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Datasheet

Clavibacter michiganensis subsp. sepedonicus
(Potato ring rot)

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Datasheet

Clavibacter michiganensis subsp. sepedonicus (Potato ring rot)

Summary

  • Last modified
  • 22 November 2019
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Clavibacter michiganensis subsp. sepedonicus
  • Preferred Common Name
  • Potato ring rot
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Actinobacteria [phylum]
  •     Class: Actinobacteria
  •       Subclass: Actinobacteridae
  •         Order: Actinomycetales
  • Summary of Invasiveness
  • Clavibacter michiganensis subsp. sepedonicus has the propensity to exist asymptomatically as latent infections in potato (Solanum tuberosum); it is not known to naturally infect other plant species. Inadvertent dissemina...

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Pictures

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PictureTitleCaptionCopyright
Foliage symptoms usually first become apparent as a wilt on the lower leaves. Margins of symptomatic leaves often curl upwards and interveinal areas become pale green to yellowish and develop necrotic areas.
TitleSymptoms on leaves
CaptionFoliage symptoms usually first become apparent as a wilt on the lower leaves. Margins of symptomatic leaves often curl upwards and interveinal areas become pale green to yellowish and develop necrotic areas.
CopyrightS.H. de Boer, Agriculture Canada
Foliage symptoms usually first become apparent as a wilt on the lower leaves. Margins of symptomatic leaves often curl upwards and interveinal areas become pale green to yellowish and develop necrotic areas.
Symptoms on leavesFoliage symptoms usually first become apparent as a wilt on the lower leaves. Margins of symptomatic leaves often curl upwards and interveinal areas become pale green to yellowish and develop necrotic areas.S.H. de Boer, Agriculture Canada

Identity

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Preferred Scientific Name

  • Clavibacter michiganensis subsp. sepedonicus (Spieckermann & Kotthoff) Dye & Kemp

Preferred Common Name

  • Potato ring rot

Other Scientific Names

  • Aplanobacter sepedonicus (Spieckermann & Kotthoff) Smith 1920
  • Bacterium sepedonicum Spieckermann & Kotthoff 1914
  • Corynebacterium michiganense pv. sepedonicum (Spieckermann & Kotthoff) Dye & Kemp 1977
  • Corynebacterium michiganense subsp. sepedonicum (Spieckermann & Kotthoff 1914) Carlson & Vidaver 1982
  • Corynebacterium sepedonicum (Spieckermann & Kotthoff 1914) Skaptason & Burk. 1942
  • Mycobacterium sepedonicum (Spieckermann & Kotthoff) Krasil'nikov 1949
  • Phytomonas sepedonica (Spieckermann & Kotthoff) Magrou 1937
  • Pseudobacterium sepedonicum (Spieckermann & Kotthoff) Krasil'nikov 1949

International Common Names

  • English: bacterial ring rot of potato; ring rot of potato; vascular potato wilt
  • Spanish: bacteriosis anular de la papa; podredumbre anular de la papa
  • French: bactériose annulaire de la pomme de terre; fletrissement bacterien de la pomme de terre; pourriture annulaire de la pomme de terre

Local Common Names

  • Germany: Bakterielle: Kartoffel Ringfaeule; Bakterienringfaeule: Kartoffel; Ringbakteriose: Kartoffel

EPPO code

  • CORBSE (Clavibacter michiganensis subsp. sepedonicus)

Summary of Invasiveness

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Clavibacter michiganensis subsp. sepedonicus has the propensity to exist asymptomatically as latent infections in potato (Solanum tuberosum); it is not known to naturally infect other plant species. Inadvertent dissemination of the bacterium to new places of production occurs with the movement of latently infected seed tubers used for planting. The bacterium also spreads from infected tubers through direct contact and by contamination of equipment used for potato production such as seed cutters, planters, harvesters, transport vehicles, storages, etc. C. michiganensis subp. sepedonicus survives for extended periods of many months to years in a dry and cool environment. Hence its persistence on farm equipment, in storages, and on transport vehicles is an important means by which the bacterium is maintained and spread within farm units and disseminated to other production units. It persists in the field in unharvested potato tubers (i.e. volunteers or ground keepers) and in infected potato plant debris.

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Actinobacteria [phylum]
  •         Class: Actinobacteria
  •             Subclass: Actinobacteridae
  •                 Order: Actinomycetales
  •                     Suborder: Micrococcineae
  •                         Family: Microbacteriaceae
  •                             Genus: Clavibacter
  •                                 Species: Clavibacter michiganensis subsp. sepedonicus

Description

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C. michiganensis subsp. sepedonicus is a short, non-motile, Gram-positive rod-shaped bacterium (Hayward and Waterston, 1964). Gram-stained cells may appear slightly club-shaped and have a tendency to be in pairs in L- or V-formation. Cells from fresh isolates grown on laboratory medium are sometimes quite pleomorphic with cell morphologies ranging from large globose forms to the typical short, slightly club-shaped rods.

