Preferred name: Curtobacterium flaccumfaciens pv. flaccumfaciens
Authority: (Hedges) Collins & Jones
Taxonomic position: Bacteria: Actinobacteria: Micrococcales: Microbacteriaceae
Other scientific names: Bacterium flaccumfaciens Hedges, Corynebacterium flaccumfaciens pv. flaccumfaciens (Hedges) Dowson, Corynebacterium flaccumfaciens (Hedges) Dowson, Phytomonas flaccumfaciens (Hedges) Bergey et al., Pseudomonas flaccumfaciens (Hedges) Stevens
Common names in English: bacterial tan spot of bean, bacterial tan spot of soybean, bacterial wilt of bean, bacterial wilt of common bean, bacterial wilt of dry beans, vascular wilt of bean
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Notes on taxonomy and nomenclature EPPO Categorization: A2 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: CORBFL

The main hosts are all Fabaceae, including edible dry beans: Phaseolus spp., especially common bean (P. vulgaris), but also runner bean (P. coccineus) and lima bean (P. lunatus); adzuki or red mung bean (Vigna angularis), mung bean (V. radiata) and black gram (V. mungo); C. flaccumfaciens pv. flaccumfaciens can also attack soybean (Glycine max), pea (Pisum sativum), cowpea (Vigna unguiculata) and dolichos bean (Lablab purpureus). On soybean the disease and its causal agent were first reported in the USA in Iowa in 1975 and the disease was named bacterial tan spot (Dunleavy, 1983). In 2013 soybean was also reported as a host from Brazil (Soares et al., 2013).

Epiphytic and endophytic colonization can occur in other non-fabaceous crops. Under field conditions in Brazil, C. flaccumfaciens pv. flaccumfaciens was found to colonize, without causing symptoms, barley (Hordeum vulgare), black oat (Avena strigosa), canola (Brassica napus), common or white oat (A. sativa), ryegrass (Lolium spp.) and wheat (Triticum spp.), when they were cultivated in rotation with common bean. All C. flaccumfaciens pv. flaccumfaciens strains isolated from these plants were pathogenic to common bean (Gonçalves et al., 2017). In the USA, Harveson et al. (2015) isolated dry bean-pathogenic orange and yellow C. flaccumfaciens pv. flaccumfaciens strains from wheat plants also infected by Xanthomonas translucens showing black chaff symptoms, which are typical for infections by the latter bacterium, and from maize leaves also infected with Goss’ wilt disease, caused by Clavibacter michiganensis subsp. nebraskensis. In Iran, dry bean-pathogenic strains of C. flaccumfaciens pv. flaccumfaciens were isolated from symptomless eggplant (Solanum melongena), pepper (Capsicum spp.), and tomato (Solanum lycopersicum) plants (Osdaghi et al., 2018a).

C. flaccumfaciens pv. flaccumfaciens has been detected in weeds such as Lupinus polyphyllus (Schuster & Sayre, 1967), Amaranthus retroflexus, Chenopodium album, Vicia villosa, (Schuster, 1959) and Ipomoea lonchophylla (Condé & Diatloff, 1991; Osdaghi et al., 2020). Nascimento et al. (2020) reported that experiments using artificial inoculation under field conditions showed that the following weeds are potential, symptomless, hosts for C. flaccumfaciens pv. flaccumfaciens: Amaranthus viridis, Conyza bonariensis, Commelina benghalensis, Cyperus rotundus, Digitaria insularis, Emilia fosbergii, Galinsoga parviflora, Gnaphalium purpureum, Ipomoea triloba, Lepidium virginicum, Nicandra physalodes, Raphanus sativus, Senna obtusifolia, and Solanum americanum.

For additional information, see Harveson et al., 2015 and Osdaghi et al., 2020.

Host list: Amaranthus retroflexus, Amaranthus viridis, Avena sativa, Avena strigosa, Brassica napus, Chenopodium album, Cicer arietinum, Commelina benghalensis, Cyperus rotundus, Digitaria insularis, Emilia fosbergii, Erigeron bonariensis, Galinsoga parviflora, Gamochaeta purpurea, Glycine max, Helianthus annuus, Hordeum vulgare, Ipomoea lonchophylla, Ipomoea triloba, Lablab purpureus, Lepidium virginicum, Lolium, Lupinus polyphyllus, Medicago sativa, Nicandra physalodes, Phaseolus coccineus, Phaseolus lunatus, Phaseolus vulgaris, Pisum sativum, Raphanus sativus, Senna obtusifolia, Solanum americanum, Triticum aestivum, Vicia faba, Vicia lens, Vicia villosa, Vigna angularis, Vigna mungo, Vigna radiata, Vigna unguiculata subsp. sesquipedalis, Vigna unguiculata, Zea mays, Zornia glabra

Bacterial wilt was first observed in the USA (South Dakota) in 1920, and in subsequent years in Idaho, Maryland, Michigan, Montana, Virginia and Washington DC (Hedges, 1926). From the 1920s to the 1960s, the disease spread to four more states (Colorado, Nebraska, North Dakota, and Wyoming) with severe outbreaks occurring in the 1930s and 1960s (Harveson, 2013). The disease was subsequently observed in Ontario, Canada in 1954 (Patrick, 1954) and Mexico in 1955 (Yerkes & Crispin, 1956). After a period of low incidence there was a substantial reoccurrence of the disease in North America, especially in Colorado, Wyoming and Nebraska in the USA and Alberta in Canada in the 2000s (Harveson et al., 2015).

In South America the bacterium was reported on common bean (Phaseolus vulgaris) from Colombia (1982), Venezuela (1990) and Brazil (1995), see Osdaghi et al. (2020). 

The first report outside the Americas was from Australia (Wood & Easdown, 1990), where mung bean (Vigna radiata) and cowpea (Vigna unguiculata) were the hosts affected.

