Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Burkholderia caryophylli
(bacterial wilt of carnation)

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Datasheet

Burkholderia caryophylli (bacterial wilt of carnation)

Summary

  • Last modified
  • 29 March 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Burkholderia caryophylli
  • Preferred Common Name
  • bacterial wilt of carnation
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Proteobacteria
  •     Class: Betaproteobacteria
  •       Order: Burkholderiales
  •         Family: Burkholderiaceae
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    Compendia
    CAB International
    Wallingford
    Oxfordshire
    OX10 8DE
    UK
    compend@cabi.org
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Identity

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Preferred Scientific Name

  • Burkholderia caryophylli (Burkholder) Yabuuchi et al.

Preferred Common Name

  • bacterial wilt of carnation

Other Scientific Names

  • Phytomonas caryophylli Burkholder
  • Pseudomonas caryophylli (Burkholder) Starr & Burkholder

International Common Names

  • English: bacterial stem crack of carnation; carnation: bacterial stem crack; carnation: bacterial wilt
  • Spanish: chancro bacteriano del clavel
  • French: chancre bacterien de l'oeillet

Local Common Names

  • Germany: Bakterien-: Nelke Stengelriss; Welkekrankheit: Nelke; Wurzelfäule der Nelken

EPPO code

  • PSDMCA (Burkholderia caryophylli)

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Proteobacteria
  •         Class: Betaproteobacteria
  •             Order: Burkholderiales
  •                 Family: Burkholderiaceae
  •                     Genus: Burkholderia
  •                         Species: Burkholderia caryophylli

Notes on Taxonomy and Nomenclature

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The combination Burkholderia caryophylli was proposed without examination of the type strain of Pseudomonas caryophylli and therefore was not valid when first published. This defect can be taken to have been corrected in subsequent studies (Urakami et al., 1994; Gillis et al., 1995).

Willems and Vandamme (2003) published a taxonomic overview of the phytopathogenic ex-Pseudomonas species of rRNA groups II and III.

Description

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B. caryophylli is a straight or slightly curved rod with rounded ends, occurring singly or in pairs; it is aerobic, non-sporing, motile with one or several polar flagella, Gram-negative, sudanophilic, 0.35-0.95 x 1.05-3.18 µm.

In PDA culture, colonies are round, smooth and shining with regular margins: while cream-coloured at first, colonies darken with age. On nutrient agar, growth is slow and cells die rapidly; subculturing is not possible after about a week.

 

Distribution

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A record of B. caryophylli in Colombia (CABI/EPPO, 2006) published in previous editions of the Compendium was erroneous and has been removed. B. caryophylli is a quarantine pest in Colombia (Instituto Colombiano Agropecuario, 2013).

See also CABI/EPPO (1998, No. 251).

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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ChinaRestricted distributionEPPO, 2014
-JilinPresentEPPO, 2014
IndiaPresentEPPO, 2014
IsraelAbsent, formerly presentEPPO, 2014
JapanPresentEPPO, 2014
-ShikokuPresentEPPO, 2014
TaiwanPresent, few occurrencesCABI/EPPO, 2006; EPPO, 2014

North America

CanadaEradicatedCABI/EPPO, 2006; EPPO, 2014
USARestricted distributionEPPO, 2014
-FloridaPresentEPPO, 2014
-IllinoisPresentBradbury, 1986; EPPO, 2014
-IndianaPresentBradbury, 1986; EPPO, 2014
-IowaPresentBradbury, 1986; EPPO, 2014
-MassachusettsPresentBradbury, 1986; EPPO, 2014
-MinnesotaPresentEPPO, 2014
-MissouriPresentBradbury, 1986; EPPO, 2014
-MontanaPresentCABI/EPPO, 2006; EPPO, 2014
-New YorkPresentBradbury, 1986; EPPO, 2014
-PennsylvaniaPresentBradbury, 1986; EPPO, 2014
-WashingtonPresentBradbury, 1986; EPPO, 2014

South America

ArgentinaPresentBradbury, 1986; EPPO, 2014
BrazilRestricted distributionEPPO, 2014
-Sao PauloPresentEPPO, 2014
ColombiaAbsent, invalid recordEPPO, 2014
UruguayPresent, few occurrencesEPPO, 2014