Distribution

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See also CABI/EPPO (1998, No. 254).

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.

Last updated: 17 Feb 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

AlgeriaAbsent, Formerly present
EgyptAbsent, Unconfirmed presence record(s)

Asia

AfghanistanAbsent, Unconfirmed presence record(s)
CambodiaAbsent, Unconfirmed presence record(s)
ChinaPresent, Localized
-AnhuiPresent
-HebeiPresent
-HeilongjiangPresent
-HenanPresent
-JiangsuPresent
-NingxiaPresent
-ShaanxiPresent
-YunnanPresent
-ZhejiangPresent
IsraelAbsent, Confirmed absent by survey
JapanPresent
KazakhstanPresent
LebanonAbsent, Unconfirmed presence record(s)
NepalPresent
North KoreaPresent
PakistanPresent
South KoreaPresent
TaiwanPresent
TurkeyPresent, Few occurrences
UzbekistanPresent
VietnamAbsent, Unconfirmed presence record(s)

Europe

AustriaAbsent, Eradicated
BelarusPresent
BelgiumAbsent, Eradicated
Bosnia and HerzegovinaAbsent, Confirmed absent by survey
BulgariaPresent, Few occurrences
CroatiaAbsent, Confirmed absent by survey
CyprusAbsent, Eradicated
CzechiaPresent, Localized1996
DenmarkAbsent, Eradicated
EstoniaPresent, Localized
FinlandPresent, Localized
FranceAbsent, Eradicated
GermanyPresent, Localized1984
GreecePresent, Localized
-CretePresent, Widespread
HungaryPresent, Few occurrences
IrelandAbsent, Confirmed absent by survey
ItalyAbsent, Confirmed absent by survey
LatviaPresent, Localized
LithuaniaPresent, Localized
MaltaAbsent, Confirmed absent by survey
NetherlandsPresent, Transient under eradication
NorwayPresent, Localized
PolandPresent, Localized
RomaniaPresent, Localized
RussiaPresent, Widespread
-Central RussiaPresent
-Eastern SiberiaPresent
-Northern RussiaPresent
-Russia (Europe)Present
-SiberiaPresent
-Western SiberiaPresent
SlovakiaPresent, Few occurrences
SloveniaAbsent, Confirmed absent by survey
SpainPresent, Few occurrences
-Balearic IslandsAbsent, Confirmed absent by survey
-Canary IslandsAbsent, Confirmed absent by survey
SwedenPresent, Localized
SwitzerlandAbsent, Unconfirmed presence record(s)
UkrainePresent, Widespread
United KingdomAbsent, Eradicated
-EnglandAbsent, Eradicated
-ScotlandAbsent, Confirmed absent by survey

North America

CanadaPresent, Widespread
-AlbertaPresent
-British ColumbiaPresent
-ManitobaPresent
-New BrunswickPresent
-Newfoundland and LabradorPresent
-Nova ScotiaPresent
-OntarioPresent
-Prince Edward IslandPresent, Few occurrences
-QuebecPresent
-SaskatchewanPresent
Costa RicaAbsent, Unconfirmed presence record(s)
HaitiAbsent, Unconfirmed presence record(s)
MexicoPresent
PanamaAbsent, Unconfirmed presence record(s)
United StatesPresent, Localized
-ColoradoPresent
-IdahoPresent
-KansasPresent
-MainePresent
-New YorkPresent
-North DakotaPresent
-OregonPresent
-WashingtonPresent
-WisconsinPresent

South America

PeruAbsent, Invalid presence record(s)
VenezuelaAbsent, Invalid presence record(s)

History of Introduction and Spread

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Bacterial ring rot disease of potato was first described in Germany in 1905 (Appel, 1906) and the causal agent given the name of Bacterium sepedonicum (Spieckermann and Kotthoff, 1914). In 1932 the disease was reported in Norway (Jorstad, 1932) and was known to be present in Sweden prior to 1956 when it was widespread in seed and ware potatoes (Olsson, 1976). It was reported to be present in France by 1934 but may have been present for a longer period of time, having been misidentified as Verticillium wilt (Lansade, 1942). In 1940 it was noted that the disease was present in Russia (Belova, 1940).

In 1931 the disease occurred in Canada, in the province of Quebec, and in 1937-1938 was known to exist in the provinces of Alberta, Manitoba, Nova Scotia, Ontario, Prince Edward Island and Saskatchewan; and in 1943 it was reported in British Columbia (Racicot, 1944). In the USA it was first reported from Maine in 1932, in Wisconsin in 1936, and in Wyoming and Colorado in 1938 (Starr and Riedl, 1941). By 1939 the disease had been reported from 27 states and by 1948 from 45 states of the USA (Baribeau, 1948).

