Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Clavibacter sepedonicus
(potato ring rot)

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Datasheet

Clavibacter sepedonicus (potato ring rot)

Summary

  • Last modified
  • 16 November 2021
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Clavibacter sepedonicus
  • Preferred Common Name
  • potato ring rot
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Actinobacteria [phylum]
  •     Class: Actinobacteria
  •       Subclass: Actinobacteridae
  •         Order: Actinomycetales
  • Summary of Invasiveness
  • Clavibacter sepedonicus is one of the few major plant pathogens which is not widely distributed in the area where the main host crop (potato) evolved. C. sepedonicus has the propensity to exist asymptomatically as latent infectio...

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Pictures

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PictureTitleCaptionCopyright
Clavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.
TitleTuber symptoms
CaptionClavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.
Copyright©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
Clavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.
Tuber symptomsClavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
Clavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.
TitleTuber symptoms
CaptionClavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.
Copyright©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
Clavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.
Tuber symptomsClavibacter sepedonicus (potato ring rot); Potato tuber cut open to display symptoms.©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
Clavibacter sepedonicus (potato ring rot); Potato tuber infected with bacterial ring rot.
TitleTuber symptoms
CaptionClavibacter sepedonicus (potato ring rot); Potato tuber infected with bacterial ring rot.
Copyright©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
Clavibacter sepedonicus (potato ring rot); Potato tuber infected with bacterial ring rot.
Tuber symptomsClavibacter sepedonicus (potato ring rot); Potato tuber infected with bacterial ring rot.©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
Clavibacter sepedonicus (potato ring rot); Potato plant infected with bacterial ring rot showing foliar symptoms.
TitleFoliar symptoms
CaptionClavibacter sepedonicus (potato ring rot); Potato plant infected with bacterial ring rot showing foliar symptoms.
Copyright©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
Clavibacter sepedonicus (potato ring rot); Potato plant infected with bacterial ring rot showing foliar symptoms.
Foliar symptomsClavibacter sepedonicus (potato ring rot); Potato plant infected with bacterial ring rot showing foliar symptoms.©William M. Brown Jr./via Bugwood.org - CC BY 3.0 US
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 sepedonicus (Spieckermann and Kotthoff 1914; Davis et al. 1984) Li et al. 2018

Preferred Common Name

  • potato ring rot

Other Scientific Names

  • Aplanobacter sepedonicus (Spieckermann & Kotthoff) Smith 1920
  • Bacterium sepedonicum Spieckermann & Kotthoff 1914
  • Clavibacter michiganensis subsp. sepedonicus (Spieckermann & Kotthoff) Davis et al. 1984
  • 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

Summary of Invasiveness

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Clavibacter sepedonicus is one of the few major plant pathogens which is not widely distributed in the area where the main host crop (potato) evolved. C. 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 and storages. C. 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 sepedonicus

Notes on Taxonomy and Nomenclature

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Potato ring rot disease was first described in Germany in 1905 (Appel, 1906) and the causal agent was named Bacterium sepedonicum Spieckermann and Kotthoff. The disease was named ‘ring rot’ because it causes a rotting of the vascular ring. The name of the pathogen was changed to Aplanobacter sepedonicus Spieckermann and Kotthoff, which described the non-motile, rod-like bacterium (Smith, 1920). Subsequently, Bergey et al. (1923) transferred the species into the genus Phytomonas and renamed it Phytomonas sepedonica. As the genus Phytomonas encompassed both Gram-negative, motile, green-fluorescent bacteria (now known as Pseudomonas spp.) and Gram-positive, non-motile, yellow/orange-pigmented bacetria (now known as Clavibacter spp.), the proposed reclassification was not accepted by most bacteriologists at that time. Thus, Dowson (1942) transferred the species into the genus Corynebacterium (‘club’ bacterium) (Lehmann and Neumann, 1896) and named it Corynebacterium sepedonicum. Finally, on the basis of the unique 2,4-diaminobutyric acid content in the peptidoglycan layer of cell wall, the pathogen was transferred to the genus Clavibacter and named Clavibacter michiganense subsp. sepedonicum as one of the five subspecies within the species (Davis et al., 1984). In subsequent years, in order to be adopted under the rules of nomenclature for bacterial taxonomy, the name was changed to C. michiganensis subsp. sepedonicus.