In the EPPO region, incidental records of C. flaccumfaciens pv. flaccumfaciens on common bean and soybean have been made and in some of these cases, the disease was later reported to be eradicated. Until now, no economic losses have been reported in bean or soybean crops (Bastas & Sahin, 2017; CABI, 2020; González et al., 2005; Ishimaru et al., 2005; O’Leary & Gilbertson, 2020; Sammer & Reiher, 2012; Sonmezalp, 1966).

The first finding in the Middle East was in Iran in 2013 in common bean and cowpea (Osdaghi et al., 2015a and 2015b).

In Africa, the first confirmed case is from Zambia in soybean (Pawlowski and Hartman, 2019).

EPPO Region: Belgium, Netherlands, Russia (Central Russia, Far East, Southern Russia), Switzerland, Tunisia, Türkiye
Africa: Mauritius, Tunisia, Zambia
Asia: Iran
North America: Canada (Alberta, Manitoba, Ontario, Québec, Saskatchewan), United States of America (Colorado, Connecticut, Idaho, Iowa, Michigan, Montana, Nebraska, North Dakota, Ohio, Oregon, Virginia, Wisconsin, Wyoming)
South America: Brazil (Distrito Federal, Goias, Mato Grosso do Sul, Minas Gerais, Parana, Santa Catarina, Sao Paulo), Colombia, Venezuela
Oceania: Australia (New South Wales, Queensland, South Australia, Victoria)

C. flaccumfaciens pv. flaccumfaciens is seedborne and can be transmitted both within and on the seed; it is very resistant to drying and has been found to remain viable for up to 24 years in seed stored under laboratory conditions (Burkholder, 1945). In soil, survival is much shorter and, in the case of bean crops rotated with wheat, survival does not exceed two winters. The bacterium is able to survive longer in plant debris and non-hosts, including non-leguminous crops and weeds. The practice of minimum tillage or no-tillage farming for soil moisture conservation therefore enhances survival of C. flaccumfaciens pv. flaccumfaciens and favours new infections in bean crops (Gonçalves et al., 2017 and 2018; Silva Júnior 2012; Urrea & Harveson, 2014).

The bacterium may enter roots and above-ground plant parts through wounds, usually under windy, hailstorm type of weather. Entry through stomata is rare, unlike other bacterial bean pathogens. There are no reports of vectors, but the nematode Meloidogyne incognita may assist entry by wounding roots (Schuster, 1959).

Inside the plant the bacterium spreads mainly via the xylem, where it is often present in biofilms.

Disease development and expression is stimulated by temperatures above 30°C. Latent infection and colonization of seeds and plants is possible, especially at lower temperatures. C. flaccumfaciens pv. flaccumfaciens can infect plants in the absence of rain; however, disease progression is associated with warm moist conditions and spread of the bacterium is favoured by overhead sprinkler irrigation. The more recent outbreaks of C. flaccumfaciens pv. flaccumfaciens in North America, observed after some 20 years of non-detection, may result from changed cultural practices (such as increased sprinkler irrigation), climate change to warmer and moister summers, spread from alternative hosts and lack of experience with the disease because of the long period in which it has not been recorded (Harveson et al., 2006; Harveson & Vidaver, 2008; Harveson, 2013; Osdaghi et al., 2016). Host species/cultivar susceptibility, weather conditions and agricultural practices are therefore important factors in disease outbreaks and their severity (Harveson et al., 2015).

There is no information on race variation. Yellow colony variants, however, are more virulent than the red/orange ones on a number of hosts including cowpea, lima bean, broad bean (Vicia faba) and pea and only these yellow colony variants cause disease on hairy vetch (Vicia villosa), a major weed in dry bean growing areas of Iran (Osdaghi et al. 2015b).

In a comparative genomics study of C. flaccumfaciens pv. flaccumfaciens with actinobacterial plant pathogens, a set of unique low G+C% content genomic islands were detected in the C. flaccumfaciens pv. flaccumfaciens genome. Homologous sequences of pathogenicity-determining loci found in these islands were those responsible for production of 1,4-beta-xylanase (xylA), pectate lyase (pelA1 and pelA2), serine protease (chpC, chpG, and pat-1), and sortase (srtA) (Chen et al., 2020).

For additional information, see also Harveson et al. (2015), Hedges (1926), Osdaghi et al., (2020), Zaumeyer (1932), Zaumeyer & Thomas (1957).

Symptoms

The most severe symptoms occur on young Phaseolus plants just emerged from seed. When infected, they usually die. If plants survive an early attack, or are infected at a later stage of growth, they may survive throughout the season and bear mature seed. All the developmental stages of the plant are susceptible. The disease is characterized by initial interveinal chlorosis that becomes later necrotic due to systemic vascular infection, leading to wilting of leaves or parts of leaves during the heat of the day and recovery as the temperature drops in the evening. Bacterial plugging of the vessels cuts off the water supply and the leaves turn brown and fall prematurely. Wilting may eventually cause plant death. During hailstorms or under strong winds necrotic tissues may easily rupture; symptomatic leaves will then have a ragged appearance and may drop down. 

Occasionally these typical wilting symptoms may be absent, but instead there are golden-yellow necrotic leaf lesions, closely resembling those of common blight caused by Xanthomonas axonopodis pv. phaseoli (EPPO/CABI, 1996). The lesion margin, however, is more irregular in C. flaccumfaciens pv. flaccumfaciens infections. In general, there is no water-soaking of stems and leaves, as found in common blight and halo blight (Pseudomonas savastanoi pv. phaseolicola) infections.

On pods the disease is much more conspicuous than common blight. All the seeds in a pod may be infected, while the pod remains apparently healthy. This is due to the pathogen infecting the seed via the vascular system, following the sutures of the pods, which may be discoloured. On young pods, water-soaked spots occasionally appear, the area turning to either a yellowish-green or darker colour than the rest of the pod. On ripe pods lesions are more conspicuous, being an olive-green colour in contrast to the yellow colour of the normal pod. It should be noted that seemingly vigorous plants may bear one or more shrivelled shoots or infected pods which are hidden by healthy foliage.

When older plants are heavily infected, flowers may also be blighted and seed set severely reduced (Wood & Easdown, 1990).