Risk of Introduction

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Risk Criteria: Category

Economic Importance: High (potato), Low (sugarbeet)
Distribution: Limited
Seedborne Incidence: Not recorded (potato), Yes (sugarbeet)
Seed Transmitted: Not recorded
Seed Treatment: None

Overall Risk: High (potato) Low (sugarbeet)


Notes on Phytosanitary Risk

C. michiganensis subsp. sepedonicus is listed as an A2 quarantine pest by EPPO. It is considered of quarantine significance throughout Europe, for example, by APPPC and IAPSC, and also in North America (COSAVE, JUNAC). Several seed-potato-producing countries in the EPPO region, and Mediterranean countries exporting ware potatoes to the north, are free from the pathogen. While the direct economic impact of ring rot would be moderate, especially where modern production systems are in place, it would constitute an additional constraint on seed potato production in countries where it does not occur, with considerable indirect effects on trade.

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial ManagedCultivated / agricultural land Secondary/tolerated habitat Productive/non-natural
OtherHost Principal habitat Harmful (pest or invasive)

Hosts/Species Affected

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Natural infection causing disease has been found only on potatoes. Sugarbeet has been described as a natural symptomless host; C. michiganensis subsp. sepedonicus has been isolated from sugarbeet seed and roots (Bugbee and Gudmestad, 1988). An unconfirmed report suggests that the bacterium may be associated with Solanum sarrachoides (hairy nightshade) (Zizz and Harrison, 1991). In inoculation tests many members of the Solanaceae, including tomatoes and aubergines, were found to be susceptible.

In the EPPO region, only potatoes are considered a significant host.

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Beta vulgaris var. saccharifera (sugarbeet)ChenopodiaceaeOther
    Solanum lycopersicum (tomato)SolanaceaeOther
      Solanum tuberosum (potato)SolanaceaeMain

        Growth Stages

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        Flowering stage, Fruiting stage, Post-harvest, Vegetative growing stage

        Symptoms

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        Potato cultivars vary greatly in their propensity to show symptoms. Foliage symptoms develop from mid to late season and usually first become apparent as a wilt on the lower leaves. Margins of symptomatic leaves often curl upwards and interveinal areas become pale green to yellowish and develop necrotic areas. Symptoms may occur on only one or a few stems of a plant and proceed upwards from the lower leaves until the entire stem is wilted. Severely infected plants die prematurely. Certain cultivars sometimes develop a rosette-like symptom characterized by short internodes without the presence of wilt. Exudation of white ooze from freshly cut cross-sections of lower stems is considered diagnostic for the disease. Symptoms are readily obscured by other wilts and foliage diseases, and natural senescence.

        The primary tuber symptom is discoloration of the vascular tissue at the stolon end and is most readily observed in tuber cross-sections. Discoloration varies from creamy-yellow to brown zones encompassing all or only a portion of the vascular ring. When pressure is applied to a cut tuber, a creamy odourless ooze may be expressed from the tissue. Distinctive corky-brown tissue sometimes surrounds hollows that develop in the vascular ring. Advanced infections are often modified by proliferation of secondary micro-organisms which obliterates typical ring rot symptoms. External tuber symptoms, apparent as reddish to brown blotches and/or surface cracks, are sometimes but not always present in severe infections. Tuber symptoms may be confused with those caused by the bacterium Ralstonia solanacearum.

        Symptomless foliage and tubers may harbour latent infections (Franc, 1999). Although some cultivars have a much greater tendency than others to remain symptomless upon infection, all cultivars can potentially serve as latent carriers of the pathogen. Latent infections can be detected by laboratory tests (see Detection and Inspection Methods).

        List of Symptoms/Signs

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        SignLife StagesType
        Leaves / abnormal colours
        Leaves / abnormal forms
        Leaves / necrotic areas
        Leaves / wilting
        Stems / internal red necrosis
        Stems / stunting or rosetting
        Vegetative organs / internal rotting or discoloration
        Vegetative organs / surface cracking
        Vegetative organs / surface lesions or discoloration
        Whole plant / plant dead; dieback

        Biology and Ecology

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        Seed potato tubers infected or contaminated with C. michiganensis subsp. sepedonicus are the primary source of infection. The bacteria migrate from the seed tuber to the stems via the vascular tissue, and subsequently into progeny tubers through the stolons. The pathogen population density increases during the growing season but sometimes can be detected in stems within 3 to 4 weeks after planting infected seed (De Boer and McCann, 1989). C. michiganensis subsp. sepedonicus does not survive well in soil but can overwinter in the field in volunteer tubers (ground keepers) and in potato tissue debris. The bacterium survives particularly well when dried in smears of decayed tuber tissue on equipment, machinery, potato sacks and storage bins. The bacterium remained infectious in the dried state for at least 18 months at temperatures from 5°C to -40°C (Nelson, 1984). C. michiganensis subsp. sepedonicus has been reported to be associated with sugarbeet and solanaceous weeds, but the role of these potential inoculum sources in the epidemiology of the ring rot disease of potato is unclear at this time. C. michiganensis subsp. sepedonicus has a low optimum growth temperature (21-23°C) and is confined mainly to cooler potato growing regions. The climate in north and central Europe, the northern USA, and Canada appears to favour the disease.

