Xanthomonas fragariae (angular leaf spot)
- Taxonomic Tree
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Xanthomonas fragariae Kennedy & King, 1962
Preferred Common Name
- angular leaf spot
International Common Names
- English: leaf blight of strawberry; vascular collapse of strawberry
- Spanish: avejentamiento del fresa; mancha angular de las hojas del fresal; marchitamiento vascular del fresal
- French: bacteriose du fraisier; fletrissement vasculaire du fraisier; taches angulaires du fraisier
- Portuguese: manch angulare da folha do morangueiro
Local Common Names
- Germany: Eckige Blattfleckenkrankheit: Erdbeere
- Italy: maculatura angolare delle foglie della fragola
- XANTFR (Xanthomonas fragariae)
Taxonomic TreeTop of page
- Domain: Bacteria
- Phylum: Proteobacteria
- Class: Gammaproteobacteria
- Order: Xanthomonadales
- Family: Xanthomonadaceae
- Genus: Xanthomonas
- Species: Xanthomonas fragariae
DescriptionTop of page X. fragariae is an aerobic, Gram-negative, non-spore-forming, non-capsulate rod; size averaging 0.4 x 1.3 µm. Most cells are non-motile, but some have a single polar flagellum. On beef-extract-peptone agar, or similar medium without added carbohydrate, colonies are circular, entire, convex, glistening, translucent to pale-yellow (Bradbury, 1977).
DistributionTop of page
X. fragariae was first described in 1962 in North America. It probably spread from there, with planting material, to other continents but this is only a presumption.
See also CABI/EPPO (1998, No. 284).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Restricted distribution||EPPO, 2018|
|-Tianjin||Restricted distribution||EPPO, 2018|
|Iran||Present, few occurrences||EPPO, 2018|
|Israel||Absent, formerly present||CABI/EPPO, 2013; EPPO, 2014|
|Korea, Republic of||Restricted distribution||EPPO, 2018|
|Taiwan||Present||CABI/EPPO, 2013; EPPO, 2014|
|Turkey||Absent, no pest record||EPPO, 2014|
|Uzbekistan||Absent, no pest record||EPPO, 2014|
|Ethiopia||Present||1991||CABI/EPPO, 2013; EPPO, 2014|
|Canada||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|-New Brunswick||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Newfoundland and Labrador||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Nova Scotia||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|-Ontario||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Quebec||Present||CABI/EPPO, 2013; EPPO, 2014|
|Mexico||Present||Fernández-Pavía et al., 2014|
|USA||Restricted distribution||1962||CABI/EPPO, 2013; EPPO, 2014|
|-California||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|-Florida||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|-Kentucky||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|-Minnesota||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|-New York||Present||CABI/EPPO, 2013|
|-North Carolina||Present||CABI/EPPO, 2013; EPPO, 2014|
|-North Dakota||Present||CABI/EPPO, 2013|
|-Wisconsin||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|Argentina||Present||CABI/EPPO, 2013; EPPO, 2014|
|Brazil||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|-Minas Gerais||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|-Rio Grande do Sul||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|-Sao Paulo||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|Chile||Eradicated||1992||CABI/EPPO, 2013; EPPO, 2014|
|Ecuador||Absent, formerly present||CABI/EPPO, 2013; EPPO, 2014|
|Paraguay||Widespread||CABI/EPPO, 2013; EPPO, 2014|
|Uruguay||Present||CABI/EPPO, 2013; EPPO, 2014|
|Venezuela||Present||CABI/EPPO, 2013; EPPO, 2014|
|Austria||Restricted distribution||CABI/EPPO, 2013|
|Belgium||Present, few occurrences||1998||Lieten, 1998; CABI/EPPO, 2013; EPPO, 2014|
|Bulgaria||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|Cyprus||Absent, no pest record||EPPO, 2014|
|Czech Republic||Absent, no pest record||EPPO, 2014|
|Estonia||Eradicated||IPPC, 2009; CABI/EPPO, 2013; EPPO, 2014|
|Finland||Present, few occurrences||CABI/EPPO, 2013; EPPO, 2014|
|France||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|Germany||Restricted distribution||1995||CABI/EPPO, 2013; EPPO, 2014|