Seeds of white-seeded bean cultivars, when infected systemically, may be discoloured and appear yellow, orange, pink, or purple; however, in cultivars with coloured seed coats the discolouration is less conspicuous. There may be a little bacterial slime present at the hilum, and seeds may be shrivelled. 

On cowpea the necrotic areas on infected leaves tend to have chlorotic margins; this is less common in other hosts. On mung bean, as well as soybean, severe wilting of infected plants rarely occurs, and the intercostal necrosis has a pale brown to tan colour, leading to the name ‘tan spot’ for the disease in these two crops.   

For additional information, see Hedges (1926), Zaumeyer (1932), Zaumeyer & Thomas (1957), Schuster et al. (1968), Harveson (2013), Harveson et al. (2015); Osdaghi et al. (2020). 

Morphology 

C. flaccumfaciens pv. flaccumfaciens is an aerobic, motile, Gram-positive, non-sporing rod, occurring singly or in pairs, 0.3-0.5 x 0.6-3.0 µm with one to three lateral or polar flagella.

Preliminary identification is hampered by the occurrence of at least five different colony colour variants on culture media: yellow, orange, pink, red and purple (yellow colony, but with purple diffusible pigment). C. flaccumfaciens pv. flaccumfaciens strains possessing different pigmentation produce bacteriocins against the other strains in culture media (Osdaghi et al., 2018a).

On non-selective media, such as yeast-peptone-glucose agar (YPGA) or nutrient broth yeast extract agar (NBY), after 48-72h of growth at 25-27°C colonies of C. flaccumfaciens pv. flaccumfaciens are circular, 2–4 mm in diameter, smooth and with entire margins, more often convex and translucent, but sometimes also flat and semi-opaque. As stated above, their pigmentation is variable, also depending on temperature and pH, and vary from creamy to bright yellow or red/orange. Therefore, in case of doubt, several colonies should be selected.

For further information, see EPPO (2011); Osdaghi et al., (2020).

Detection and identification methods 

Inspection in the field

Visual inspection of plants with symptoms should be followed, when possible, by laboratory diagnosis.

Bacteria may be detected beneath the seedcoat by means of a combined cultural and immunofluorescence (IF) test (see below). Bean seed from countries where the disease is known to occur should be visually inspected for discolouration of the seed coat. 

Laboratory detection and diagnosis

Direct isolation, IF and/or PCR can be used as screening tests. IF protocols have been described for seed tests, using polyclonal (Calzolari et al., 1987) or monoclonal antibodies (Diatloff et al., 1993). Specificity (false-negatives) and sensitivity, however, are less than PCR-based tests (McDonald & Wong, 2000). 

Semi-selective media for in vitro growth of C. flaccumfaciens pv. flaccumfaciens were developed by Mizuno & Kawai, 1993; Tegli et al., 1998; Maringoni & Camara, 2006. The medium of Tegli et al. (1998), is detailed in EPPO (2011). 

Two polymerase chain reaction (PCR) tests with different specific primer sets have been described for the identification of C. flaccumfaciens pv. flaccumfaciens isolated colonies and for its detection in bean seed extracts: one according to Guimaraēs et al. (2001) and the other according to Tegli et al. (2002). They are detailed in EPPO (2011). A method improving the isolation of bacteria and DNA from bean leaves, using the primers of Tegli et al. (2002) was developed by Puia et al. (2021b).

A sensitive Loop-Mediated Isothermal Amplification (LAMP) based detection method for C. flaccumfaciens pv. flaccumfaciens has recently been developed by Tegli et al. (2020), and could be, after further validation, useful for on-site testing of seeds and plants.

When positive PCR results on plant/seed samples are obtained, direct isolation of viable C. flaccumfaciens pv. flaccumfaciens cells on non-specific and semi-selective agar media should be performed.

BOX-PCR and multilocus sequence analysis (MLSA) with the housekeeping genes atpD, gyrB, ppk, recA and rpoB can be used for identification; both methods were able to discriminate between yellow-pigmented strains and red/orange pigmented strains. Non-pathogenic strains of C. flaccumfaciens pv. flaccumfaciens could be discriminated from pathogenic strains on the basis of sensitivity to sodium arsenate and sodium arsenite (Osdaghi et al., 2018b). Rep PCR, including Box-PCR, is described in detail in EPPO (2010).

Details about presumptive diagnosis with rapid tests, detection and identification methods (including methods for extraction of bacterial cells and DNA), biochemical, serological and molecular and pathogenicity tests (using inoculation of bean plantlets or hilum injury/seed inoculation) for latent and symptomatic infected material, flow chart, culture media, chemicals and reference material) are provided in the EPPO Standard PM 7/102 (1), 2011 on Curtobacterium flaccumfaciens pv. flaccumfaciens.

Spread of the bacterium over short and long distances is mainly through movement of infected seeds (Hedges, 1926; Zaumeyer, 1932; Zaumeyer & Thomas, 1957; Hsieh et al., 2006; Camara et al., 2009; Bastas & Sahin, 2017, Osdaghi et al., 2020). Other parts of infected plants or their residues, however, are also potential inoculum sources (Silva Júnior et al., 2012b; Gonçalves et al., 2017). Especially sprinkler irrigation and windy/hailstorm type of weather may enhance survival and dispersion of C. flaccumfaciens pv. flaccumfaciens within fields where infected plants and/or their residues are present. Dispersal via machinery/humans/animals/surface water has been little investigated and is poorly understood. Persistence and continuation of infection can be due to colonization (epiphytic and endophytic) of symptomless-host plants such as crops (e.g., barley, canola, ryegrass, oat) grown in rotation with fabaceous hosts, or weeds (e.g., Amaranthus retroflexus, Chenopodium album). 

In conclusion, contaminated/infected seeds are the most likely pathway of spread to cause infection of host plants in other areas of the world. Symptomless weed and crop hosts play a local role. No insect vectors have been found.

Economic impact

Economic losses due to bacterial wilt disease result from lower crop yields as well as lower marketability as a result of quality loss due to discoloured and shrivelled seeds (Huang et al., 2009).