        Climate

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        ClimateStatusDescriptionRemark
        C - Temperate/Mesothermal climate Preferred Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C

        Means of Movement and Dispersal

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        Infected tubers are the main source of C. michiganensis subsp. sepedonicus and the pathogen is spread to other tubers by direct contact or via contamination of machinery and other equipment with which potatoes come in contact. Cutting knives and picker-type planters are particularly prone to spread infection. Spread of the pathogen on contaminated grading machines and transport trucks is also important. Plant-to-plant spread in the field is usually low (Mansfield-Giese, 1997) but there is experimental evidence that insects can transmit the disease (Christie et al., 1991). Infected volunteer plants may also serve as a source of infection.

        Seedborne Aspects

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        C. michiganensis subsp. sepedonicus occurs in seed tubers produced from infected potato plants, the primary host of this pathogen, as well as the seeds itself (Gudmestad et al., 2009).

        Pathogenic strains of C. michiganensis subsp. sepedonicus were recovered from sugarbeet seeds produced in the Willamette Valley, Oregon, USA, in 1984. The bacterium was isolated directly from culture plates of diluted sugarbeet seed extracts and from aubergines that had been inoculated with sugarbeet seed strains of the pathogen. All strains from sugarbeet seed were pathogenic to potatoes and aubergines. Indirect immunofluorescent antibody staining (IFAS) using highly specific monoclonal antibodies detected the pathogen in seed extracts (Bugbee and Gudmestad, 1988). C. michiganensis subsp. sepedonicus is not recognized as a pathogen of sugarbeet.

        Pathway Causes

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        CauseNotesLong DistanceLocalReferences
        Breeding and propagation Yes Franc (1999)
        Seed trade Yes Yes Boer et al. (2005); Boer SHde (1987)

        Pathway Vectors

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        VectorNotesLong DistanceLocalReferences
        Clothing, footwear and possessionsTransfer of tubers. Yes
        Containers and packaging - wood Yes
        Land vehiclesSoil on machinery. Yes
        Plants or parts of plantsPotato tuber Yes Yes
        Soil, sand and gravelTransfer of tubers. Yes

        Plant Trade

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        Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
        Bulbs/Tubers/Corms/Rhizomes Yes Pest or symptoms usually invisible
        Growing medium accompanying plants Yes Pest or symptoms usually invisible
        Leaves Yes Pest or symptoms usually invisible
        Roots Yes Pest or symptoms usually invisible
        Seedlings/Micropropagated plants Yes Pest or symptoms usually invisible
        Stems (above ground)/Shoots/Trunks/Branches Yes Pest or symptoms usually invisible
        Plant parts not known to carry the pest in trade/transport
        Bark
        Flowers/Inflorescences/Cones/Calyx
        Fruits (inc. pods)
        True seeds (inc. grain)
        Wood

        Wood Packaging

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        Wood Packaging not known to carry the pest in trade/transport
        Loose wood packing material
        Non-wood
        Processed or treated wood
        Solid wood packing material with bark
        Solid wood packing material without bark

        Impact Summary

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        CategoryImpact
        Cultural/amenity Negative
        Economic/livelihood Negative

        Impact

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        C. michiganensis subsp. sepedonicus causes early death of plants, rotting of progeny tubers and extensive yield reduction. A high level of infection can cause total crop loss. However, with current certification practices for seed potatoes, the disease occurs only sporadically and generally at low levels in regions where the disease is endemic. Economic losses for seed crops are usually a result of loss of certification and requirements for disinfection of equipment and stores. Seed certification programmes have a zero tolerance for bacterial ring rot, so all lots with even a trace of the disease lose certified status and in some countries loss of certification extends to all potato crops produced by the farm. In ware crops economic losses are due to yield reduction and decay in storage, and sometimes loss of markets.

        Economic Impact

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        Introduction of the bacterium to a production unit could, in a worst case scenario, cause total loss of a potato crop. Potato crops grown for seed are not certified, or are decertified, upon finding the bacterium associated with the production unit resulting in concomitant reduction in value or non-saleability of the crop. Additionally, production units found to be contaminated with the bacterium must bear the cost of clean-up, disinfection, and the purchase of new seed.

        Social Impact

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        Contamination of a production unit with the bacterium has negative social impact for the producer, on account of the risk of spread of the bacterium to other units, and reluctance of seed growers to purchase from such a production unit.

