Preferred name: Clavibacter michiganensis
Authority: (Smith) Davis et al.
Taxonomic position: Bacteria: Actinobacteria: Micrococcales: Microbacteriaceae
Other scientific names: Bacterium michiganense Smith, Clavibacter michiganensis subsp. michiganensis (Smith) Davis et al., Corynebacterium michiganense pv. michiganense (Smith) Dye & Kemp, Corynebacterium michiganense pv. michiganense (Smith) Jensen, Corynebacterium michiganense subsp. michiganense (Smith) Jensen, Corynebacterium michiganense (Smith) Jensen
Common names in English: bacterial canker of tomato, bird's eye of tomato fruits, vascular wilt of tomato
view more common names online...
Notes on taxonomy and nomenclature EPPO Categorization: A2 list
EU Categorization: RNQP (Annex IV)
view more categorizations online...
EPPO Code: CORBMI

The only major host of economic importance is tomato (Solanum lycopersicum). Several strains which had been isolated from Capsicum annuum and Capsicum frutescens have been reclassified as Clavibacter capsici (Oh et al., 2016). Additionally, several weeds from the Solanaceae family have been shown to be susceptible to C. michiganensis under natural or experimental conditions (e.g. Solanum douglasii, Solanum nigrum and Solanum triflorum; Laj, 1976; Latin et al., 1995; Lewis Ivey & Miller, 2000; Nandi et al., 2018; Yim et al., 2012), and could be potential reservoirs of the pathogen. A number of solanaceous plants are susceptible after artificial inoculation (for details see Thyr et al., 1975; Yim et al., 2012), as well as other plant species including cucumber (Cucumis sativus), sunflower (Helianthus spp.) and watermelon (Citrullus lanatus). Additional monocotyledonous host plants reported susceptible after artificial inoculation, e.g. barley (Hordeum vulgare), maize (Zea mays), oat (Avena sativa) and wheat (Triticum spp.; Stamova & Sotirova, 1987) are considered doubtful pending confirmation.

Host list: Solanum douglasii, Solanum lycopersicum, Solanum nigrum, Solanum pectinatum, Solanum quitoense, Solanum triflorum, Solanum tuberosum

The bacterial canker of tomato was first identified in tomato greenhouses in Michigan (USA) in 1909, and is now widespread in Africa, Asia, Europe, North America, Oceania and South America. Since the mid-twentieth century, the intensification of the international tomato seed trade has caused C. michiganensis to spread within and between continents. It has also become widespread within a number of tomato producing countries of the EPPO region, but also in tomato producing countries outside the EPPO region.

EPPO Region: Armenia, Azerbaijan, Belarus, Belgium, Bulgaria, Cyprus, Czech Republic, France (mainland), Germany, Greece (mainland, Kriti), Hungary, Israel, Italy (mainland, Sardegna, Sicilia), Jordan, Latvia, Morocco, Poland, Portugal (mainland), Romania, Russia (Central Russia, Southern Russia, Western Siberia), Serbia, Slovenia, Spain (mainland, Islas Canárias), Switzerland, Tunisia, Türkiye, Ukraine
Africa: Egypt, Kenya, Madagascar, Morocco, South Africa, Tanzania, Togo, Tunisia, Uganda, Zambia, Zimbabwe
Asia: China (Liaoning, Xinjiang), India (Andhra Pradesh, Karnataka, Madhya Pradesh, Maharashtra, Tamil Nadu), Indonesia (Java), Iran, Israel, Japan (Honshu), Jordan, Korea, Republic, Lebanon, Syria
North America: Canada (Alberta, British Columbia, Manitoba, Nova Scotia, Ontario, Québec, Saskatchewan), Mexico, United States of America (Alabama, Arkansas, California, Colorado, Connecticut, Florida, Georgia, Hawaii, Illinois, Indiana, Iowa, Kentucky, Maine, Maryland, Massachusetts, Michigan, Minnesota, Montana, Nebraska, New Hampshire, New Jersey, New York, North Carolina, North Dakota, Ohio, Oklahoma, Oregon, Pennsylvania, South Dakota, Utah, Vermont, Wyoming)
Central America and Caribbean: Belize, Costa Rica, Cuba, Dominica, Dominican Republic, Grenada, Guadeloupe, Panama
South America: Argentina, Brazil (Pernambuco, Sao Paulo), Chile, Colombia, Ecuador, Peru, Uruguay
Oceania: Australia (New South Wales, Queensland, South Australia, Tasmania, Victoria, Western Australia), Fiji, Guam, New Caledonia, New Zealand, Tonga

Contaminated/infected tomato seeds and plants for planting are the primary source for C. michiganensis outbreaks. Contamination/infection levels as low as 1 in 10000 seeds can be enough to cause an epidemic. Plant debris containing the pathogen and alternative hosts can also play a role in disease outbreaks but are considered less important (De León et al., 2011; EPPO, 2016a; Fatmi et al., 1991; Moffett & Wood, 1984; Nandi et al., 2018).