Recently, a reclassification of Clavibacter spp. into six new species was proposed based on the genomic information, e.g. average nucleotide identity (ANI) and digital DNA-DNA hybridization (dDDH) indices (Li et al., 2018). The original subspecies of C. michiganensis sensu lato were elevated to species level and the potato ring rot pathogen was designated Clavibacter sepedonicus. Further complete genome sequence-based investigations, i.e. comparative genomics and phylogenetic analyses using all the publicly available genome sequences of the genus, have confirmed the new taxonomic changes and showed that C. sepedonicus is a monophyletic taxon encompassing only potato pathogenic strains of the genus (Osdaghi et al., 2018a; 2020a). Although several comprehensive investigations have been performed to estimate the genetic diversity and population structure of other coryneform plant pathogenic bacteria (Jacques et al., 2012; Osdaghi et al., 2018b; Ansari et al., 2019), little information is available about the genetic diversity of the worldwide population of C. sepedonicus.

Description

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Clavibacter sepedonicus is a short, non-motile, Gram-positive, rod-shaped bacterium (Hayward and Waterston, 1964). The pathogen is aerobic, but slow growth can be observed in anaerobic conditions. Colonies are creamy and yellowish. The optimal growth temperature is 20-23°C (Davis et al., 1984). 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 (Li et al., 2018; Bragard et al., 2019)..

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: 12 May 2022
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
GeorgiaPresent, Few occurrences
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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Potato ring rot was first observed in Germany in 1905 (Appel, 1906) and the causal agent given the name of Bacterium sepedonicum. 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 (Solanum tuberosum) (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). The disease was reported for the first time in the USA in 1938 (Burkholder, 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 (sugar beet)
Distribution: Limited to cool and humid areas of the northern hemisphere
Seedborne Incidence: Not recorded (potato), Yes (sugar beet)
Seed Transmitted: Not recorded
Seed Treatment: None

Overall Risk: High (potato) Low (sugar beet)


Notes on Phytosanitary Risk

C. 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 Present, no further details Harmful (pest or invasive)
Terrestrial ManagedProtected agriculture (e.g. glasshouse production) Present, no further details
Terrestrial ManagedManaged grasslands (grazing systems) Present, no further details
OtherHost Present, no further details

Hosts/Species Affected

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Natural infection causing disease has been found only on potatoes (Solanum tuberosum). Sugar beet (Beta vulgaris var. saccharifera) has been described as a natural symptomless host; C. sepedonicus has been isolated from sugar beet seed and roots (Bugbee and Gudmestad, 1988; Ignatov et al., 2018). An unconfirmed report suggests that the bacterium may be associated with Solanum sarrachoides (hairy nightshade) (Zizz and Harrison, 1991). Natural infection of tomato (Solanum lycopersicum) with C. sepedonicus has also been reported (van Vaerenbergh et al., 2016). In inoculation tests, many members of the Solanaceae, including tomatoes and aubergines (Solanum melongena), were found to be susceptible.

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

Growth Stages

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

Symptoms

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Potato (Solanum tuberosum) 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. First symptoms were observed in field grown potatoes within 55 to 91 days after planting in the USA (Whitworth et al., 2019). 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. Because ring rot symptoms normally only develop late in the growing season, it is often difficult or impossible to detect the disease by visual inspection of the crop in the field (De Boer and Boucher, 2011).
 

The primary tuber symptom is discolouration of the vascular tissue at the stolon end and is most readily observed in tuber cross-sections. Discolouration 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 (Solanum tuberosum) tubers infected or contaminated with C. 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. 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° to -40°C (Nelson, 1984). C. sepedonicus is capable of surviving for up to 7 days in non-sterile surface water at 10°C (van der Wolf et al., 2004).

Epiphytic growth on non-host plant species is one of the survival methods of plant pathogenic bacteria (Harveson et al., 2015; Osdaghi et al., 2018c; Zarei et al., 2018). C. sepedonicus has been detected in a number of field crops grown in rotation with potato (van der Wolf et al., 2005). The bacterium has been reported to be associated with sugar beet (Beta vulgaris var. saccharifera) 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.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.

Infection with C. sepedonicus reduces transpiration and xylem function in potato prior to and during wilting. Transpiration depression and subsequent wilting of infected plants appears to result from reduced xylem function (Bishop and Slack, 1992).