        Risk and Impact Factors

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        Invasiveness
        • Benefits from human association (i.e. it is a human commensal)
        • Long lived
        • Has high reproductive potential
        • Has propagules that can remain viable for more than one year
        • Reproduces asexually
        Impact outcomes
        • Host damage
        • Infrastructure damage
        • Negatively impacts agriculture
        • Negatively impacts cultural/traditional practices
        • Negatively impacts livelihoods
        Impact mechanisms
        • Pest and disease transmission
        • Pathogenic
        Likelihood of entry/control
        • Highly likely to be transported internationally accidentally
        • Difficult to identify/detect as a commodity contaminant
        • Difficult to identify/detect in the field
        • Difficult/costly to control

        Detection and Inspection

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        Detection of ring rot by visual field inspection of potato foliage is hampered by latency of the disease, late development of symptoms, the presence of other diseases, and senescence. Similarly the detection of the disease by post-harvest tuber inspection is limited by the presence of symptomless infections and secondary decay. However, when typical symptoms are present, the disease can readily be confirmed by application of the Gram stain or a serological test which, when positive, reveals the presence of many Gram-positive bacteria or specific antigen, respectively (Manzer and Slack, 1979).

        Latent infections can be detected by several serological tests including immunofluorescence, ELISA and latex agglutination. Specificity of the serological tests depends on the antibodies used; specific monoclonal antibodies for detection by immunofluorescence and ELISA are available (De Boer et al., 1996). For unequivocal determination of latent infection, positive serological results can be confirmed by bioassay on aubergine and isolation of C. michiganensis subsp. sepedonicus (Anon., 1987). Laboratory protocols for testing composite samples of tubers or stems for possible latent ring rot infections have been established (De Boer and Hall, 2000).

        DNA-based detection methods involving DNA amplification by the polymerase chain reaction have been developed but are not yet widely used (Li and De Boer, 1995; Mills et al., 1997; Schneider et al., 1993). Additional sensitivity can be achieved by the use of nested or real time PCR (Lee et al., 1997; Schaad et al., 1999). These technologies probably have greater potential for confirming preliminary diagnoses rather than as routine detection methods.

        A method for inspection, detection (of latent infections) and identification of the pathogen has been described by OEPP/EPPO (1990b).

        The development of an enzyme-linked immunosorbent assay on nitrocellulose membranes (NCM-ELISA), which allows for the rapid testing and diagnosis of potato ring rot, is detailed in Hu et al. (2007).

        Similarities to Other Species/Conditions

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        Symptoms on potato tubers may be confused with those caused by Ralstonia solanacearum. The two may be distinguished by a bacterial ooze that often emerges from the eyes and stem-end attachment of R. solanacearum-infected tubers. When this bacterial exudate dries, soil may adhere to the tubers at the eyes.

        Prevention and Control

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        Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

        Control is achieved primarily through strict application of seed certification rules with a zero tolerance for the disease. By laboratory testing for latent infections, infected lots can be detected early and eliminated from seed programmes before further spread of the pathogen occurs. Implementation of crop rotation, disinfection and other sanitation practices is most important whenever the disease has occurred to prevent recurrence of the disease and spread of the pathogen. Disinfectants such as quaternary ammonia, chlorine, iodine or phenol-containing compounds applied to equipment and other contaminated surfaces for a minimum of 10 min under low organic load are effective against C. michiganensis subsp. sepedonicus (Secor et al., 1988). The peracids, Degaclean and Clarmarin, in combination with the catalase inhibitor KH10 destroyed C. michiganensis subsp. sepedonicus in waste water from a commercial potato processing plant (Niepold, 1999). The use of whole rather than cut seed and avoidance of picker-type planters helps to reduce the spread of the disease.

        Micropropagation of potato under aseptic conditions and in combination with laboratory testing for C. michiganensis subsp. sepedonicus, can be used to establish ring rot free production schemes.

        No immune cultivars are available and the use of tolerant cultivars is discouraged because they could serve as symptomless carriers of the pathogen.

        Phytosanitary measures must be aimed at the entire potato production system on account of the insidious nature of the disease. Consideration must be given to the use of micropropagated material, implementation of field inspection and laboratory testing, seed potato certification, and regional geographic isolation. In addition, inspection of individual consignments is warranted.

        EPPO's specific quarantine requirements for C. michiganensis subsp. sepedonicus (OEPP/EPPO, 1990a) recommend that seed potatoes be imported only from countries which can show, by surveys and tests, that they operate a seed-potato production and distribution system free from ring rot. Laboratory testing for latent infections by the EPPO-recommended method (OEPP/EPPO, 1990b) is required. These restrictions apply both to countries where ring rot is present but does not enter the particular seed-potato production system under consideration and also to countries where ring rot has never been recorded. All seed and ware potatoes must come from stock and a place of production that is free from ring rot, and from a field inspected during the last growing season (or two growing seasons if the previous crop was also potatoes) and found free from ring rot. Applicable sanitary precautions must be taken in storage and packing houses. Only new or disinfected packing material and containers must be used.