Following the first report of its occurrence in 1920, bacterial wilt became one of the most important bacterial diseases of beans in the USA, causing almost total losses in some years, but the disease gradually declined in later years. By the 1970s the disease had become manageable by planting pathogen-free/tested seeds, crop rotation, and sanitation measures. In the early 2000s, however, bacterial wilt re-emerged (first in North Dakota in 1995 and later in Colorado, Nebraska, and Wyoming from 2004 to 2007) and became an economically-damaging disease in those states, as well as in Canada where the yellow and orange variants were found in 2002, followed by the purple variant in 2006 (Harveson et al. 2015; Huang et al., 2009). In soybean, yield losses were reported to be very variable depending on the year; losses were often only minor, but could reach 18.5% in the USA (Dunleavy et al., 1983; Dunleavy, 1984).

Over the past ten years outbreaks with economically important yield losses have been reported from Australia, Brazil, Canada, Iran and the central high plains in the USA (Osdaghi et al, 2020; Puia et al., 2021a). In most of these countries the disease is sporadic, and its incidence varies greatly. In C. flaccumfaciens pv. flaccumfaciens endemic areas in the USA and Australia (on mung bean), disease incidence has reached more than 90% in the past (Harveson et al., 2015; Wood & Easdown, 1990).

There is practically no information on yield losses or economic impact of the outbreaks or introductions recorded in Europe, including the Russian Federation.

Control 

The most effective measure to prevent the entry, establishment and spread of C. flaccumfaciens pv. flaccumfaciens is the use of healthy seeds. Seed grown in dry climates is usually free from infection and therefore whenever possible it is advisable to grow seed crops in these dry areas.

Chemical control

Chemical (seed) treatments, including NaOCl 5% for 10 min, copper compounds and antibiotics have not been found effective against C. flaccumfaciens pv. flaccumfaciens. Antibiotics eliminated bacteria only from the seed surface and showed phytotoxicity (Estefani et al., 2007; Harveson, 2019; Tripepi & George, 1991). The use of antibiotics against plant pathogens is not permitted in many EPPO countries.

Soares et al. (2004) found that treatment with acibenzolar-S-methyl was ineffective in inducing resistance of the plant to the bacterium.

However, Harveson (2019) reported the results of a 7-year (2010-2016) field study investigating treatments with hydrogen peroxide and peroxyacetic acid and plant-based fatty acids. These consistently resulted in higher seed yields than copper/antibiotic treatments, although disease incidence was not reduced. This positive yield effect held true especially for heavily-infested crops.

Heat treatments

No suitable heat treatments have been developed for use in practice. Dry heat treatments (at 52°C for 20 h and 85°C for 5 h or at 60°C and even at 70ºC for more than 3 h) alone, or in combination with pre-soaking seeds in water for more than 3 h, significantly reduced the vigour of the seeds but usually did not eliminate the bacterium (Zaumeyer & Thomas, 1957; Estafena et al., 2007).

Biological control

No biological control method for C. flaccumfaciens pv. flaccumfaciens is operational in practice to date (Osdaghi et al., 2020). Under greenhouse conditions and artificial seed inoculation with C. flaccumfaciens pv. flaccumfaciens, a treatment of seeds with a strain of Bacillus subtilis (ALB629rif) gave a disease reduction of 71% and 75%, at 20 and 30°C respectively, (Martins et al., 2014). Soaking seeds of great northern bean cv. US1140 in a suspension of the bacterium Pantoea agglomerans gave good endophytic colonization of the entire bean seedling and in combination with artificial infection with C. flaccumfaciens pv. flaccumfaciens, gave reduction in disease severity of up to 70% and better emergence and seedling growth (Hsieh et al., 2005). Seed treatment under greenhouse conditions with Rhizobium leguminosarum biovar viceae R2 had a mild protective effect for seeds that showed no or light symptoms only (Huang et al., 2007a).

Plant resistance

In addition to the use of healthy, tested seed, the other main control measure is the broader use of resistant cultivars. However, resistant, commercially attractive varieties are still scarce. For example, the common bean cv. Emerson is resistant, but has only a small (Europe-targeted) market. True resistance was found in a germplasm collection accession PI 325691, a wild common bean (P. vulgaris) from near Tzitzio, Michoacán, Mexico (Urrea & Harveson, 2014). In greenhouse tests, Huang et al. (2007b) determined resistance in some varieties and a line of common bean against the purple variant of C. flaccumfaciens pv. flaccumfaciens.

A high level of resistance to three variants of C. flaccumfaciens pv. flaccumfaciens (yellow, orange, and purple) was observed in the light red kidney bean cultivars AC Litekid, Chinook 2000, and Redkanner as well as dark red kidney bean cultivars Cabernet and Red Hawk in Canada and could be useful in breeding programmes (Conner et al., 2008).

Under greenhouse conditions in Brazil, Maringoni et al. (2015) observed resistance in a number of local, varieties and lines of common bean. A rapid method for screening of resistance against C. flaccumfaciens pv. flaccumfaciens has been described by Hsieh et al. (2003).

Cultural control

Common bean should preferably be grown in a rotation with non-hosts and not in succession (in the rotation scheme) with barley, black oat, oilseed rape, maize, ryegrass, sunflower, wheat and white oat when the disease is prevalent (Gonçalves et al., 2017 and 2021; Nascimento et al., 2020). Crop debris, weed hosts and volunteer plants should be carefully removed when the disease is already present. 

Phytosanitary risk

From its existing distribution and biology, the disease seems most likely to be important in the southern part of the EPPO region where dry bean species and soybean are widely grown. A risk evaluation of C. flaccumfaciens pv. flaccumfaciens for the European Union has been made by the European Food Safety Authority which concluded that the pathogen had the potential to establish, spread and have an impact on its host crops (EFSA, 2018).

C. flaccumfaciens pv. flaccumfaciens is most likely to re-enter pest-free areas or spread further via infected host seeds. No records of interception of this bacterium were made in the European Union database between 2005 and 2018 (Europhyt, 2019). Past records of the disease in Spain and Germany could possibly be linked to the import of infected seeds, although the origin of these seeds was not reported (González et al., 2005; Sammer & Reiher, 2012).

