| 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 & Allorhizobium vitis (Ti-plasmid) (1AGRBG & AGRBVI)
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: Vine 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: Vine 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: Vitis (1VITG) for the Vine sector.
Origin of the listing:
New proposal
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):
EPPO Standard PM 4/8 Pathogen-tested material of grapevine varieties and rootstocks recommends inspection for freedom from crown gall (Agrobacterium tumefaciens and A. vitis). However, it is noted that latent infections of A. tumefaciens and A. vitis may occur.
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:
Agrobacteria are known to be soil-borne plant pathogens. Agrobacteria will remain active in the soil for a minimum of two years in the absence of a host or longer on decaying infected tissues (Watt, 2010), so soils are generally considered as sources of infection; but while this is true for fruit trees, grapevine crown gall is usually due to infected propagation material (Tzfira and Citovsky, 2008). A recent study in Canada showed that A. vitis was present in the planting material of all nurseries tested (Voegel et al., 2023). The number of pathogenic agrobacteria is known to show a significant seasonal fluctuation: during the growing season, the number of pathogenic bacteria is high, but decreases drastically during autumn and winter, indicating an essential role of the weed rhizosphere in regulating A. tumefaciens populations in nursery soils (Krimi et al., 2002). In fact, some studies in US vineyards have shown that A. vitis can only be isolated from the rhizosphere of diseased plants. Analysis of soils from several vineyards in Amenia revealed that only A. tumefaciens and not A. vitis was detected in the samples (Jäger et al., 1990), confirming that in the case of grapevine it is not the soil but the infected plant material that is mainly responsible for the spread of the disease (Tzfira and Citovsky, 2008). However, A. vitis survives in root pieces for years and can therefore initiate new infections from soil on which previously infected plants were grown (Burr et al., 1995). Although infected propagating material is the main source of A. vitis on grapevines, infection of Agrobacterium-free grapevines from soil has also been reported (Pu and Goodman, 1993), probably favoured by nematodes, as agrobacteria can enter roots through nematode wounds (Süle et al., 1995; Rubio-Cabetas et al., 2001). By analysing the xylem, it was found that 53% of originally pathogen-free grapevines planted in infested soil contained Agrobacterium two years after planting (Pu and Goodman, 1993). Wild grapevines are a significant reservoir of inoculum (Orel et al., 2017).
There are no references to Agrobacterium being a seed pathogen in Vitis.
In the case of grapevine, the Fruit SEWG considered that the importance of soil-borne inoculum in replanted vineyards is not well understood and the primary source of diseased vines reported appears to be through propagation of diseased wood (PlantwisePlus Knowledge Bank, 2012).
There are no references to Agrobacterium being a seed pathogen in Vitis.
In the case of grapevine, the Fruit SEWG considered that the importance of soil-borne inoculum in replanted vineyards is not well understood and the primary source of diseased vines reported appears to be through propagation of diseased wood (PlantwisePlus Knowledge Bank, 2012).
5 - Economic impact:
Are there documented reports of any economic impact on the host?
Yes
Justification:
It is said that crown gall is one of the most devastating diseases of grapevine (Burr and Otten, 1999), causing large economic losses associated with lower productivity and the cost of vine replacement, because Agrobacterium can survive for a long time in infected roots, on decaying vines and in the soil (Kuzmanović et al., 2018), even after the plants have been removed, as the bacterium is active and viable in the soil and can infect new planting material (Vizitiu et al., 2012). Incidence may range from a few vines in a vineyard to 100% of the vines. In addition to reducing vigour and yield, gall development may result in the girdling of vines. The amount of crown gall present from year to year appears to be related to the severity of the preceding winter and the maturity of the vines (PlantwisePlus Knowledge Bank, 2012). But the only study with economic data that seems to exist is from 2004 in Pennsylvania, where losses amounted to 46,500 US dollars per 0.4 hectares over a 6-year period (Stewart and Wenner, 2004).
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 vines. No impact for old vines 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:
There are studies in which the pathogen was detected in all nursery material for planting, although with uneven distribution between nurseries (Voegel et al., 2023). Once the crown gall pathogen is present in regions or vineyards, it is practically impossible to eradicate.
To date, the most successful strategy for disease prevention is planting healthy nursery material in non-infected soil (Johnson et al., 2013; Gordon et al., 2024). Propagating material should be obtained from disease-free sources (PlantwisePluse Knowledge Bank, 2023; Vizitiu et al., 2012)
However, systemic survival of the pathogen in asymptomatic grapevines makes it difficult to produce clean grapevine stock (Burr et al., 2016), and the pathogen is often disseminated through the vegetative propagation of infected symptomless vines or with rhizosphere soil (Burr et al., 1987; Yepes et al., 2019). Disease expression highly depends on environmental conditions and the Fruit SEWG considered that testing asymptomatic material was not reliable enough.