        References

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        ===, 1978. Data sheets on quarantine organisms. Set 1. Bulletin, Organisation Europeenne et Mediterraneenne pour la Protection des Plantes, 8(2)

        1990. Quarantine procedure No. 25. Clavibacter michiganensis subsp. sepedonicus. Inspection and test methods. Bulletin OEPP, 20(2):235-254

        Altundag S, Karahan A, KIlInç AO, Özakman M, 2009. First report of Clavibacter michiganensis subsp. sepedonicus causing bacterial ring rot of potato in Turkey. Plant Pathology, 58(4):794. http://www.blackwell-synergy.com/loi/ppa

        Anon., 1987. Scheme for the detection and diagnosis of the ring rot bacterium Corynebacterium sepedonicum in batches of seed potatoes. EUR 11288. Luxembourg: Office for Official Publications of the European Communities.

        Appel O, 1906. [English title not available]. (Neuere Untersuchungen uber Kartoffel und Tomatenerkrankungen.) Jahresber. Ver. Agew. Bot, 3:122-136

        BARIBEAU B, 1948. Bacterial ring rot of potatoes. American Potato Journal, 25:71-82

        Belova OD, 1940. Ring rot of potato and its control (in Russian). Lenin Acad. Agr. Sci, 19:21-26

        Bhutta AR, 2008. Survey of tuber borne diseases of potato in Northern Areas, Pakistan. Pakistan Journal of Phytopathology [Papers presented at the 3rd International Conference of Plant Pathology, Lahore, Pakistan, 19-21 November 2007.], 20(1):20-33

        Boer SHde, 1987. The relationship between bacterial ring rot and North American seed potato export markets. In: American Potato Journal, 64(12). 683-694

        Boer SHde, Boucher A, Haan TLde, 1996. Validation of thresholds for serological tests that detect Clavibacter michiganensis subsp. sepedonicus in potato tuber tissue. Bulletin OEPP, 26(2):391-398; 10 ref

        Boer SHDe, Charkowski AO, Zink RT, Martinez-Soriano JP, Flores-Olivas A, 2005. Procedure for detection and identification of Clavibcter michiganensis subsp. sepedonicus (Spieckermann and Kotthoff) Davis, Gillaspie, Vidaver and Harris, in potato (Solanum tuberosum L.) tubers. Revista Mexicana de Fitopatologia, 23:329-334

        Boer SHde, Hall JW, 2000. Proficiency testing in a laboratory accreditation program for the bacterial ring rot pathogen of potato. Plant Disease, 84(6):649-653; 15 ref

        Boer SHde, McCann M, 1989. Determination of population densities of Corynebacterium sepedonicum in potato stems during the growing season. Phytopathology, 79(9):946-951; 27 ref

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

        Bugbee WM, Gudmestad NC, 1988. The recovery of Corynebacterium sepedonicum from sugar beet seed. Phytopathology, 78(2):205-208; 13 ref

        Bugbee WM, Gudmestad NC, Secor GA, Nolte P, 1987. Sugar beet as a symptomless host for Corynebacterium sepedonicum.. Phytopathology, 77(5):765-770; 19 ref

        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, 2006. Clavibacter michiganensis subsp. sepedonicus. Distribution Maps of Plant Diseases, No. 20. Wallingford, UK: CAB International

        Christie RD, Sumalde AC, Schulz JT, Gudmestad NC, 1991. Insect transmission of the bacterial ring rot pathogen. American Potato Journal, 68(6):363-372; 17 ref

        EPPO, 1990. Specific quarantine requirements. EPPO Technical Documents, No. 1008. Paris, France: European and Mediterranean Plant Protection Organization

        EPPO, 1992. Quarantine pests for Europe. Wallingford, UK: CAB International, 210-212

        EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

        EPPO, 2015. Clavibacter michiganensis subsp. sepedonicus does not occur in Egypt. EPPO Reporting Service, no. 09-2015. EPPO, Num. article: 2015/162. [EPPO Reporting Service, no. 09-2015, Num. article: 2015/162.] https://gd.eppo.int/reporting/article-5108

        EPPO, 2016. EPPO Global database (available online). Paris, France: EPPO. https://gd.eppo.int/

        EPPO/CABI, 1997. Clavibacter michiganensis subsp. sepedonicus. In: Quarantine Pests for Europe [ed. by Smith, I. M. \McNamara, D. G. \Scott, P. R. \Holderness, M.]. Wallingford, UK: CAB International

        Franc GD, 1999. Persistence and latency of Clavibacter michiganensis subsp. sepedonicus in field-grown seed potatoes. Plant Disease, 83(3):247-250; 17 ref