Based on the various literature sources cited here, C. flaccumfaciens pv. flaccumfaciens can establish itself, climate-wise, in the EPPO region. Host plants are widely grown throughout the EPPO region. In 2019, dry pulses were grown on 2.17 million hectares in the European Union territory (about 2% of the total arable land), with a production of about 4.75 million tonnes. France, the United Kingdom, Poland and Spain were the largest producers in 2019 (Eurostat, 2021).

The production of soybean has been recently increasing in Europe. In 2018, 10 million tonnes of soybean were produced from the cultivation of 4.3 million ha. The acreage of soybean has doubled over the last seven years (Donausoja, 2021). The relatively steady growth in soybean production in the European Union halted in 2019 there was a decline in the area harvested (-5.0 %) and production (-3.4 %). Nevertheless, the 2.8 million tonnes of soybean produced in the European Union in 2019 was 1.9 million tonnes more than a decade earlier (Eurostat, 2021).

The disease caused by C. flaccumfaciens pv. flaccumfaciens has an erratic character, prevalent in some years, absent or very minor in others. Its present distribution in Europe may therefore may well be underestimated, as in many EU/EPPO region countries no systematic surveys for this bacterium are carried out. Declarations of eradication and absence should therefore be regarded with caution.

Phytosanitary (quarantine) measures can be implemented to reduce the risk of long-distance dissemination of the pathogen. It can be recommended that consignments of host seeds should have been produced from pest-free areas, or from pest-free places or sites of production.

Seed inspections of dry beans in intra- and international transport will assist in preventing the pathogen’s spread to areas with no history of the disease. However, visual inspection of imported seeds is not very reliable due to the occurrence of latent infections and therefore, when material is imported from areas where the disease is known to occur, field inspections and laboratory testing are necessary (EPPO 2011, 2021). For the European Union, measures on certification and inspections of dry bean seeds and soybean to guarantee the health status of seeds before marketing in the EU are provided by Council Directive 2002/55/EC.

Management of bacterial blight can also be achieved by rapid, reliable detection and identification of C. flaccumfaciens pv. flaccumfaciens (EPPO 2011) and, the use of pathogen-free/tested seeds. 

The EPPO diagnostic standard (EPPO 2011), whose wide and systematic application is another essential way to prevent entry and spread of the pathogen, should be used for diagnosis. 

The presence and possible importance of C. flaccumfaciens pv. flaccumfaciens needs to be checked in countries or regions where it was previously reported. This would include awareness campaigns for stakeholders. Over the past forty years, disease outbreaks/introductions have been sporadic; many years may pass between outbreaks in an infected area without any noticeable symptoms being observed (Harveson, 2013; Harveson et al., 2015).

Agarkova IV, Lambrecht PA, Vidaver AK & Harveson RM (2012) Genetic diversity among Curtobacterium flaccumfaciens pv. flaccumfaciens populations in the American High Plains. Canadian Journal of Microbiology 58, 788–801.

Allen DJ (1995) An annotated list of diseases of common bean in Eastern and Southern Africa. Phytopathological Papers 34, 42 pp. CAB International, Wallingford, UK.

Bastas KK & Sahin F (2017) Evaluation of seedborne bacterial pathogens on common bean cultivars grown in central Anatolia region, Turkey. European Journal of Plant Pathology 147, 239–253.

Bergey DH, Breed RS, Murray EGD & Hitchens AP (1939) Manual of Determinative Bacteriology. Fifth Edition, London, Bailliere, Tindall & Cox, 1032 pp.

Burkholder WH (1945) The longevity of the pathogens causing the wilt of the common bean. Phytopathology 35, 743–744.

CABI (2020) Curtobacterium flaccumfaciens pv. flaccumfaciens. https://www.cabi.org/isc/datasheet/15333

Calzolari A, Tomesani M & Mazzucchi U (1987) Comparison of immunofluorescence staining and indirect isolation for the detection of Corynebacterium flaccumfaciens in bean seeds. EPPO Bulletin 17, 157-163.

Camara RC, Vigo SC & Maringoni AC (2009) Plant to seed transmission of Curtobacterium flaccumfaciens pv. flaccumfaciens in a dry bean cultivar. Journal of Plant Pathology 91, 549–554.

Carlson RR & Vidaver AK (1982) Taxonomy of Corynebacterium plant pathogens, including a new pathogen of wheat, based on polyacrylamide gel electrophoresis of cellular proteins. International Journal of Systematic Bacteriology 32, 315-326.

Chavarro CA, Lopez GCA & Lenne JM (1985) Characteristics and pathogenicity of Corynebacterium flaccumfaciens pv. flaccumfaciens (Hedges) Dows causal agent of bacterial wilt of Zornia spp. and its effect on production of Z. glabra CIAT 7847 and Phaseolus vulgaris. Acta Agronomica 35, 64-79.

Chen YF, Guo JH & Fang ZD (2000) A new pathovar of Curtobacterium flaccumfaciens on malabar spinach. Acta Phytopathologica Sinica 30,171–175.

Chen YF, Yin YN, Zhang XM & Guo JH (2007) Curtobacterium flaccumfaciens pv. beticola, a new pathovar of pathogens in sugar beet. Plant Disease 91, 677–684.

Chen G, Khojasteh M, Taheri-Dehkordi A, Taghavi SM, Rahimi T & Osdaghi E (2020) Complete genome sequencing provides novel insight into the virulence repertories and phylogenetic position of dry beans pathogen Curtobacterium flaccumfaciens pv. flaccumfaciens. Phytopathology 111, 268-280. https://doi.org/10.1094/PHYTO-06-20-0243-R.

Collins MD & Jones D (1983) Reclassification of Corynebacterium flaccumfaciens, Corynebacterium betae, Corynebacterium oortii and Corynebacterium poinsettiae in the genus Curtobacterium, as Curtobacterium flaccumfaciens comb. nov. Journal of General Microbiology 129, 3545-3548.