From the primary source the bacterium spreads locally mainly by water (rain splash, irrigation) and/or during cultural practices (e.g. trimming, chemical sprays). The bacterium can enter the plant tissue through hydathodes as well as different types of wounds on shoots and roots (Carlton et al., 1998; Huang & Tu, 2001). Young plants have been shown to be more susceptible to C. michiganensis (Van Vaerenbergh & Chauveau, 1985). However, under natural conditions, tomato plants are susceptible throughout their life (Nandi et al., 2018). After infection, there is a latent period which can range from 7 days up to almost 3 months (EFSA, 2014; Gleason et al., 1993). C. michiganensis can cause systemic infections, generally when the infection occurs at an early stage of plant development, or only a local infection, when the plant is infected later during its development (Sharabani et al., 2013).

The bacterium colonizes and multiplies in the xylem vessels which allows it to spread rapidly through the plant. Inside the xylem C. michiganensis expresses a large set of virulence factors and enzymes leading, for example, to the degradation of the vascular tissue. Heavily infected vessels contain viscous granular deposits, tyloses and bacterial masses that block water transport which causes wilting of the plant. From the xylem, C. michiganensis can also enter the seed coat and endosperm leading to (new) seed infections (Nandi et al., 2018). During later stages of infection, the stem can crack, leading to the exudation of droplets containing C. michiganensis, and allowing further spreading.

The optimum temperature for growth of C. michiganensis populations is 24-28°C. The bacterium is highly tolerant to desiccation and can survive on seeds and dried plant material for years. In dried soil, the survival time is shorter, but can last up to 7 or 8 months (EFSA, 2014).

Symptoms

The EPPO Diagnostic Standard PM 7/42 for C. michiganensis gives a detailed description of the disease symptoms (EPPO, 2016a). Symptoms can be divided in those that are triggered during a systemic infection and those that can appear during a local infection.

In systemic infections early symptoms include the appearance of dull green, oily areas that desiccate and later turn brown. With temperatures of 25-30°C and strong evapotranspiration a reversible wilting of leaves occurs which, within a few days, will become irreversible. Entire leaves, and eventually the whole plant, will wilt and desiccate. Contaminated/infected seeds usually give rise to apparently healthy seedlings, symptoms only appearing as plants approach maturity. Fruits may fail to develop and fall, or ripen unevenly. They also often show external marbling and internal bleaching of vascular and surrounding tissue. Less frequently, fruits may show characteristic ‘bird's eye’ spots. Initially slightly raised and white, these spots develop light-brown roughened centres surrounded by a flat whitish halo. On cutting stems, petioles and peduncles, particularly at their junctions, a creamy-white, yellow or reddish-brown discoloration of vascular tissue and pith and cavities within the pith will be evident. These discolorations are only visible at advanced stages of the disease (EPPO, 2016a).

Local infections can cause a granular appearance of leaves, stems and calyces which is caused by the presence of raised or sunken white to pale orange blisters. Infections through hydathodes commonly lead to dark brown spots that are surrounded by a yellow to orange area at the edge of the leaf. At later stages the edges of these leaves can curl and wilt. Local infections can sometimes cause yellow streaks along the stem that might split open and form cankers (EPPO, 2016a).

Morphology

C. michiganensis is an aerobic, non-motile, Gram-positive and non-spore forming bacteria, with a curved rod shape (for details see Bradbury, 1986).

Isolation of the causal organism can be performed on e.g. yeast peptone glucose agar. On this medium the bacterium develops flat and semi-fluidal, round or irregular, yellow colonies in 3 to 4 days (EPPO, 2016a). White, pink, red and orange mutants may also occur (Hayward & Waterston, 1964).

Detection and inspection methods

Visual inspection will generally allow detection of symptoms during the growing season. However, plantlets are usually symptomless when they are traded, and symptoms are not visible on seeds. Plants for planting should be inspected according to EPPO Standard PM 3/77 Vegetable plants for planting under protected conditions – inspection of places of production (EPPO, 2016b), whereas sampling of seeds for testing should follow EPPO PM 3/80 Consignment inspection of seed of Solanum lycopersicum (EPPO, 2021).