        Gudmestad NC, Mallik I, Pasche JS, Anderson NR, Kinzer K, 2009. A real-time PCR assay for the detection of Clavibacter michiganensis subsp. sepedonicus based on the cellulase A gene sequence. Plant Disease, 93(6):649-659. http://apsjournals.apsnet.org/loi/pdis

        Hayward AC, Waterston JM, 1964. Corynebacterium sepedonicum. CMI Descriptions of Pathogenic Fungi and Bacteria No. 14. Wallingford, UK: CAB International

        Hu LinShuang, Wang XiaoDan, Min FanXiang, Guo Mei, Li XueZhan, Bai YanJu, 2007. Establishment of NCM-ELISA (enzyme-linked immunosorbent assay on nitrocellulose membranes) for rapid test of potato ring rot. Chinese Potato Journal, 21(3):142-145

        Ignatov, A. N., Panycheva, J. S., Spechenkova, N., Taliansky, M., 2018. First report of Clavibacter michiganensis subsp. sepedonicus infecting sugar beet in Russia. Plant Disease, 102(12), 2634-2635. http://apsjournals.apsnet.org/loi/pdis doi: 10.1094/PDIS-04-18-0693-PDN

        Jorstad I, 1932. Beretning om planteskdemmer i land-og-hage bruket VII. Sopp-og. bakteriesykdommer pa potater. Landbruksdircktorens beretning. Tillegg, C:-63

        Lansade M, 1942. La maladie du Fletrissement Bacterien de la pomme de terre. Jour. La Pomme de Terre Francaise, 41

        Lee IM, Bartoszyk IM, Gundersen DE, Mogen B, Davis RE, 1997. Nested PCR for ultrasensitive detection of the potato ring rot bacterium, Clavibacter michiganensis subsp. sepedonicus. Applied and Environmental Microbiology, 63(7):2625-2630; 30 ref

        Li Xiang, Boer SHde, 1995. Selection of polymerase chain reaction primers from an RNA intergenic spacer region for specific detection of Clavibacter michiganensis subsp. sepedonicus. Phytopathology, 85(8):837-842

        Mansfeld-Giese K, 1997. Plant-to-plant transmission of the bacterial ring rot pathogen Clavibacter michiganensis subsp. sepedonicus. Potato Research, 40(2):229-235; 19 ref

        Manzer FE, Slack SA, 1979. Report of the pathology section committee on bacterial ring rot diagnosis. American Potato Journal, 56:551-555

        Mills D, Russell BW, Hanus JW, 1997. Specific detection of Clavibacter michiganensis subsp. sepedonicus by amplification of three unique DNA sequences isolated by subtraction hybridization. Phytopathology, 87(8):853-861; 45 ref

        Nelson GA, 1984. Survival of Corynebacterium sepedonicum in potato stems and on surfaces held at freezing and above-freezing temperatures. American Potato Journal, 62(1):23-28; [2 tab.]; 13 ref

        Niepold F, 1999. Efficiency surveys of the peracids Degaclean and Clarmarin in combination with the catalase inhibitor KH10 from the Degussa company for eradicating the two quarantine bacteria Clavibacter michiganensis ssp. sepedonicus and Ralstonia solanacearum in an aqueous suspension and in the sewage water of the starch industry. Journal of Phytopathology, 147(11-12):625-634; 25 ref

        OEPP/EPPO, 2006. Clavibacter michiganensis subsp. sepedonicus. Diagnostic protocols for regulated pests, PM7/59(1). EPPO Bulletin, 36(1):99-109

        Olsson K, 1976. Experience of ring rot caused by Corynebacterium sepedonicum (Spieck. et Kotth.) Skapt. et Burkh. in Sweden. Particularly detection of the disease in its latent form. EPPO Bulletin [Olsson, K. : Experience of brown rot caused by Pseudomonas solanacearum (Smith) Smith in Sweden.], 6(4):209-219

        Racicot HN, 1944. The present status of bacterial ring rot in Canada. In: Canadian Phytopathological Society Symposium on Bacterial Ring Rot of Potatoes. 1-10

        Rueda Puente EO, Duarte Medina M, Alavarado Martínez AG, García Ortega AM, Tarazón Herrera MA, Holguín Peña RJ, Murillo Amador B, García Hernández JL, Flores Hernández A, Orona Castillo I, 2010. Clavibacter michiganensis ssp. sepedonicus: a bacterial disease in potato crop (Solanum tuberosum L.) in Sonora, México. (Clavibacter michiganensis ssp. sepedonicus: una enfermedad bacteriana en el cultivo de papa (Solanum tuberosum L.) en Sonora, México.) Tropical and Subtropical Agroecosystems, 10(2):169-175. http://www.veterinaria.uady.mx/ojs/index.php/TSA/article/view/148/34