Europe

AustriaAbsent, formerly presentEPPO, 2014
BelgiumAbsent, no pest recordEPPO, 2014
BulgariaAbsent, intercepted onlyEPPO, 2014
DenmarkAbsent, formerly presentBradbury, 1986; EPPO, 2014
FranceAbsent, formerly presentBradbury, 1986; EPPO, 2014
GermanyAbsent, formerly present194*Bradbury, 1986; EPPO, 2014
HungaryAbsent, formerly presentBradbury, 1986; EPPO, 2014
IrelandAbsent, formerly presentEPPO, 2014
ItalyRestricted distributionBradbury, 1986; EPPO, 2014
NetherlandsAbsent, confirmed by surveyNPPO of the Netherlands, 2013; Bradbury, 1986; EPPO, 2014
NorwayAbsent, unreliable recordBradbury, 1986; EPPO, 2014
PolandAbsent, formerly presentBradbury, 1986; EPPO, 2014
SerbiaRestricted distributionEPPO, 2014
SlovakiaAbsent, unreliable recordEPPO, 2014
SwedenAbsent, formerly presentBradbury, 1986; EPPO, 2014
SwitzerlandAbsent, formerly presentEPPO, 2014
UKAbsent, formerly presentEPPO, 2014
-England and WalesAbsent, formerly presentEPPO, 2014
Yugoslavia (former)PresentCABI/EPPO, 2006
Yugoslavia (Serbia and Montenegro)Restricted distributionBradbury, 1986

Risk of Introduction

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B. caryophylli is an EPPO A2 quarantine pest (OEPP/EPPO, 1978), in view of the limited number of EPPO countries in which it has been reported, and the fact that it is readily carried on cuttings in international trade. However, the lack of recent publications on this organism and the disease it causes indicate that its importance is now very minor. It is also of quarantine significance for JUNAC.
 

Hosts/Species Affected

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Carnations are the main host. However, Dianthus barbatus and D. allwoodii can be infected through artificial inoculation. In Florida, USA, and Japan, Limonium sinuatum is also reported to be infected (Jones and Engelhard, 1984; Nishiyama et al., 1988).

Growth Stages

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Symptoms

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Symptoms may take 2-3 years to manifest themselves, particularly when cuttings are mildly infected and maintained at relatively low temperatures. Foliage becomes greyish-green, later yellowing and wilting and then death may occur.

In stems, at soil temperatures below about 17°C, a rapid multiplication of cells leads to tension around the vessels and longitudinal, internodal stem cracks appear, usually at the base of the plant, and later develop into deep cankers. Initially, this cracking is very similar to the physiological cracking observed in certain cultivars. However, in pathogen-induced cracks, a brownish-yellow bacterial slime is visible, often overgrown with saprophytic fungi such as Mycosphaerella tassiana. In some cases, the extrusions from the cankers leave the stems hollow. At 20-25°C, cankers are more rare and wilting is the common symptom. Visual observation of peeled stems reveals sticky, brownish-yellow, narrow or broad, longitudinal stripes in the vascular tissue; in cross section, these appear as irregular brownish spots with a water-soaked margin.

Roots of infected plants, once wilting occurs, are more or less rotten, the plants being easily pulled out of the soil and, on cutting, roots show discontinuous brown spots which distinguish the disease from that caused by Phialophora cinerescens which leaves the roots apparently symptomless (EPPO/CABI, 1996a).

Plants may survive about 1-2 months, but secondary invasion by fungi, such as Fusarium spp., accelerates death. Heavily infected cuttings wilt and die before roots are formed. For more information, see Dimock (1950), Hellmers (1958), Lemattre et al. (1964), Garibaldi (1967), Lemattre (1969) and Saddler (1994).

List of Symptoms/Signs

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SignLife StagesType
Leaves / abnormal colours
Roots / soft rot of cortex
Stems / gummosis or resinosis

Biology and Ecology

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The bacterium can only enter plants through wounds, and subsequently colonizes the vascular system of the stem and roots. The primary infection source is infected cuttings taken from mother plants with a latent infection. Bacteria can pass from one cutting to another in the water of the propagating bed or, if the cuttings are held in water, before planting out. The observed slow, scattered spread of the disease indicates that spread occurs only from one root system to another. Bacterial slime is exposed when stems crack and this inoculum may be transferred from one plant to another. Temperatures over 20°C accelerate bacterial growth and therefore symptom expression, while at low temperatures infected plants may show no symptoms. For more information, see Dowson (1929), Burkholder (1942), Dimock (1950), Hellmers (1958), Garibaldi (1967).

 

Means of Movement and Dispersal

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The natural spread of the pathogen is very slow and over extremely short distances. The main path of distribution is by means of infected cuttings which may be obtained from infected but symptomless mother plants.
 

Plant Trade

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

Impact

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B. caryophylli has caused serious damage in the USA since its first report in 1940. Only minor losses occur in Europe and the Mediterranean region at present (EPPO/CABI, 1996c).