The EPPO Diagnostic Standard PM 7/42 for C. michiganensis provides thorough instructions on sampling, extracting, plating and diagnosing both symptomatic and symptomless plants. These include plating on both semi-selective and non-selective media and detection by immunofluorescence (IF) as well as PCR. Additionally, two procedures for detection of C. michiganensis in seeds are provided. The first procedure is based on plating seed extracts on different semi-selective media while the second procedure provides details on IF, PCR and selective enrichment protocols (EPPO, 2016a).

In addition, in recent years, a number of often TaqMan based qPCR protocols and a loop-mediated isothermal amplification assay were developed that can be used to confirm the identity of isolated bacteria suspected of being C. michiganensis and/or to specifically detect the bacterium in infected seeds and plant material (Dobhal et al., 2019; Han et al., 2018; Larrea-Sarmiento et al., 2019; Ramachandran et al., 2021; Thapa et al., 2020).

Seed is the main long-distance pathway for movement of the pathogen. Cultivation measures contribute to local dispersion of the disease. Overhead irrigation, chemical sprays, handling during transport and wound inflicting actions such as clipping and pruning all favour the spread of C. michiganensis. The use of rotary mowers for clipping tomato plants has especially favoured disease dissemination (Carlton et al., 1998; Huang & Tu, 2001; Sharabani et al., 2013). Additionally, remaining contaminated crop debris can allow re-infection of the seedlings in the following season (EFSA, 2014).

Economic impact

Tomato is the world’s most important vegetable crop with an annual production of over 180 million tonnes, representing a value of 93 billion USD (Food and agricultural organization, 2020). Since the first report of the disease in the USA in 1910, C. michiganensis has spread throughout the world and causes serious losses to both glasshouse and field tomato crops, either by killing the young plants or disfiguring the fruits making them unmarketable as fresh produce. Disease incidence in affected fields can be as high as 100% leading to severe yield losses. However, a high reduction in crop damage has been observed following the considerable efforts into preventing the introduction and dissemination of the pathogen, which involves the integral testing of seeds and plantlets (see Control). Compared to the damage in tomato, economic losses in pepper are limited (Baysal et al., 2011; EFSA, 2014; Lamichhane et al., 2011; Nandi et al., 2018).

Control 

Use of healthy seeds is the first and most important condition for controlling the disease. Seed lots should be laboratory tested for the presence of C. michiganensis and tomato seeds are often acid extracted to disinfect the seed surface (EPPO, 2021). A substantial reduction of infection can be achieved by chemical treatment of the seed (Dhanvantari, 1989). Once the disease has appeared in a crop, strict hygiene measures such as eradication of infected plants and isolation of infected rows can minimize yield loss. Prophylactic measures (destruction of crop residues, disinfection of structures and equipment) are essential to prevent infection in protected crops. At the moment there are no commercial tomato varieties which are fully resistant to C. michiganensis (Nandi et al., 2018). 

To prevent tomato seed and plant lots from being infected by C. michiganensis the ‘Good Seed and Plant Practices’ (GSPP) system was developed about a decade ago. GSPP provides standards for (hygiene) practices and participating companies are audited to ensure proper implementation (https://www.gspp.eu/).

Phytosanitary risk 

Tomato is widely grown in glasshouses in the EPPO region, and the bacterium causes one of the most serious bacterial diseases of glasshouse tomatoes. For tomato field crops, the climatic conditions in southern Europe are favourable for disease development (EFSA, 2014). Disease outbreaks caused by C. michiganensis are sporadic but the impact of these outbreaks can be high. Since the pathogen is seed borne and contaminated/infected seed usually gives rise to apparently healthy seedlings, this facilitates introduction, establishment and spread. This combined with the fact that there are no curative treatments and no fully resistant commercial varieties available, make C. michiganensis a major threat for tomato cultivation (EFSA, 2014).

Since seeds are the main pathway for entry, appropriate measures could consist of treating the seeds (i.e. by means of an appropriate acid extraction method or an equivalent method) and testing seed lots according to EPPO Standards PM 7/42 (EPPO, 2021; EPPO, 2016a). Alternatively, seeds could be produced in a pest free area or in a pest free production site.

When not regulated as a quarantine pest, the EU Quality pest project recommended C. michiganensis for regulation as a RNQP, for propagation material (including seeds) of tomato (Picard et al., 2018). An alternative measure was recommended, involving the absence of symptoms of disease caused by C. michiganensis observed in inspections, at appropriate times, during the complete cycle of vegetation of the plants at the site of production. 