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. 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 (Mansfeld-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. The bacterium grows relatively slowly on artificial surfaces and is easily out competed by other micro-organisms commonly found in environmental samples (Ward et al., 2001). Storage of healthy potato tubers in crates superficially contaminated with C. sepedonicus and then planted in greenhouse produced infected plants (Abdel-Kader et al., 2004).

Seedborne Aspects

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Clavibacter sepedonicus occurs in seed tubers produced from infected potato plants (Gudmestad et al., 2009).

Pathogenic strains of C. sepedonicus were recovered from sugar beet (Beta vulgaris var. saccharifera) seeds produced in the Willamette Valley, Oregon, USA, in 1984. The bacterium was isolated directly from culture plates of diluted sugar beet seed extracts and from aubergines (Solanum melongena) that had been inoculated with sugar beet seed strains of the pathogen. All strains from sugar beet 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. sepedonicus was detected in potato volunteer tuber samples from different locations in the Czech Republic (Pánková et al., 2007). At high inoculum level of C. sepedonicus in potato tubers, 51-93% of stems were infected at 80 days after planting and 10-59% of the tubers were infected at harvest (De Boer et al., 1996).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Breeding and propagation Yes Yes Franc (1999)
Crop production Yes Yes
Food Yes Yes
Garden waste disposal Yes
Live food or feed trade Yes Yes
Research Yes Yes
Seed trade Yes Yes Boer et al. (2005); De Boer (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 Yes
Plants or parts of plantsPotato tuber Yes Yes
Soil, sand and gravelTransfer of tubers. Yes Yes
Debris and waste associated with human activities Yes
Germplasm Yes Yes
Machinery and equipment Yes
Water 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
Flowers/Inflorescences/Cones/Calyx Yes
Growing medium accompanying plants Yes Pest or symptoms usually invisible
Leaves Yes 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 Yes Pest or symptoms usually invisible
Plant parts not known to carry the pest in trade/transport
Bark
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. 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
  • Invasive in its native range
  • Tolerant of shade
  • 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
  • Damages animal/plant products
  • Negatively impacts trade/international relations
Impact mechanisms
  • Pest and disease transmission
  • Pathogenic
  • Rapid growth
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

Uses List

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General

  • Laboratory use
  • Research model

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).

Recently, De Boer et al. (2017) described a detail-oriented procedure for different detection methods of C. sepedonicus. The colony colour and pigmentation on solid media, e.g. NBY agar, is a useful diagnostic characteristic for coryneform plant pathogenic bacteria (Vidaver, 1982; Davis, 1986; Chen et al., 2020; Hamidizade et al., 2020; Osdaghi et al., 2020b). As for Clavibacter species, C. sepedonicus is usually non-pigmented on solid media. However, the wheat pathogen (C. tessellarius) and the maize pathogen (C. nebraskensis) produce orange-pigmented colonies, while the lucerne pathogen (C. insidiosus) and tomato pathogen (C. michiganensis) are yellow (Carlson and Vidaver, 1982). Multi-coloured colony pigmentation has also been reported for other coryneform plant pathogens, e.g. Curtobacterium flaccumfaciens (Osdaghi et al., 2016; 2018d). A semi-selective culture medium, MTNA, that is based on the YGM-medium was developed to detect C. sepedonicus in seed potato tuber lots (Jansing and Rudolph, 1998). C. sepedonicus could be identified specifically using API 50CH and API ZYM and could be distinguished from the remaining species of Clavibacter as well as other bacterial pathogens affecting potatoes (Palomo et al., 2006).

An enzyme-linked immunosorbent assay on nitrocellulose membranes (NCM-ELISA) has been developed which allows for the rapid testing and diagnosis of potato ring rot (Hu et al., 2007). 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. 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).

The accuracy, sensitivity and specificity of the ELISA method in the detection of C. sepedonicus has been compared in five laboratories (De Boer et al., 1992), where the correlation between values for each experimental treatment from the five laboratories was greater (r=0.86) than correlation between values for individual samples (r=0.71).

DNA-based detection methods involving DNA amplification by polymerase chain reaction (PCR) have been developed for detection of the ring rot pathogen (Schneider et al., 1993; Li and De Boer, 1995; Mills et al., 1997). Additional sensitivity can be achieved by the use of nested PCR, Bio-PCR or real time PCR (Schaad et al., 1999).

