Xanthomonas fragariae
(angular leaf spot)

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Identity

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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

EPPO code

• XANTFR (Xanthomonas fragariae)

Taxonomic Tree

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• Domain: Bacteria
•     Phylum: Proteobacteria
•         Class: Gammaproteobacteria
•             Order: Xanthomonadales
•                 Family: Xanthomonadaceae
•                     Genus: Xanthomonas
•                         Species: Xanthomonas fragariae

Description

Top 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).

Distribution

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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 Table

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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.

Risk of Introduction

Top 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.


Phytosanitary measures

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 Affected

Top 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 Affected

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Growth Stages

Top of page Vegetative growing stage

Symptoms

Top 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/Signs

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Biology and Ecology

Top 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).

Impact

Top 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 Inspection

Top 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 Control

Top 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).

References

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Alippi AM, Ronco BL, Carranza MR, 1989. Angular leaf spot of strawberry, a new disease in Argentina. Comparative control with antibiotics and fungicides. Advances in Horticultural Science, 1:3-6

Bradbury JF, 1977. Xanthomonas fragariae. CMI Descriptions of Pathogenic Fungi and Bacteria No. 558. Wallingford, UK: CAB International

Bradbury JF, 1984 Xanthomonas. In: Bergey's manual of systematic bacteriology, vol. 1. Krieg NR, Holt JG, eds. Baltimore, USA: Williams & Wilkins

Bradbury JF, 1986. Guide to Plant Pathogenic Bacteria. Wallingford, UK: CAB International

Brence A, 2002. Strawberry corner. (Jagodni koticek.) SAD, Revija za Sadjarstvo, Vinogradni?tvo in Vinarstvo, 13(2):25

CABI/EPPO, 1998. Distribution maps of quarantine pests for Europe (edited by Smith IM, Charles LMF). Wallingford, UK: CAB International, xviii + 768 pp

CABI/EPPO, 2013. Xanthomonas fragariae. [Distribution map]. Distribution Maps of Plant Diseases, No.October. Wallingford, UK: CABI, Map 520 (Edition 4)

EPPO, 1986. EPPO data sheets on quarantine organisms. Bulletin OEPP/EPPO Bulletin, 16(1):13-78

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

Fernandes AMM, Pinto-Ganhao JF, 1981. Xanthomonas fragarip Kennedy & King, a bacteriosis new to Portugal. Agros, 64(1):5-8

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

Grimm R, Lips T, Vogelsanger J, 1993. Angular leaf spot of strawberries. Schweizerische Zeitschrift fur Obst- und Weinbau, 129(5):130-131

Hildebrand DC, Schroth MN, Wilhelm S, 1967. Systemic invasion of strawberry by Xanthomonas fragariae causing vascular collapse. Phytopathology, 57:1260-1261

IMI, 1993. Distribution Maps of Plant Diseases No. 253 (edition 5). Wallingford, UK: CAB International

IPPC, 2009. First finding of Xanthomonas fragariae in Estonia. IPPC Official Pest Report, EST-01/1. Rome, Italy: FAO. https://www.ippc.int/index.php?id=1110520&no_cache=1&type=pestreport&L=0

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

Lieten F, 1998. Strawberries. Bacterial disease Xanthomonas in strawberries. Proeftuinnieuws, 8(18):49-50

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

Lopez MM, Cambra M, Aramburu JM, Bolinches J, 1987. Problems of detecting phytopathogenic bacteria by ELISA. Bulletin OEPP/EPPO Bulletin, 17(1):113-117

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, Alberghina A, Dalli A, 1973. Occurrence of Xanthomonas fragariae Kennedy et King in Italy. Phytopathologische Zeitschrift, 76(4):367-370

Mazzucchi U, Calzolari A, 1987. Detection of Xanthomonas fragariae in symptomless strawberry plants. Acta Horticulturae, 265:601-604

Opgenorth DC, Smart CD, Louws FJ, Bruijn FJde, Kirkpatrick BC, 1996. Identification of Xanthomonas fragariae field isolates by rep-PCR genomic fingerprinting. Plant Disease, 80(8):868-873; 31 ref

Panagopoulos CG, Psallidas PG, Alivizatos AS, 1978. A bacterial leafspot of strawberry in Greece caused by Xanthomonas fragarip. Phytopathologische Zeitschrift, 91(1):33-38

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

Scortichini M, Rossi MP, 1994. Updating the presence of Xanthomonas fragariae in Italy. Informatore Fitopatologico, 44(6):33-35

Severin V, Stancescu C, Zambrowicz E, 1985. Angular leaf spot, a new bacterial disease of strawberry in Romania. Buletinul de Protectia Plantelor, 1-2:21-23

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 Maps

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