Condè BD & Diatloff A (1991) Diseases in mungbean. In: Imrie BC, Lawn RJ (eds.). Mungbean: The Australian Experience. Proceedings of the first Australian mungbean workshop. CSIRO Division of Tropical Crops and Pastures, Brisbane. pp. 73–77.

Conner RL, Balasubramanian P, Erickson RS, Huang HC & Mündel HH (2008) Bacterial wilt resistance in kidney beans. Canadian Journal of Plant Science 88, 1109–1113.

Diatloff A, Wong WC & Wood BA (1993) Non-destructive methods of detecting Curtobacterium flaccumfaciens pv. flaccumfaciens in mungbean seeds. Letters in Applied Microbiology 16, 269–273.

Donausoja (2021) Soya cultivation in Europe. https://www.donausoja.org/fileadmin/user_upload/Downloads/Soya_cultivation_in_Europe_plus_DS_Benefits.pdf. Retrieved 2021-06-11.

Dowson WJ (1942) The generic name of the Gram-positive bacterial plant pathogens. Transactions of the British Mycological Society 25, 311-314.

Dunleavy JM (1983) Bacterial tan spot, a new foliar disease of soybeans. Crop Science 23, 473–476.

Dunleavy JM (1984) Yield losses in soybeans caused by bacterial tan spot. Plant Disease 68, 774-776. 

EFSA (2018) EFSA Panel on Plant Health (M. Jeger et al.) Pest categorisation of Curtobacterium flaccumfaciens pv. flaccumfaciens. EFSA Journal 2018, 16, 5299, 22 pp. https://doi.org/10.2903/j.efsa.2018.5299

EPPO (2021) EPPO Global Database. Accessed May 2018. Available online: https://gd.eppo.int. Retrieved June 2021.

EPPO/CABI (1996) Xanthomonas axonopodis pv. phaseoli. In: Quarantine pests for Europe. 2nd edition (Ed. by Smith, I.M.; McNamara, D.G.; Scott, P.R.; Holderness, M.). CAB INTERNATIONAL, Wallingford, UK. 

EPPO (2010) PM 7 ⁄ 100 Rep-PCR tests for identification of bacteria. EPPO Bulletin 40, 365–368.

EPPO (2011) PM 7/102(1) Curtobacterium flaccumfaciens pv. flaccumfaciens. EPPO Bulletin 41, 320-328 (see also corrigendum to this Standard published EPPO Bulletin (2021) 51 (1), 234).

Europhyt (2019) Europhyt-interceptions, European Union notification system for plant health interceptions Annual Report 2018. DG(SANTE) 2019-6845,55 pp.

Estefani RCC, Miranda Filho RJ & Uesugi CH (2007) [Thermal and chemical treatments of common bean seeds: efficiency in Curtobacterium flaccumfaciens pv. flaccumfaciens eradication and effects on the physiological quality of seeds]. Fitopatologia Brasileira 32, 434-438 (in Portuguese). https://doi.org/10.1590/S0100-41582007000500011

Eurostat (2021) https://ec.europa.eu/eurostat/web/products-datasets/-/tag00094. Retrieved 2021-06-11.

Gonçalves RM, Schipanski CA, Koguishi L, Soman JM, Sakate RK, Silva Junior TAF & Maringoni AC (2017) Alternative hosts of Curtobacterium flaccumfaciens pv. flaccumfaciens, causal agent of bean bacterial wilt. European Journal of Plant Pathology 148, 357–365.

Gonçalves RM, Balbi-Peña MI, Soman JM, Maringoni AC, Taghouti G, Fischer-le Saux M & Portier P (2019) Genetic diversity of Curtobacterium flaccumfaciens revealed by multilocus sequence analysis. European Journal of Plant Pathology, 154 189-202. https://doi.org/10.1007/s10658-018-01648-0

Gonçalves RM, da Silva Júnior TAF, Soman JM & Maringoni AC (2021) Effect of crop rotation on common bean cultivars against bacterial wilt caused by Curtobacterium flaccumfaciens pv. flaccumfaciens. European Journal of Plant Pathology 159, 485–493. https://doi.org/10.1007/s10658-020-02176-6

González AJ, Tello JC & Rodicio MR (2005) Bacterial wilt of beans (Phaseolus vulgaris) caused by Curtobacterium flaccumfaciens in south-eastern Spain. Plant Disease 89, 1361.

Guimaraēs PM, Palmano S, Smith JJ, Grossi de Sá MF & Saddler MF (2001) Development of a PCR test for the detection of Curtobacterium flaccumfaciens pv. flaccumfaciens. Antonie Van Leeuwenhoek 80, 1–10. https://doi.org/10.1023/A:1012077425747.

Harveson RM (2013) The multicolored bacterium. In: APS Features. https://www.apsnet.org/edcenter/apsnetfeatures/Pages/bacterium.aspx

Harveson RM (2019) Managing dry bean bacterial diseases in Nebraska with new copper-alternative chemicals. Plant Health Progress 20,14–19.

Harveson RM, Schwartz HF, Vidaver AK, Lambrecht PA & Otto KL (2006) New outbreaks of bacterial wilt of dry bean in western Nebraska observed from field infections. Plant Disease 90, 81.

Harveson RM, Schwartz HF, Urrea CA & Yonts CD (2015) Bacterial wilt of dry-edible beans in the central high plains of the U.S.: past, present, and future. Plant Disease 99, 1665–1677.

Harveson RM & Vidaver AK (2008) A new color variant of the dry bean bacterial wilt pathogen (Curtobacterium flaccumfaciens pv. flaccumfaciens) found in western Nebraska. Plant Health Progress. Published online: https://doi.org/10.1094/php-2008-0815-01-br

Hedges F (1922) A bacterial wilt of bean caused by Bacterium flaccumfaciens nov. sp. Science 55, 433-434.

Hedges F (1926) Bacterial wilt of beans (Bacterium flaccumfaciens Hedges), including comparisons with Bacterium phaseoli. Phytopathology 16, 1-22.