|Greece||Absent, formerly present||CABI/EPPO, 2013; EPPO, 2014|
|Guernsey||Absent, no pest record||EPPO, 2014|
|Italy||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|-Italy (mainland)||Restricted distribution||CABI/EPPO, 2013|
|-Sicily||Present||Bradbury, 1986; CABI/EPPO, 2013; EPPO, 2014|
|Latvia||Absent, no pest record||EPPO, 2014|
|Malta||Absent, no pest record||EPPO, 2014|
|Netherlands||Restricted distribution||1996||NPPO of the Netherlands, 2013; CABI/EPPO, 2013; EPPO, 2014||Present in several areas where host crops are grown.|
|Norway||Absent, confirmed by survey||EPPO, 2014|
|Portugal||Widespread||CABI/EPPO, 2013; EPPO, 2014|
|Romania||Absent, formerly present||CABI/EPPO, 2013; EPPO, 2014|
|Slovakia||Absent, no pest record||EPPO, 2014|
|Slovenia||Restricted distribution||Brence, 2002; CABI/EPPO, 2013; EPPO, 2014|
|Spain||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|Switzerland||Widespread||1993||CABI/EPPO, 2013; EPPO, 2014|
|UK||Eradicated||CABI/EPPO, 2013; EPPO, 2014|
|-England and Wales||Eradicated||EPPO, 2014|
|Ukraine||Absent, formerly present||CABI/EPPO, 2013; EPPO, 2014|
|Australia||Eradicated||CABI/EPPO, 2013; EPPO, 2014|
|-New South Wales||Eradicated||CABI/EPPO, 2013; EPPO, 2014|
|-Queensland||Eradicated||CABI/EPPO, 2013; EPPO, 2014|
|-South Australia||Eradicated||1994||CABI/EPPO, 2013; EPPO, 2014|
|-Victoria||Eradicated||CABI/EPPO, 2013; EPPO, 2014|
|New Zealand||Eradicated||1971||CABI/EPPO, 2013; EPPO, 2014|
Risk of IntroductionTop of page EPPO considers X. fragariae as an A2 quarantine organism (OEPP/EPPO, 1986), while IAPSC also considers it as of quarantine significance. The disease is absent from most strawberry-growing countries in Europe but probably has the potential to establish there. Indeed, the general climatic conditions which are said to favour disease in North America tend to occur in Central and Northern Europe rather than in the Mediterranean countries where X. fragariae has been recorded until now. However, the specific influence of overhead sprinkler irrigation may be more characteristic of the Mediterranean countries. X. fragariae is certainly sufficiently damaging to deserve its quarantine status.
EPPO recommends, in its specific quarantine requirements (OEPP/EPPO, 1990), that strawberry planting material from infested countries should be derived from mother plants kept free from X. fragariae as part of a certification
scheme (in preparation by EPPO), and in addition that the place of production should have been found free from the disease during the last five growing seasons. In addition, visual inspections during the dormant period can be useful. Inspectors should look for typical angular spots on old leaves or on their remains still attached to the runners. Samples from lots kept in cold storage must be inspected immediately after the runners are taken out and thawed. The spots can no longer be seen after only 1 day at room temperature.
Hosts/Species AffectedTop of page Cultivated strawberries (Fragaria ananassa) are the only host of concern. The numerous cultivars vary a great deal in susceptibility. F. virginiana, F. vesca, Potentilla fruticosa and P. glandulosa have been infected following experimental inoculation. Among Fragaria spp. only F. moschata is immune (Kennedy and King, 1962a; Kennedy, 1965; Maas, 1984).
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page Vegetative growing stage
SymptomsTop of page On leaves, 1-4 mm, angular, shiny, water-soaked spots appear surrounded by the smallest veins. In the early stage the spots are only visible on the lower surface and appear translucent against the light. They enlarge, coalesce and after about 2 weeks are also visible on the upper surface as water-soaked, angular spots, which become reddish-brown in colour. They have a shiny appearance and are usually covered by bacterial exudate which when dry turns brown and appears as gum-like scales. Spots coalesce more frequently along the primary and secondary veins. The dead tissues tear and break off, and the diseased leaf may assume a ragged appearance.