Detection and Inspection

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To make a reliable diagnosis, many old and young stems should be examined and isolations made from diseased tissue. Microscopic observation of stem sections shows neoformations around infected vessels, plugging of vessels, hyperlignification of their walls and necrosis. Since latent infections on cuttings cannot be readily detected, cuttings should be kept at a relatively high temperature to ensure maximum symptom expression. The bacterium can be reliably detected by immunofluorescence staining (IFAS) and direct isolation even in material with latent infection (Muratore et al., 1986). B. caryophylli has also been detected from inoculated carnation by PCR and LAMP (Loop-mediated isothermal amplification) (Kazushi et al., 2005).

Similarities to Other Species/Conditions

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To make a reliable diagnosis, many old and young stems should be examined and isolations made from diseased tissue. Microscopic observation of stem sections shows neoformations around infected vessels, plugging of vessels, hyperlignification of their walls and necrosis. Since latent infections on cuttings cannot be readily detected by direct observation, cuttings should be kept at a relatively high temperature to ensure maximum symptom expression.

Both B. caryophylli and Dickeya chrysanthemi, the slow wilt-pathogen, can be latently transmitted in cuttings taken from infected mother plants. Differences in symptom expression are evident (Bazzi et al., 1987), however in both cases early detection is desirable (Minardi et al., 1988). Both bacteria can be detected by immunofluorescence staining (IFAS) and direct isolation even in material with latent infection (Muratore et al., 1986). For more information, see EPPO/CABI (1996b, c).

The carnation strain of D. chrysanthemi (EPPO/CABI, 1996b), which causes a similar disease, is readily distinguishable in nutrient agar culture by its rapid growth of greyish-white, lobate colonies. In addition, internal symptoms of the two diseases are different.

In addition, Burkholderia andropogonis, also a pathogen of carnation, though generally considered to be foliar rather than systemic, can be detected using serological methods. Whilst this method is effective the specific monoclonal antibody developed was shown to possess cross-reactivity with B. caryophylli (Li et al., 1993).

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.

There are no direct control measures against B. caryophylli. Disease-free mother plants should be used and rooting beds and soil should be fumigated. In countries where the disease occurs, cuttings should be taken from separately grown mother plants derived from biologically tested, healthy cuttings. EPPO accordingly recommends that consignments should come from a place of production found free from B. caryophylli during the last growing season (OEPP/EPPO, 1990). However, the introduction of an EPPO-recommended certification scheme for carnation (OEPP/EPPO, 1991) provides a satisfactory alternative to such plant quarantine requirements.

Breeding of resistant cultivars is another strategy to control the disease (Onozaki et al., 1998, 1999). RAPD markers associated with genes controlling wilt resistance have been identified (Onozaki et al., 2003, 2004). 

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).

1991. Certification scheme. Pathogen-tested material of carnation. Bulletin OEPP, 21(2):279-290

Bazzi C; Minardi P; Mazzucchi U, 1987. Bacterial diseases of flower and ornamental plants in Italy. Informatore Fitopatologico, 37(6):15-24

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

Burkholder WH, 1942. Three bacterial plant pathogens. Phytomonas caryophylli sp. n., Phytomonas alliicola sp. n. and Phytomonas manihotis (Artaud, Berthet and Bondar) Viegas. Phytopathology, 32:141-149.

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. Burkholderia caryophylli. Distribution Maps of Plant Diseases, No. 411. Wallingford, UK: CAB International.

Dimock AW, 1950. Major carnation diseases and their spread. Florists Exchange Horticulture, Trade World, 114:21-72.

Dowson WS, 1929. On the stem rot or wilt disease of carnation. Annals of Applied Biology, 16:261-280.

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

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

Furuya N; Masunaga T; Khan AA; Iiyama K; Matsumoto M; Matsuyama N, 2000. Bacterial wilt of Russell prairie gentian caused by Burkholderia caryophylli. Journal of General Plant Pathology, 66(4):316-322.

Gao J; Yuan ML, 1991. Studies on bacterial stalk rot in sunflower. I. Symptoms and identification of causal pathogens. Acta Phytopathologica Sinica, 21(3):173-179

Garibaldi A, 1967. A new bacterial disease of carnation in Italy. Informatore Fitopatologico, 17:9-11.

Gillis M; Van VanT; Bardin R; Goor M; Hebbar P; Willems A; Segers P; Kersters K; Heulin T; Fernandez MP, 1995. Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov. for N-fixing isolates from rice in Vietnam. International Journal of Systematic Bacteriology, 45:274-289.

Hellmers E, 1958. Four wilt diseases of perpetual flowering carnation in Denmark. Dansk Botanisk Arkiv, 18:1-200.

IMI, 1995. Distribution Maps of Plant Diseases, No. 511. Wallingford, UK: CAB International.