To date, the most successful strategy for disease prevention is planting healthy nursery material in non-infected soil (Johnson et al., 2013; Gordon et al., 2024). Propagating material should be obtained from disease-free sources (PlantwisePluse Knowledge Bank, 2023; Vizitiu et al., 2012)
However, systemic survival of the pathogen in asymptomatic grapevines makes it difficult to produce clean grapevine stock (Burr et al., 2016), and the pathogen is often disseminated through the vegetative propagation of infected symptomless vines or with rhizosphere soil (Burr et al., 1987; Yepes et al., 2019). Disease expression highly depends on environmental conditions and the Fruit SEWG considered that testing asymptomatic material was not reliable enough.
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:
No (new regulation proposal)
Proposed Tolerance levels:
No listing.
9 - Risk management measures:
Is there a need to change the Risk management measure:
No
Proposed Risk management measure:
No listing.
Justification (if necessary):
Testing soil for Agrobacterium presents challenges due to low concentrations and the inhibitors of PCR present in soil.
Hot water treatment is applied in some nurseries, but is not completely effective, as there is work on the survival of A. vitis (Burr et al., 1996, Am J, Enol Vitic 47: 119-123)]
Hot water treatment is applied in some nurseries, but is not completely effective, as there is work on the survival of A. vitis (Burr et al., 1996, Am J, Enol Vitic 47: 119-123)]
REFERENCES:
- Anonymous (2024) Fact Sheet Viticulture: Crown gall in Australian vineyards. Australian Wine Research Institute.
- Boiu-Sicuia O-A, Dinu S, Barbu L (2020) Physiological profile of some pathogenic bacteria associated with grapevine crown gall. Sci Pap-Ser B Hortic. 64, 230–237.
- Burr T, Johnson K, Reid C, Orel CD, Yepes M, Fuchs M (2016) Environmental sources of Agrobacterium vitis, the cause of crown gall on grape. New York Fruit Quarterly, 24, 15-18.
- Burr TJ, Otten L (1999) Crown gall of grape: Biology and disease management. Ann. Rev. Phytopathol. 37, 53–80.
- Burr TJ, Reid CL, Yoshimura M, Momol EA & Bazzi C (1995) Survival and tumorigenicity of Agrobacterium vitis in living and decaying grape roots and canes in soil. Plant Disease 79: 677-682.
- Burr TJ, Bazzi C, Süle S & Otten L (1998) Crown gall of grape: biology of Agrobacterium vitis and the development of disease control strategies. Plant Disease 82, 1288–97.
- Burr TJ, Katz BH, Bishop AL (1987) Populations of Agrobacterium in vineyard and nonvineyard soils and grape roots in vineyards and nurseries. Plant Disease 71, 617-620.
- Filo A, Sabbatini P, Sundin GW, Zabadal TJ, Safir GR, Cousins PS (2013) Grapevine crown gall suppression using biological control and genetic engineering: a review of recent research. Am J Enol Vitic 64: 1.
- Flores-Félix JD, Menéndez E, Peix A, García-Fraile P, Velázquez E (2020) History and current taxonomic status of genus Agrobacterium. Syst Appl Microbiol 43 (1), 126046.
- Genov I, Atanassov I, Tsvetkov I, Atanassov A (2006) Isolation and characterization of Agrobacterium strains from grapevines in Bulgarian vineyards and wild grapes, V. vinifera spp. silvestris. Vitis 45: 97-101.
- Gordon MI, Thomas WJ, Putnam ML (2024) Transmission and management of pathogenic Agrobacterium tumefaciens and Rhodococcus fascians in select ornamentals. Plant Dis 108(1):50-61.
- Jäger J, Lorenz D, Plapp R, Eichhorn KW (1990) Untersuchungen zum latenten Vorkommen von Agrobacterium tumefaciens Biovar 3 in der Weinrebe (Vitis vinifera L.). Die Weinwissenschaft 45: 14-20.
- Johnson KL, Zheng D, Kaewnum S, Reid CL, Burr T (2013) Develoment of a magnetic capture hybridization rel-time PCR assay for detection of tumorigenic Agrobacterium vitis in grapevines. Phytopathol 103: 633-640.
- Knauf VC, Panagopoulos CG, Wester EW (1982) Genetic factors controlling the host range of Agrobacterium tumefaciens. Phytopthol 72: 1545-1549.
- Krimi Z, Petit A, Mougel C, Dessaux Y, Nesme X (2002) Seasonal fluctuations and long-term persistence of pathogenic populations of Agrobacterium spp. in soils. Appl Environ Microbiol 68: 3358-3365.
- Kuzmanović N, Smalla K, Gonow S, Pulawska J (2018) Rhizobium tumorigenes sp. nov., a novel plant tumorigenic bacterium isolated from cane gall tumors on thornless blackberry. Sci Rep 8, 13006.
- Mousavi SA, Willems A, Nesme X, de Lajudie P, Lindström K (2015) Revised phylogeny of Rhizobiaceae: proposal of the delineation of Pararhizobium gen. nov., and 13 new species combinations. Syst Appl Microbiol 38, 84–90.
- Nguyen-Huu T, Doré J, Barka EA, Lavire C, Clément C, Vial L, Sanchez L (2021) Development of a DNA-based real-time PCR assay to quantify Allorhizobium vitis over time in grapevine (Vitis vinifera L.) plantlets. Plant Dis 105: 384-391.
