Prunus spp. (Burr, 1995), Rubus spp. (Putnam, 2017) and Vaccinium spp. (Bristow & Moore, revised by Putnam, 2017).
Plants for planting (excluding seeds): plant material can be a pathway for Agrobacterium tumefaciens. 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 (CABI, 2021).
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). It is present in many European countries. Crown gall occurs worldwide in nurseries, orchards and landscapes (cultivated and natural), but it is especially troublesome in nurseries (CABI, 2021).
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.
Plants for planting (excluding seeds): plant material can be a pathway for Agrobacterium tumefaciens. 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 (CABI, 2021).
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). It is present in many European countries. Crown gall occurs worldwide in nurseries, orchards and landscapes (cultivated and natural), but it is especially troublesome in nurseries (CABI, 2021).
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:
Infected plants may be stunted or weak compared with healthy ones. When older plants (2-5 years old) are affected, the foliage discolors prematurely in the summer. The foliage on an affected branch or plant initially takes on a reddish hue and then becomes yellowish brown as the disease progresses. Very young plants may be killed outright (Bristow & Moore, revised by Putnam, 2017).
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:
All blueberry cultivars are apparently susceptible to crown gall. Thus, the most effective means of control is to establish plantings in uninfested soil with pathogen-free planting stock. Fields where the previous crop was infected should be avoided for 2 or 3 years or more. A nonhost crop, such as grasses (grains or pasture) or vegetables, should be grown during this period to significantly reduce the population of the pathogen (Bristow & Moore, revised by Putnam, 2017).
Good cultural practices, including sanitation, minimize the risk of introducing the pathogen into disease-free plantings. All nursery stock should be carefully inspected, and all plants with crown gall symptoms should be removed from the site and discarded. This practice is especially important in nurseries to avoid the contamination of healthy plants. Bare-root stock is easier to inspect than stock grown in soil in plastic bags or pots. Plants grown in containers should be inspected when they are planted (Bristow & Moore, revised by Putnam, 2017).
The adoption of management practices that minimize wounding of plant tissues is beneficial in controlling crown gall. Soil insects, such as root weevils, should be controlled to reduce root wounding. Practices such as crown grinding to narrow the base of large, mature plants in order to accommodate mechanical harvesters should be avoided (Bristow & Moore, revised by Putnam, 2017).
Use of an uninfested planting medium in propagation beds is critical. Pruning equipment should be sterilized when propagation wood is collected. Pruners may be sterilized with a 10-20% solution of commercial bleach, a 0.5% solution of potassium permanganate, or shellac thinner (70% ethyl alcohol) (Bristow & Moore, revised by Putnam, 2017).
However, since symptom expression was highly dependant on environmental conditions, and that testing was probably not reliable enough for asymptomatic plants, the Fruit SEWG considered that there was no feasible and effective measures available.
Good cultural practices, including sanitation, minimize the risk of introducing the pathogen into disease-free plantings. All nursery stock should be carefully inspected, and all plants with crown gall symptoms should be removed from the site and discarded. This practice is especially important in nurseries to avoid the contamination of healthy plants. Bare-root stock is easier to inspect than stock grown in soil in plastic bags or pots. Plants grown in containers should be inspected when they are planted (Bristow & Moore, revised by Putnam, 2017).
The adoption of management practices that minimize wounding of plant tissues is beneficial in controlling crown gall. Soil insects, such as root weevils, should be controlled to reduce root wounding. Practices such as crown grinding to narrow the base of large, mature plants in order to accommodate mechanical harvesters should be avoided (Bristow & Moore, revised by Putnam, 2017).
Use of an uninfested planting medium in propagation beds is critical. Pruning equipment should be sterilized when propagation wood is collected. Pruners may be sterilized with a 10-20% solution of commercial bleach, a 0.5% solution of potassium permanganate, or shellac thinner (70% ethyl alcohol) (Bristow & Moore, revised by Putnam, 2017).
However, since symptom expression was highly dependant on environmental conditions, and that testing was probably not reliable enough for asymptomatic plants, the Fruit SEWG considered that there was no feasible and effective measures available.