Additionally, good hygiene practices are important to prevent large disease outbreaks. The guidelines provided by GSPP describe measures that will help to limit the risks for C. michiganensis infections. These guidelines focus on managing risk factors, continuous monitoring and seed testing (https://www.gspp.eu/; EFSA, 2014).

Arizala D, Dobhal S, Alvarez AM & Arif M (2022) Elevation of Clavibacter michiganensis subsp. californiensis to species level as Clavibacter californiensis sp. nov., merging and re-classification of Clavibacter michiganensis subsp. chilensis and Clavibacter michiganensis subsp. phaseoli as Clavibacter phaseoli sp. nov. based on complete genome in silico analyses. International Journal of Systematic and Evolutionary Microbiology 72(9). https://doi.org/10.1099/ijsem.0.005427

Baysal Ö, Mercati F, İkten H, Yıldız RÇ, Carimi F, Aysan Y & Teixeira Da Silva JA (2011) Clavibacter michiganensis subsp. michiganensis: Tracking strains using their genetic differentiations by ISSR markers in Southern Turkey. Physiological and Molecular Plant Pathology 75, 113-119.

Bradbury JF (1986) Guide to plant pathogenic bacteria. CAB International, Wallingford (GB).

Carlton WM, Braun EJ & Gleason ML (1998) Ingress of Clavibacter michiganensis subsp. michiganensis into tomato leaves through hydathodes. Phytopathology 88, 525-529.

De León L, Siverio F, López MM & Rodríguez A (2011) Clavibacter michiganensis subsp. michiganensis, a seedborne tomato pathogen: healthy seeds are still the goal. Plant Disease 95, 1328-1338.

Dhanvantari BN (1989) Effect of seed extraction methods and seed treatments on control of tomato bacterial canker. Canadian Journal of Plant Pathology 11, 400-408.

Dobhal S, Larrea‐Sarmiento A, Alvarez AM & Arif M (2019) Development of a loop-mediated isothermal amplification assay for specific detection of all known subspecies of Clavibacter michiganensis. Journal of Applied Microbiology 126, 388-401.

EFSA (2014) Scientific Opinion on the pest categorisation of Clavibacter michiganensis subsp. michiganensis (Smith) Davis et al. EFSA Journal 12, 3721.

EPPO (2016a) EPPO Standards PM 7/42 (3) Clavibacter michiganensis subsp. michiganensis. EPPO Bulletin 46, 202-225.

EPPO (2016b) Phytosanitary procedures. EPPO Standard PM 3/77 Vegetable plants for planting under protected conditions – inspection of places of production. EPPO Bulletin 46, 40-48.

EPPO (2021) EPPO standards PM 3/80 (2) Consignment inspection of seed of Solanum lycopersicum and its hybrids. EPPO Bulletin 46, 68-72.

Fatmi M, Schaad NW & Bolkan HA (1991) Seed treatments for eradicating Clavibacter michiganensis subsp. michiganensis from naturally infected tomato seeds. Plant Disease 75, 383-385.

Gleason ML, Gitaitis RD & Ricker MD (1993) Recent progress in understanding and controlling bacterial canker of tomato in eastern North America. Plant Disease 77, 1069-1076.

Han S, Jiang N, Lv Q, Kan Y, Hao J, Li J & Luo L (2018) Detection of Clavibacter michiganensis subsp. michiganensis in viable but nonculturable state from tomato seed using improved qPCR. Plos One 13, e0196525.

Hayward AC & Waterston JM (1964) Corynebacterium michiganense. IMI Descriptions of Fungi and Bacteria. 2, 19, CAB International, Wallingford (UK).

Huang R & Tu JC (2001) Effects of nutrient solution pH on the survival and transmission of Clavibacter michiganensis ssp. michiganensis in hydroponically grown tomatoes. Plant Pathology 50, 503-508.

Laj M (1976) Bacterial canker of bell pepper caused by Corynebacterium michiganense. Plant Disease Reporter 60, 339-342.

Lamichhane JR, Balestra GM & Varvaro L (2011) Severe outbreak of bacterial canker caused by Clavibacter michiganensis subsp. michiganensis on tomato in central Italy. Plant Disease 95, 221-221.