- Oliveira H, Nascimento T (1993) Characteristics of portuguese strains of Agrobacterium tumefaciens isolated from grapevine and stone fruit trees. Anais do Instituto Superior de Agronomia (1993): 201-218.
- Orel DC, Reid CL, Fuchs M, Burr TJ (2017) Identifying environmental sources of Agrobacterium vitis in vineyards and wild grapevines. Am J Enol Vitic 68: 213-217.
- Oren A, Garrity GM (2016) Validation List no. 172. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 66, 4299–4305.
- Panagopoulos CG, Psallidas PG (1973) Characteristics of Greek isolates of Agrobacterium tumefaciens (E.F. Smith & Townsend) Conn. J Appl Bact 36: 233-240.
- PlantwisePlus Knowledge Bank (2023) Rhizobium vitis (crown gall of grapevine). https://doi.org/10.1079/pwkb.species.47515 (accessed: October 2024).
- PlantwisePlus Knowledge Bank (2012) External Factsheet: Crown gall (Agrobacterium vitis). Canada Ministry of Agriculture BC https://plantwiseplusknowledgebank.org/doi/10.5555/pwkb.20127802584#tab-contributors (accessed: October 2024).
- Poppenberger B, Leonhardt W, Redl H (2002) Latent persistence of Agrobacterium vitis in micropropagated Vitis vinifera. Vitis 41: 113-114.
- Pu XA, Goodman RN (1993) Effects of fumigation and biological control on infection of indexed crown gall free grape plants. Am J Enol Vitic 44: 241-248.
- Riedle-Bauer M, Mörtel J, Bauer H & Knobling A (2012) Möglichkeiten und Grenzen beim Nachweis von Agrobacterium vitis in Reben mittels unterschiedlicher auf PCR basierender Methoden. Mitteilungen Klosterneuburg 62, 1-9.
- Rubio-Cabetas MJ, Minot JC, Voisin M, Esmenjaud D (2001) Interaction of rootknot nematodes (RKN) and the bacterium Agrobacterium tumefaciens in roots of Prunus cerasifera: evidence of the protective effect of the Ma RKN resistance genes against expression of crown gall symptoms. Eur J Plant Pathol 107: 433-441.
- Šabec-Paradiž M., Koruza B., Pečar-Fonović U., Škerlevaj V., Topolovec A., Urek G. 2002. Agrobacterium in grapevine nursery production. Vinogradi in vina za tretje tisočletje? (2. slovenski vinogradniško-vinarski kongres z mednarodno udeležbo, Otočec, 31.1. do 2.2. 2002), Ljubljana: 203-205.
- Šabec-Paradiž M., Škerlevaj V. (2000) Crown gall of grapevine in Slovenia. Acta Agriculturae Slovenica, 75(1), 27–33.
- Sawada H, Ieki H & Matsuda I (1995) PCR detection of Ti and Ri plasmids from phytopathogenic Agrobacterium strains. Applied and Environmental Microbiology 61 (2), 828-831.
- Stewart EL, Wenner NG (2004) Grapevine decline in Pennsylvania and New York. Wine East. 32:12-21, 51-53.
- Süle S, Lehoczky J, Jenser G, Nagy P, Burr TJ (1995) Infection of grapevine roots by Agrobacterium vitis and Meloidogyne hapla. J Phytopathol 143: 169-171.
- Turgut A, Basim H (2021) Development of a real-time PCR assay using locked nucleic acid probe for the detection of octopine, nopaline, and vitopine strains of tumorigenic Allorhizobium vitis in grapevines. Crop Prot 145: 105620.
- Tzfira T and Citovsky V (2008) Agrobacterium: From Biology to Biotechnology. 10.1007/978-0-387-72290-0.
- Vizitiu DE, Dejeu L, Radulescu I, Popescu CF (2012) Preventing and limiting the spread of crown gall in vineyards. Scientific Papers. Series B, Horticulture, ISSN Online 2286-1580, ISSN-L 2285-5653.
- Voegel TM, Nelson LM (2018) Quantification of Agrobacterium vitis from grapevine nursery stock and vineyard soil using droplet digial PCR. Plant Dis 102: 2136-2141.
- Voegel TM, McGonigal P, Nelson LM, Úrbez-Torres JR (2023) Health status of ready-to-plant grapevine nursery material in Canada regarding crown gall and description of the first Allorhizobium vitis strain OP-G1 isolated from British Columbia. Plant Dis 107: 12, 3666-3673.
- Watt BA (2010) Crown gall. Pest Management Fact Sheet #5095. The University of Maine Cooperative Extension. https://extension.umaine.edu/ipm/ipddl/publications/5095e/ (accessed: October 2024) Weisberg AJ, Wu Y, Chang JH, Lai E-M, Kuo C-H (2023) Virulence and ecology of agrobacteria in the context of evolutionary genomics. Annu. Rev. Phytopathol. 2023. 61:1–23.
- Yepes LM, Burr T, Reid C, Fuchs M (2019) Elimination of the crown gall pathogen, Agrobacterium vitis, from systemically infected grapevines by tissue culture. American Journal of Enology and Viticulture, 70(3), 243–248.