7- Is the quality of the data sufficient to recommend the pest to be listed as a RNQP?
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:
- Anderson AR & Moore LW (1979) Host specificity in the genus Agrobacterium. Phytopathology 69(4), 320-323.
- Bristow PR, Moore LW, revised by Putnam ML (2017) Crown gall. In Compendiumof Blueberry, Cranberry, and Lingonberry Diseases and Pests 2nd edition (eds Polashock JJ, Caruso FL, Averill AL & Schilder AC). American Phytopathological Society, St Paul, MN, USA. pages 82-84.
- Burr TJ (1995) Crown gall. In Compendium of Stone Fruit Diseases (eds Ogawa JM, Zehr EI, Bird GW, Ritchie DF, Uriu K & Uyemota JK). American Phytopathological Society, St Paul, MN, USA. page 52-53.
- CABI (2021) Rhizobium radiobacter. Crop Protection Compendium. (last accessed on 19/Mar/2024). https://www.cabidigitallibrary.org/doi/10.1079/cabicompendium.3745.
- Cleene M de & Ley J de (1976) The host range of crown gall. Botanical Review 42(No. 4), 389-466.
- Close TJ, Tait RC & Kado CI (1985) Regulation of Ti plasmid virulence genes by a chromosomal locus of Agrobacterium tumefaciens. Journal of Bacteriology 164(2), 774-781.
- D'Souza-Ault MR, Cooley MB & Kado CI (1993) Analysis of the Ros repressor of Agrobacterium virC and virD operons: molecular intercommunication between plasmid and chromosomal genes. Journal of Bacteriology 175(11), 3486-3490.
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- Fichtner EJ (2018) Crown gall on walnuts: assessing origin of infection, disease management and prevention. Nut, Olive And Prune Programmatic News, Agriculture and Natural Resources, University of California. Published on: December 13, 2018 (accessed on 17/Mar/2024). https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=28927.
- Grant JA, McGranahan GH (2005) English walnut rootstocks help avoid blackline disease, but produce less than ´Paradox´ hybrid. California Agriculture 59, 249–251. Available online: http://californiaagriculture.ucanr.org/landingpage.cfm?article=ca.v059n04p249&fulltext=yes.
- Huang MLW, Cangelosi GA, Halperin W & Nester EW (1990) A chromosomal Agrobacterium tumefaciens gene required for effective plant signal transduction. Journal of Bacteriology 172(4), 1814-1822.
- Kado CI (2002) Crown gall. The plant health instructor. 2002(2) (Accessed 17/Sep/2024). https://www.apsnet.org/edcenter/disandpath/prokaryote/pdlessons/Pages/CrownGall.aspx
- Kluepfel DA, McClean AE, Yakabe LE, Maccree MM & Parker SR (2010) Detection and implication of early Agrobacterium tumefaciens infection of paradox seeds and seedlings. Acta Horticulturae 861, 497-500. DOI: 10.17660/ActaHortic.2010.861.70
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- Loper JE & Kado CI (1979) Host range conferred by the virulence-specifying plasmid of Agrobacterium tumefaciens. Journal of Bacteriology 139(2), 591-596.
- Moore LW, revised by Burr J (2017) Crown gall. In Compendium of Apple and Pear Diseases and Pests, 2nd edition (eds Sutton, TB, Aldwinckle HS, Agnello AM & Walgenbach JF). American Phytopathological Society, St Paul, MN, USA. pages 93-94.
- Moore LW & Cooksey DC (1981). Biology of Agrobacterium tumefaciens: Plant Interactions. In The Biology of Rhizobiaceae, Supplement to International Review of Cytology, Supplement 13 (ed Giles K).: Academic Press, NY, USA pages 15-46.
- NCPPB (2024) Rhizobium rubi. National Collection of Plant Pathogenic Bacteria, FERA, UK (Accessed 17/Sep/2024).
- Putnam ML (2017) Crown and cane gall. 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 61-63.
- UC PMG (2017a) Crown gall. In Apricot – Pest management guidelines. University of California, Agriculture and Nature Resources, Publication 3433, page 64. .
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