Hsieh TF, Huang HC, Mündel HH & Erickson SR (2003) A rapid indoor technique for screening common bean (Phaseolus vulgaris L.) for resistance to bacterial wilt [Curtobacterium flaccumfaciens pv. flaccumfaciens (Hedges) Collins and Jones]. Revista Mexicana de Fitopatología 21, 370–374.

Hsieh TF, Huang HC, & Erickson RS (2005) Biological control of bacterial wilt of bean using a bacterial endophyte, Pantoea agglomerans. Journal of Phytopathology 153, 608–614.

Hsieh TF, Huang HC & Erickson RS (2006) Bacterial wilt of common bean: effect of seedborne inoculum on disease incidence and seedling vigour. Seed Science and Technology 34, 57-67.

Huang HC, Erickson RS, Yanke LJ, Chelle CD & Mündel HH (2006) First report of the purple variant of Curtobacterium flaccumfaciens pv. flaccumfaciens, causal agent of bacterial wilt of bean, in Canada. Plant Disease 90, 1262.

Huang HC, Erickson RS & Hsieh TF (2007a) Control of bacterial wilt of bean (Curtobacterium flaccumfaciens) by seed treatment with Rhizobium leguminosarum. Crop Protection 26, 1055–1061.

Huang HC, Mündel HH, Erickson RS, Chelle CD, Balasubramanian PM, Kiehn F & Conner RL (2007b) Resistance of common bean (Phaseolus vulgaris L.) cultivars and germplasm lines to the purple variant of bacterial wilt (Curtobacterium flaccumfaciens pv. flaccumfaciens). Plant Pathology Bulletin 16, 91–95.

Huang HC, Erickson RS, Balasubramanian PM, Hsieh TF & Conner RL (2009) Resurgence of bacterial wilt of common bean in North America. Canadian Journal of Plant Pathology 31, 290–300.

Ishimaru C, Mohan SK & Franc GD (2005) Bacterial wilt. In: Schwartz, H.F., Steadman, J.R., Hall, R. and Forster, R.L. (Eds.). Compendium of Bean Diseases, 2nd edition. St. Paul, MN: American Phytopathological Society, pp. 50–52.

Martins SJ, Medeiros FHV, Souza RM & Vilela LAF (2014) Is curtobacterium wilt biocontrol temperature dependent? Acta Scientiarum – Agronomy, Maringá 36, 409–415.

Maringoni AC & Camara RC (2006) Curtobacterium flaccumfaciens pv. flaccumfaciens detection in bean seeds using a semi-selective culture medium. Brazilian Journal of Microbiology 37, 451–455.

Maringoni AC, Ishiszuka MS, da Silva AP, Soman JM, Moura MF, dos Santos RL, da Silva Júnior TAF, Chiorato AF, Carbonell SAM & Fonseca Júnior NS (2015) Reaction and colonization of common bean genotypes by Curtobacterium flaccumfaciens pv. flaccumfaciens. Crop Breeding and Applied Biotechnology 15, 87–93.

McDonald JG & Wong E (2000) High diversity in Curtobacterium flaccumfaciens pv. flaccumfaciens characterized by serology and rep-PCR genomic fingerprinting. Canadian Journal of Plant Pathology 22, 17–22.

Mizuno A & Kawai A (1993) Studies on the diagnosis of foreign bacterial diseases of quarantine significance, VI: Curtobacterium flaccumfaciens pv. flaccumfaciens. Research Bulletin of the Plant Protection Service Japan 29, 27–36.

Nascimento DM, Oliveira LR, Melo LL, Silva JC, Soman JM, Ribeiro-Junior MR, Sartori MMP, Silva Júnior TAF & Maringoni AC (2020) Survival of Curtobacterium flaccumfaciens pv. flaccumfaciens in the phyllosphere and rhizosphere of crops. European Journal of Plant Pathology 160, 161–172. https://doi.org/10.1007/s10658-021-02232-9

O'Leary M & Gilbertson R (2020) Complete genome sequence resource of a strain of Curtobacterium flaccumfaciens pv. flaccumfaciens, the causal agent of bacterial wilt of common bean, from Turkey. Phytopathology doi: 10.1094/PHYTO-04-20-0131-A.

Osdaghi E, Sardrood PB, Bavi M, Akbari Oghaz N, Kimiaei S & Hadian S (2015a) First report of Curtobacterium flaccumfaciens pv. flaccumfaciens causing cowpea bacterial wilt in Iran. Journal of Phytopathology 163, 653–656. https://doi.org/10.1111/jph.12300

Osdaghi E, Taghavi SM, Fazliarab A, Elahifard E & Lamichhane JL (2015b) Characterization, geographic distribution and host range of Curtobacterium flaccumfaciens: An emerging bacterial pathogen in Iran. Crop Protection 78, 185-192. https://doi.org/10.1016/j.cropro.2015.09.015.

Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Harveson RM & Lamichhane JR (2016) Occurrence and characterization of a new red-pigmented variant of Curtobacterium flaccumfaciens, the causal agent of bacterial wilt of edible dry beans in Iran. European Journal of Plant Pathology 146, 129–145. https://doi.org/10.1007/s10658-016-0900-3.

Osdaghi E, Taghavi SM, Hamzehzarghani H, Fazliarab A, Harveson RM, Tegli S & Lamichhane JR (2018a) Epiphytic Curtobacterium flaccumfaciens strains isolated from symptomless solanaceous vegetables are pathogenic on leguminous but not on solanaceous plants. Plant Pathology 67, 388-398. 

Osdaghi E, Taghavi SM, Calamai S, Biancalani C, Cerboneschi M, Tegli S & Harveson RM (2018b) Phenotypic and molecular-phylogenetic analysis provide novel insights into the diversity of Curtobacterium flaccumfaciens. Phytopathology 108, 1154–1164.