Jones JB; Engelhard AW, 1984. Crown and leaf rot of statice incited by a bacterium resembling Pseudomonas caryophylli. Plant Disease, 68(4):338-340

Kazushi O; Tetsuhisa K; Toshio O, 2005. Detection of Burkhoderia caryophylli from inoculated carnation by PCR and LAMP (Loop-mediated isothermal amplification). Annual Report of the Kansai Plant Protection Society, No.47:75-77.

Lemattre M, 1969. Maladies bactériennes des cultures florales. In: Les maladies des plantes. Journées frantaises d'études et d'information, Paris, février 1969. Paris, France: ACTA-FNGPC, 461, 485.

Lemattre M; Mercier S; Tramier R, 1964. Une maladie bactérienne de l'oeillet nouvelle pour la France. Comptes Rendus Hebdomadaires des Séances de l'Académie d'Agriculture de France. Année, 1008-1014.

Li X; Dorsch M; Dot T del; Sly LI; Stackebrandt E; Hayward AC, 1993. Phylogenetic studies of the rRNA group II pseudomonads based on 16S rRNA gene sequences. Journal of Applied Bacteriology, 74(3):324-329

Li X; Wong WC; Hayward AC, 1993. Production and use of monoclonal antibodies to Pseudomonas andropogonis. Journal of Phytopathology, 138(1):21-30

Liu HL, 1990. Bacterial wilt of Gypsophila paniculata caused by Pseudomonas caryophylli. Bulletin of Taichung District Agricultural Improvement Station, No. 28:33-42

Minardi P; Mazzucchi U; Beruto M; Lercari B; Mainolfi P, 1988. A survey of bacterial slow wilt and canker in carnation in Italian nurseries. Bulletin OEPP, 18(3):365-368; 9 ref.

Muratore MG; Mazzucchi U; Gasperini C; Fiori M, 1986. Detection of latent infection of Erwinia chrysanthemi and Pseudomonas caryophylli in carnation. EPPO Bulletin, 16(1):1-12

Nishiyama J; Kobayashi T; Azegami K, 1988. Bacterial wilt of statice caused by Pseudomonas caryophylli. Annals of the Phytopathological Society of Japan, 54(4):444-452

Onozaki T; Ikeda H; Tanikawa N; Shibata M; Kudo K; Funayama T, 2003. .

Onozaki T; Ikeda H; Yamaguchi T; Himeno M, 1998. .

Onozaki T; Ikeda H; Yamaguchi T; Himeno M; Amano M; Shibata M, 2002. 'Carnation Nou No.1', a carnation breeding line resistant to bacterial wilt (Burkholderia caryophylli). Horticultural Research (Japan), 1(1):13-16.

Onozaki T; Tanikawa N; Taneya M; Kudo K; Funayama T; Ikeda H; Shibata M, 2004. A RAPD-derived STS marker is linked to a bacterial wilt (Burkholderia caryophylli) resistance gene in carnation. Euphytica, 138(3):255-262.

Onozaki T; Yamaguchi T; Himeno M; Ikeda H, 1999. Evaluation of 277 carnation cultivars for resistance to bacterial wilt (Pseudomonas caryophylli). Journal of the Japanese Society for Horticultural Science, 68(3):546-550.

Onozaki T; Yamaguchi T; Himeno M; Ikeda H, 1999. Evaluation of wild Dianthus accessions for resistance to bacterial wilt (Pseudomonas caryophylli). Journal of the Japanese Society for Horticultural Science, 68(5):974-978.

Saddler GS, 1994. Burkholderia caryophylli. IMI Descriptions of Pathogenic Fungi and Bacteria, No. 1215. Wallingford, UK: CAB International.

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.

Urakami T; Ito-Yoshida C; Araki H; Kijima T; Suzuki KI; Komagata K, 1994. Transfer of Pseudomonas plantarii and Pseudomonas glumae to Burkholderia as Burkholderia spp. and description of Burkholderia vandii sp. nov. International Journal of Systematic Bacteriology, 44(2):235-245

Willems A; Vandamme P, 2003. .

Yabuuchi E; Kosako Y; Oyaizu H; Yano I; Hotta H; Hashimoto Y; Ezaki T; Arakawa M, 1992. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiology and Immunology, 36(12):1251-1275; 30 ref.

Yagi M; Kimura T; Yamamoto T; Isobe S; Tabata S; Onozaki T, 2012. QTL analysis for resistance to bacterial wilt (Burkholderia caryophylli) in carnation (Dianthus caryophyllus) using an SSR-based genetic linkage map. Molecular Breeding, 30(1):495-509. http://www.springerlink.com/link.asp?id=100317

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