A nested PCR has been developed for ultrasensitive detection of C. sepedonicus where the nested PCR with primer pair CMSIF1-CMSIR1, followed by primer pair CMSIF2-CMSIR2, specifically detected C. sepedonicus (Lee et al., 1997, 2011). Several attempts have been made to develop a highly sensitive, selective, rapid and easy-to-use method for simultaneous detection and identification of economically important bacterial pathogens of potato (Fessehaie et al., 2003; Mills et al., 2003; Massart et al., 2014; Nikitin et al., 2018). The PCR detection limit on DNA extracted from potato and potato processing water by a commercial kit is 103 c.f.u./ml and 104 c.f.u./ml, respectively, while the PCR assays performed on crude extract of potato processing water showed a sensitivity increase to 102 c.f.u./ml (Lucchese et al., 2012). Recently, Żaczek et al. (2019) have introduced PCR melting profile (PCR MP) and variable number tandem repeat methods which may be useful in investigating the epidemiology of C. sepedonicus.

Vreeburg et al. (2016) validated a real time PCR test that is sensitive and specific for detection of C. sepedonicus in potato tubers and performs at least as well as immunofluorescence. Since 2017, TaqMan real time PCR has been recommended for inclusion in EU Directives and EPPO Standards as a reliable primary (core) screening method for detection of C. sepedonicus (Gudmestad et al., 2009; van Vaerenbergh et al., 2017). As for the most recent updates in the quarantine detection of the ring rot pathogen, a new DNA extraction method and a new multiplex real‐time TaqMan PCR test for detection of C. sepedonicus in asymptomatic potato tubers has been developed (Vreeburg et al., 2018). The latter method was adopted from the procedure described by Gudmestad et al. (2009) for detection of C. sepedonicus. A test performance study conducted through ten official testing laboratories to evaluate the performance of different real‐time PCR tests for the detection of C. sepedonicus indicates that the four real‐time PCR tests (Vreeburg et al., 2018) were fit for purpose as principal screening methods (Vreeburg et al., 2020). An efficient loop-mediated isothermal amplification (LAMP) method for the detection of C. sepedonicus has also been developed (Sagcan and Kara, 2019). Two primers random amplified polymorphic DNA (TP-RAPD) technique can be used as a reliable and fast method to identify C. sepedonicus (Rivas et al., 2002). However, Degefu et al. (2016) have noted that the analytical sensitivity of diagnostic microarray for detection of major bacterial pathogens of potato including C. sepedonicus (Aittamaa et al., 2008) is not sufficient to detect bacteria directly from tubers.

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. Dickeya dadantii (formerly known as Erwinia chrysanthemi [Dickeya chrysanthemi]) has been detected in potato extracts prepared for detection of latent ring rot infections. Interestingly, D. dadantii is capable of multiplying and causing ring rot like symptoms in initial stages of disease development in the test plant, Solanum melongena (Persson and Janse, 1988).

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.

Considering the side effects of the use of chemical compounds in edible crops (Lamichhane et al., 2018), control of ring rot disease 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 Clavibacter sepedonicus (Secor et al., 1988). The peracids, Degaclean and Clarmarin, in combination with the catalase inhibitor KH10 destroyed C. 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.

De Boer and Boucher (2011) have provided an overview on the feasibility of eradicating the bacterial ring rot disease in the potato industry under different circumstances.

Sodium hypochlorite is the most effective disinfectant on a wooden surface and hydrogen peroxide is best on mild steel surfaces for eradication of the biofilms of C. sepedonicus (Howard et al., 2015). Further, the biofilm formation was reduced when exposed to sodium monoiodoacetate, as well as ‘Lazurite’ preparation, while 2,4-D and ‘Ridomil Gold’ stimulated the biofilm formation (Perfileva et al., 2018b). Selenium-containing nanobiocomposites of fungal origin reduce the viability and biofilm formation of C. sepedonicus (Perfileva et al., 2018a, b). Regular sanitation treatments on potato residues from processing industries are not sufficient to inactivate C. sepedonicus. Hence, there is a risk of dissemination of the pathogen via potato waste materials used in agriculture (Steinmöller et al., 2013). Petroleum ether fraction of Laminaria japonica [Saccharina japonica] extracts showed antibacterial activity against C. sepedonicus (Cai et al., 2014). The potential of flusulfamide as a control agent for C. sepedonicus was confirmed by testing the bactericidal activity of this compound in vitro, followed by greenhouse and field trials. Flusulfamide has protective rather than curative properties against C. sepedonicus (Slack and Westra, 1998). Further, jet cleaning in a crate washer for 2 min using the authorized dose of sodium-p-toluenesulfochloramide is an effective method for disinfecting processing materials e.g. wooden potato crates contaminated with C. sepedonicus (Stevens et al., 2017).