Osdaghi E, Young AJ & Harveson RM (2020) Bacterial wilt of dry beans caused by Curtobacterium flaccumfaciens pv. flaccumfaciens: A new threat from an old enemy. Molecular Plant Pathology 21, 605-621. https://doi.org/10.1111/mpp.12926

Patrick ZA (1954) The antibiotic activity of soil microorganisms as related to bacterial plant pathogens. Canadian Journal of Botany 32, 705-735.

Pawlowski ML & Hartman GL (2019) First report of Curtobacterium flaccumfaciens pv. flaccumfaciens causing bacterial tan spot on soybean in Africa. Plant Disease 103, 2665.

Puia JD, Ferreira MGDB, Hoshino AT, Borsato LC, Canteri MG & Vigo SC (2021a) Occurrence of Curtobacterium flaccumfaciens pv. flaccumfaciens in the state of Paraná and its pathogenicity in beans. European Journal of Plant Pathology 159, 627–636. https://doi.org/10.1007/s10658-020-02193-5

Puia JD, Murari RR, Borsato LC, Sugahara VH, da Silva MG, Canteri MG & Vigo SC (2021b). Protocol for detecting Curtobacterium flaccumfaciens pv. flaccumfaciens in the leaves of infected bean plants (Phaseolus vulgaris L.). Acta Scientiarum. Agronomy, 43, e51031. https://doi.org/10.4025/actasciagron.v43i1.51031

Sammer UF & Reiher K (2012) Curtobacterium flaccumfaciens pv. flaccumfaciens on soybean in Germany - a threat for farming. Journal of Phytopathology 160, 314–316.

Schuster ML & Christiansen DW (1957) An orange-colored strain of Corynebacterium flaccumfaciens causing bean wilt. Phytopathology 47, 51–53.

Schuster ML (1959) Relation of root-knot nematodes and irrigation water to the incidence and dissemination of bacterial wilt of bean. Plant Disease Reporter 43, 27–32.

Schuster ML & Sayre RM (1967) A coryneform bacterium induces purple-coloured seed and leaf hypertrophy of Phaseolus vulgaris and other Leguminosae. Phytopathology 57, 1064–1066.

Schuster ML, Vidaver AK & Mandel M (1968) A purple pigment producing bean wilt bacterium, Corynebacterium flaccumfaciens var. violaceum n. var. Canadian Journal of Microbiology 14, 423-427.

Silva Júnior TAF, Negrão DR, Itako AT, Soman JM & Maringoni AC (2012) Survival of Curtobacterium flaccumfaciens pv. flaccumfaciens in soil and bean crop debris. Journal of Plant Pathology 94, 331-337.

Soares RM, Maringoni AC & Lima GPP (2004) [Inefficiency of acibenzolar-S-methyl in induction of resistance against bacterial wilt in common bean]. Fitopatologia Brasileira 29, 373-377 (in Portuguese). 

Soares RM, Fantinato GGP, Darben LM, Marcelino-Guimarães FC, Seixas CDS & Carneiro GES (2013) First report of Curtobacterium flaccumfaciens pv. flaccumfaciens on soybean in Brazil. Tropical Plant Pathology 38, 452–454.

Sonmezalp S (1966) [Two important bacterial diseases on beans (Corynebacterium flaccumfaciens and Xanthomonas phaseoli)]. Bitki Koruma Bulteni 6, 103–110 (in Turkish).

Tegli S, Surico G & Esposito A (1998) Studi sulla diagnosi di Curtobacterium flaccumfaciens pv. flaccumfaciens nei semi di fagiolo. Notiziario sulla Protezione delle Piante 9, 63–71.

Tegli S, Sereni A & Surico G (2002) PCR-based assay for the detection of Curtobacterium flaccumfaciens pv. flaccumfaciens in bean seeds. Letters in Applied Microbiology 35, 331–337.

Tegli S, Biancalani C, Ignatov AN & Osdaghi EA (2020) Powerful LAMP weapon against the threat of the quarantine plant pathogen Curtobacterium flaccumfaciens pv. flaccumfaciens. Microorganisms 8, 1705. https://doi.org/10.3390/microorganisms8111705

Tripepi RR & George MW (1991) Identification of bacteria infecting seedlings of mung bean used in rooting bioassays. Journal of the American Society for Horticultural Science 116, 80-84.

Urrea CA & Harveson RM (2014) Identification of sources of bacterial wilt resistance in common bean (Phaseolus vulgaris). Plant Disease 98, 973-976. https://doi.org/10.1094/PDIS-04-13-0391-RE

Wood BA & Easdown WJ (1990) A new bacterial disease of mungbean and cowpea for Australia. Australasian Plant Pathology 19, 16–21.

Yerkes WD & Crispin AM (1956) Bean diseases of importance in Mexico in 1955. Plant Disease Reporter 40, 222-223.

Zaumeyer WJ (1932) Comparative pathological history of three bacterial diseases of bean. Journal of Agricultural Research 44, 605-632.

Zaumeyer WJ & Thomas HR (1957) A monographic study of bean diseases and methods for their control. Technical Bulletin, USDA No. 865, 255 pp.

CABI and EFSA resources used when preparing this datasheet

CABI Datasheet on Curtobacterium flaccumfaciens pv. flaccumfaciens (CABI (2020) Curtobacterium flaccumfaciens pv. flaccumfaciens. https://www.cabi.org/isc/datasheet/15333

EFSA Pest categorisation of Curtobacterium flaccumfaciens pv. flaccumfaciens (EFSA (2018) EFSA Panel on Plant Health (M. Jeger et al.):   Pest categorisation of Curtobacterium flaccumfaciens pv. flaccumfaciens.EFSA Journal 2018 16, 5299, 22 pp. https://doi.org/10.2903/j.efsa.2018.5299

This datasheet was extensively revised in 2021 by Dr Jaap D. Janse, independent consultant, bacteriologist. His valuable contribution is gratefully acknowledged.

EPPO (2024) Curtobacterium flaccumfaciens pv. flaccumfaciens. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-12-21)

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 2021. 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 flaccumfaciens. Bulletin OEPP/EPPO Bulletin 12(1), 1-4. https://doi.org/10.1111/j.1365-2338.1982.tb01948.x