In the most severe cases crown infection pockets may be seen inside after dissection. They appear as localized, water-soaked zones, frequently confined to one side of the crown.
For more information, see Kennedy and King (1962b), Hildebrand et al. (1967), Mazzucchi et al. (1973), Panagopoulos et al. (1978) and Maas (1984).
List of Symptoms/SignsTop of page
|Growing point / rot|
|Leaves / abnormal colours|
|Leaves / necrotic areas|
Biology and EcologyTop of page Residues of infected leaves and crown infections on runners used for planting are sources of inoculum for primary infections. In the residues of infected leaves, in or on soil, the bacterium survives from one crop to the
next. In dried infected leaves, kept in the laboratory, the bacterium may survive for at least 2.5 years. Bacterial cells are transferred from residues to young leaves at the beginning of the growing season. From crown infection pockets, the bacterium causes lesions along the veins at the base of the youngest leaves, which develop in the apical crown region.
X. fragariae is exuded from primary lesions, and bacterial cells are spread by aerosols, caused by rain and sprinkler irrigation, and transported by wind to healthy leaves. Penetration occurs through the stomata. Infections of the
crowns occur through local wounds or downwards from the affected leaves. During the growing season several cycles of secondary infections may occur. The bacterium may attack flowers, but not fruits.
During epidemics, when environmental conditions favour exudation and spread, X. fragariae may cause systemic infections associated with crown pockets. Systemic infections may arise under damp nursery conditions. The
conditions favouring infection are moderate to cool daytime temperatures (about 20°C), low night-time temperatures and high humidities (Maas, 1984). For more information, see Kennedy and King (1962b), Hildebrand et al. (1967), Maas (1984).
Means of movement/dispersal
X. fragariae is spread locally by splash dispersal. Commercial strawberry runners used for planting may spread the bacterium. They may still bear old, whole or torn, infected leaves or have crown infection pockets. Moreover, almost invisible fragments of infected leaves may be hidden in the apical crown region or between the roots (Kennedy and King, 1962a).
ImpactTop of page Like other strawberry leaf blights, X. fragariae causes a certain reduction in yield, but generally the disease is not destructive. However, heavy losses may occur with frequent overhead sprinkler irrigation.
Detection and InspectionTop of page The presence of the bacterium in affected plants may be confirmed by direct isolation or indirect immunofluorescence antibody staining (IFAS) of suspensions obtained by macerating in a mortar some water-soaked spots in a small volume of distilled water (Mazzucchi et al., 1973).
Direct isolation is difficult because the growth of the bacterium is very slow and its colonies are easily overgrown by those of secondary organisms. Isolation may be successful if the suspension is streaked on yeast dextrose chalk agar plates and incubated at 27°C at high humidities. Colonies develop more frequently where a mass of cells is transferred in close association. The first colonies are visible after 4-5 days. The colonies are circular, 0.5-1.0 mm in diameter, yellow-pigmented, dome-shaped, with entire edges. The pure culture is distinguishable from other phytopathogenic xanthomonads by at least seven characteristics (no growth at 33°C; no hydrolysis of aesculin; no acid from arabinose, galactose, trehalose, cellobiose; 0.5-1.0% maximum NaCl tolerance) (Kennedy and King, 1962b; Bradbury, 1984).
IFAS can be used successfully on the concentrated suspension or on its ten-fold dilution. In positive cases millions of small, rounded fluorescent bacteria can be seen. When using differential dilutions of antiserum, no interference has yet been reported due to the existence of cross-reactions with other bacteria. Detection is quite difficult on symptomless runners (Mazzucchi and Calzolari, 1987). Any crown infection pockets can only be detected by histological examination of single runners, which is difficult to apply to large lots. Moreover the runners may be so well cleaned that any small residues of old infected leaves are almost invisible. Recently a sampling detection method for symptomless runners was studied. Cleaned crowns of the sample are cut in quarters and homogenized. The bacteria are concentrated from the thick suspension by centrifuging. IFAS is applied to the final pellet. Although the method is not very sensitive, preliminary applications were quite encouraging. ELISA has also been tried out as a detection method (Lopez et al., 1987).