Larrea-Sarmiento A, Alvarez AM, Stack JP & Arif M (2019) Synergetic effect of non-complementary 5’ AT-rich sequences on the development of a multiplex TaqMan real-time PCR for specific and robust detection of Clavibacter michiganensis and C. michiganensis subsp. nebraskensis. Plos One 14, e0218530.

Latin R, Tikhonova I & Rane K (1995) First report of bacterial canker of pepper in Indiana. Plant Disease 79, 860.

Lewis Ivey ML & Miller SA (2000) First report of bacterial canker of pepper in Ohio. Plant Disease 84, 810-810.

Li X, Tambong J, Yuan K, Chen W, Xu H, Lévesque CA & De Boer SH (2018) Re-classification of Clavibacter michiganensis subspecies on the basis of whole-genome and multi-locus sequence analyses. International Journal of Systematic and Evolutionary Microbiology 68, 234-240.

Moffett ML & Wood BA (1984) Survival of Corynebacterium michiganense subsp. michiganense within host debris in soil. Australasian Plant Pathology 13, 1-3.

Nandi M, Macdonald J, Liu P, Weselowski B & Yuan Z-C (2018) Clavibacter michiganensis ssp. michiganensis: bacterial canker of tomato, molecular interactions and disease management. Molecular Plant Pathology 19, 2036-2050.

Nouioui I, Carro L, García-López M, Meier-Kolthoff JP, Woyke T, Kyrpides NC, Pukall R, Klenk H-P, Goodfellow M & Göker M (2018) Genome-based taxonomic classification of the phylum Actinobacteria. Frontiers in Microbiology 9, 1-119.

Oh EJ, Bae C, Lee HB, Hwang IS, Lee HI, Yea MC, Yim KO, Lee S, Heu S, Cha JS, Oh CS (2016) Clavibacter michiganensis subsp. capsici subsp. nov., causing bacterial canker disease in pepper. International Journal of Systematic and Evolutionary Microbiology 66(10), 4065-4070.

Osdaghi E, Rahimi T, Taghavi SM, Ansari M, Zarei S, Portier P, Briand M & Jacques MA (2020) Comparative genomics and phylogenetic analyses suggest several novel species within the genus Clavibacter, including nonpathogenic tomato-associated strains. Applied and Environmental Microbiology 86, e02873-19.

Ramachandran S, Dobhal S, Alvarez AM & Arif M (2021) Improved multiplex TaqMan qPCR assay with universal internal control offers reliable and accurate detection of Clavibacter michiganensis. Journal of Applied Microbiology 131, 1405-1416.

Sharabani G, Shtienberg D, Borenstein M, Shulhani R, Lofthouse M, Sofer M, Chalupowicz L, Barel V & Manulis-Sasson S (2013) Effects of plant age on disease development and virulence of Clavibacter michiganensis subsp. michiganensis on tomato. Plant Pathology 62, 1114-1122.

Stamova L & Sotirova V (1987) Reaction of different crops to artificial inoculation with Corynebacterium michiganense (E.F. Sm.) H.L. Jensen. Archiv fur Phytopathologie und Pflanzenschutz 23, 211-216.

Thapa SP, O’Leary M, Jacques M-A, Gilbertson RL & Coaker G (2020) Comparative genomics to develop a specific multiplex PCR assay for detection of Clavibacter michiganensis. Phytopathology 110, 556-566.

Thyr BD, Samuel MJ & Brown PG (1975) New solanaceous host records for Corynebacterium michiganensis. Plant Disease Reporter 59, 595-598.

Van Vaerenbergh J & Chauveau JF (1985) Host plant inoculations for the detection of (latent) Corynebacterium michiganense (E. F. Smith) Jensen. Mededelingen van de faculteit landbouwwetenschappen Rijksuniversiteit Gent 50, 973-995.

Yim K-O, Lee H-I, Kim J-H, Lee S-D, Cho J-H & Cha J-S (2012) Characterization of phenotypic variants of Clavibacter michiganensis subsp. michiganensis isolated from Capsicum annuum. European Journal of Plant Pathology 133, 559-575.

This datasheet was extensively revised in 2022 by Michiel J.C. Pel and Maria Bergsma-Vlami (NVWA, Netherlands Food and Consumer Product Safety Authority). Their valuable contribution is gratefully acknowledged.

EPPO (2024) Clavibacter michiganensis. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-11-21)

This datasheet was first published in the EPPO Bulletin in 1982 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2022. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1982) Data sheets on quarantine organisms, Corynebacterium michiganense. EPPO Bulletin 12(1), 13-18. https://doi.org/10.1111/j.1365-2338.1982.tb01950.x