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

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. sepedonicus (OEPP/EPPO, 1990b) 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, 1990a) 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. No immune cultivars are available and the use of tolerant cultivars is discouraged because they could serve as symptomless carriers of the pathogen.

References

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Osdaghi, E., Young, A. J., Harveson, R. M., 2020. Bacterial wilt of dry beans caused by Curtobacterium flaccumfaciens pv. flaccumfaciens: a new threat from an old enemy. Molecular Plant Pathology, 21(5), 605-621. doi: 10.1111/mpp.12926

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Pánková, I., Krejzar, V., Čepl, J., Kůdela, V., 2007. Detection of Clavibacter michiganensis subsp. sepedonicus in daughter tubers of volunteer potato plants. Plant Protection Science, 43(4), 127-134. http://www.cazv.cz

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Perfileva, A. I., Pavlova, A. G., Bukhyanova, B. B., Tsivileva, O. M., 2018. Pesticides impact on Clavibacter michiganensis ssp. sepedonicus biofilm formation. Journal of Environmental Science and Health. Part B, Pesticides, Food Contaminants, and Agricultural Wastes, 53(7), 464-468. doi: 10.1080/03601234.2018.1455356

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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

Rivas, R., Velázquez, E., Palomo, J. L., Mateos, P. F., García-Benavides, P., Martínez-Molina, E., 2002. Rapid identification of Clavibacter michiganensis subspecies sepedonicus using two primers random amplified polymorphic DNA (TP-RAPD) fingerprints. European Journal of Plant Pathology, 108(2), 179-184. doi: 10.1023/A:1015044911913

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Sadunishvili, T., Węgierek-Maciejewska, A., Arseniuk, E., Gaganidze, D., Amashukeli, N., Sturua, N., Amiranashvili, L., Kharadze, S., Kvesitadze, G., 2020. Molecular, morphological and pathogenic characterization of Clavibacter michiganensis subsp. sepedonicus strains of different geographic origins in Georgia. European Journal of Plant Pathology, 158(1), 195-209. doi: 10.1007/s10658-020-02066-x

Sagcan, H., Kara, N. T., 2019. Detection of potato ring rot pathogen Clavibacter michiganensis subsp. sepedonicus by loop-mediated isothermal amplification (LAMP) assay. Scientific Reports, 9(1), 20393. doi: 10.1038/s41598-019-56680-9

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Slack, S. A., Westra, A. A. G., 1998. Evaluation of flusulfamide for the control of bacterial ring rot of potato. American Journal of Potato Research, 75(5), 225-230.

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Steinmöller, S., Müller, P., Bandte, M., Büttner, C., 2013. Risk of dissemination of Clavibacter michiganensis ssp. sepedonicus with potato waste. European Journal of Plant Pathology, 137(3), 573-584. doi: 10.1007/s10658-013-0271-y

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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

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

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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, 2022. EPPO Global database. In: EPPO Global database, Paris, France: EPPO. 1 pp. 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

Sadunishvili T, Węgierek-Maciejewska A, Arseniuk E, Gaganidze D, Amashukeli N, Sturua N, Amiranashvili L, Kharadze S, Kvesitadze G, 2020. Molecular, morphological and pathogenic characterization of Clavibacter michiganensis subsp. sepedonicus strains of different geographic origins in Georgia. European Journal of Plant Pathology. 158 (1), 195-209. DOI:10.1007/s10658-020-02066-x

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

Contributors

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20/11/20 Updated by:

Ebrahim Osdaghi, Department of Plant Protection, University of Tehran, Iran

21/12/07 Updated by:

Solke de Boer, Centre for Animal & Plant Health, Charlottetown, Prince Edward Island, Canada

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