See also Opgenorth et al. (1996), Zhang and Goodwin (1997) and Mahuku and Goodwin (1997).
Prevention and ControlTop of page The use of healthy planting material and avoidance of conditions favouring disease are the main control methods. Treatments with copper-containing products have some effectiveness, but have to be applied very intensively,
with a risk of phytotoxicity. Resistance to X. fragariae exists in breeding material, but not yet in commercial cultivars (Maas, 1984, 2000).
ReferencesTop of page
Bradbury JF, 1984 Xanthomonas. In: Bergey's manual of systematic bacteriology, vol. 1. Krieg NR, Holt JG, eds. Baltimore, USA: Williams & Wilkins
EPPO, 1990. Specific quarantine requirements. EPPO Technical Documents, No. 1008. Paris, France: European and Mediterranean Plant Protection Organization
EPPO, 2011. EPPO Reporting Service. EPPO Reporting Service. Paris, France: EPPO. http://archives.eppo.org/EPPOReporting/Reporting_Archives.htm
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
EPPO, 2018. EPPO Global Database (available online). https://gd.eppo.int
Fernández-Pavía SP, Rodríguez-Alvarado G, Garay-Serrano E, Cárdenas-Navarro R, 2014. First report of Xanthomonas fragariae causing angular leaf spot on strawberry plants in México. Plant Disease, 98(5):682-683. http://apsjournals.apsnet.org/loi/pdis
Gillings MR, Fahy PC, Bradley J, 1998. Identification of Xanthomonas fragariae, the cause of an outbreak of angular leaf spot on strawberry in South Australia, and comparison with the cause of previous outbreaks in New South Wales and New Zealand. Australasian Plant Pathology, 27(2):97-103; 25 ref
Hildebrand DC, Schroth MN, Wilhelm S, 1967. Systemic invasion of strawberry by Xanthomonas fragariae causing vascular collapse. Phytopathology, 57:1260-1261
Kennedy BW, 1965. Infection of Potentilla by Xanthomonas fragariae. Plant Disease Reporter, 49:491-492
Kennedy BW, King TH, 1962. Angular leaf spot of strawberry caused by Xanthomonas fragariae sp. nov. Phytopathology, 52:873-875
Kennedy BW, King TH, 1962. Studies on epidemiology of bacterial angular leaf spot on strawberry. Plant Disease Reporter, 46:360-363
Lopez MM, Aramburu JM, Cambra M, Borras V, 1985. [Detection and identification of Xanthomonas fragariae in Spain.] Anales del Instituto Nacional de Investigaciones Agrarias. Serie Agricola, 28:245-259
Maas JL, 1984. Compendium of Strawberry Diseases. St. Paul, Minnesota, USA: American Phytopathology Society
Maas JL, Gouin-Behe C, Hartung JS, Hokanson SC, 2000. Sources of resistance for two differentially pathogenic strains of Xanthomonas fragariae in Fragaria genotypes. HortScience, 35(1):128-131; 15 ref
Mahuku GS, Goodwin PH, 1997. Presence of Xanthomonas fragariae in symptomless strawberry crowns in Ontario detected using a nested polymerase chain reaction (PCR). Canadian Journal of Plant Pathology, 19(4):366-370; 12 ref
Mazzucchi U, Calzolari A, 1987. Detection of Xanthomonas fragariae in symptomless strawberry plants. Acta Horticulturae, 265:601-604
Pruvost O, FabrFgue C, Luisetti J, 1988. Mise en évidence de la maladie des taches angulaires du fraisier à l'île de la Réunion. Fruits (France), 43:369-373
Rat B, 1974. Présence en France de la maladie des taches angulaires du fraisier. Annales de Phytopathologie, 6:223
Zhang S, Goodwin PH, 1997. Rapid and sensitive detection of Xanthomonas fragariae by simple alkaline DNA extraction and the polymerase chain reaction. Journal of Phytopathology, 145(5/6):267-270; 13 ref
Distribution MapsTop of page
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