        Schaad NW, Berthier-Schaad Y, Sechler A, Knorr D, 1999. Detection of Clavibacter michiganensis subsp. sepedonicus in potato tubers by BIO-PCR and an automated real-time fluorescence detection system. Plant Disease, 83(12):1095-1100; 23 ref

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        Secor GA, DeBuhr L, Gudmestad NC, 1988. Susceptibility of Corynebacterium sepedonicum to disinfectants in vitro.. Plant Disease, 72(7):585-588; 24 ref

        Seleim M, Abo-Elyousr K, Mohamed A, Saead F, 2014. First report of potato bacterial ring rot caused by Clavibacter michiganensis subsp. sepedonicus in Africa. New Disease Reports, 30:15. http://www.ndrs.org.uk/article.php?id=030015

        Smith IM, McNamara DG, Scott PR, Holderness M, 1997. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization. Quarantine pests for Europe. Second Edition. Data sheets on quarantine pests for the European Union and for the European and Mediterranean Plant Protection Organization., Ed. 2:vii + 1425 pp.; many ref

        Spieckermann A, Kotthoff P, 1914. Untersuchunger uber die Kartoffelpflanze und ihre Krankheiten. I. Die Bakterienringfaule der Kartoffelpflanze. Landw. Jahrb, 46:659-732

        Starr GH, Riedl WA, 1941. Bacterial ring-rot of potatoes. Wyoming Agricultural Experiment Station Bulletin, 244:3-12

        Vaerenbergh Jvan, Paepe Bde, Hoedekie A, Malderghem Cvan, Zaluga J, Vos Pde, Maes M, 2016. Natural infection of Clavibacter michiganensis subsp. sepedonicus in tomato (Solanum tuberosum). New Disease Reports, 33:7. http://www.ndrs.org.uk/pdfs/033/NDR_033007.pdf

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        Distribution References

        Altundağ Ș, Karahan A, Kılınç A O, Özakman M, 2009. First report of Clavibacter michiganensis subsp. sepedonicus causing bacterial ring rot of potato in Turkey. Plant Pathology. 58 (4), 794. http://www.blackwell-synergy.com/loi/ppa DOI:10.1111/j.1365-3059.2009.02034.x

        Bhutta A R, 2008. Survey of tuber borne diseases of potato in Northern Areas, Pakistan. Pakistan Journal of Phytopathology. 20 (1), 20-33.

        Bradbury J F, 1986. Guide to plant pathogenic bacteria. Farnham Royal, Slough, UK: CAB International. xviii + 332pp.

        CABI, EPPO, 1997. Clavibacter michiganensis subsp. sepedonicus. [Distribution map]. In: Distribution Maps of Plant Diseases, Wallingford, UK: CAB International. Map 20. DOI:10.1079/DMPD/20066500020

        CABI, Undated. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

        EPPO, 2020. EPPO Global database. In: EPPO Global database, Paris, France: EPPO. https://gd.eppo.int/

        Ignatov A N, Panycheva J S, Spechenkova N, Taliansky M, 2018. First report of Clavibacter michiganensis subsp. sepedonicus infecting sugar beet in Russia. Plant Disease. 102 (12), 2634-2635. http://apsjournals.apsnet.org/loi/pdis DOI:10.1094/PDIS-04-18-0693-PDN

        NPPO of the Netherlands, 2013. Pest status of harmful organisms in the Netherlands., Wageningen, Netherlands:

        Rueda Puente E O, Duarte Medina M, Alavarado Martínez A G, García Ortega A M, Tarazón Herrera M A, Holguín Peña R J, Murillo Amador B, García Hernández J L, Flores Hernández A, Orona Castillo I, 2010. Clavibacter michiganensis ssp. sepedonicus: a bacterial disease in potato crop (Solanum tuberosum L.) in Sonora, México. (Clavibacter michiganensis ssp. sepedonicus: una enfermedad bacteriana en el cultivo de papa (Solanum tuberosum L.) en Sonora, México.). Tropical and Subtropical Agroecosystems. 10 (2), 169-175. http://www.veterinaria.uady.mx/ojs/index.php/TSA/article/view/148/34

        Seleim M, Abo-Elyousr K, Mohamed A, Saead F, 2014. First report of potato bacterial ring rot caused by Clavibacter michiganensis subsp. sepedonicus in Africa. New Disease Reports. 15. http://www.ndrs.org.uk/article.php?id=030015

        Vaerenbergh J van, Paepe B de, Hoedekie A, Malderghem C van, Zaluga J, Vos P de, Maes M, 2016. Natural infection of Clavibacter michiganensis subsp. sepedonicus in tomato (Solanum tuberosum). New Disease Reports. 7. http://www.ndrs.org.uk/pdfs/033/NDR_033007.pdf

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        21/12/2007 Updated by:

        Solke de Boer, Centre for Animal & Plant Health, 93 Mount Edward Road, Charlottetown, Prince Edward Island, C1A 5T1, Canada

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