This datasheet covers the four bacterial species and pathovars that are associated with the bacterial spot of tomato and pepper: Xanthomonas euvesicatoria pv. euvesicatoria, Xanthomonas euvesicatoria pv. perforans, Xanthomonas hortorum pv. gardneri, Xanthomonas vesicatoria.

Preferred name: Xanthomonas euvesicatoria pv. perforans
Authority: (Jones, Lacy, Bouzar, Stall & Schaad) Constantin, Cleenwerck, Maes, Baeyen, Van Malderghem, De Vos, Cottyn
Taxonomic position: Bacteria: Proteobacteria: Gammaproteobacteria: Lysobacterales: Lysobacteraceae
Other scientific names: Xanthomonas perforans Jones, Lacy, Bouzar, Stall & Schaad
Common names in English: bacterial leaf spot of pepper, bacterial scab of tomato, bacterial spot of pepper, bacterial spot of tomato, black spot of tomato, leaf spot of tomato, stem canker 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: XANTPF

The main hosts of bacterial spot xanthomonads are tomato (Solanum lycopersicum) and pepper (Capsicum spp.). X. euvesicatoria pv. euvesicatoria and X. hortorum pv. gardneri are reported as pathogens for both tomato and pepper. Meanwhile, X. vesicatoria primarily infects tomato and, until recently, X. euvesicatoria pv. perforans strains had only been isolated from tomato (Timilsina et al., 2015). However, over in recent years X. euvesicatoria pv. perforans has been isolated from pepper fields in Florida and Alabama (USA) (Potnis et al., 2015; Newberry et al., 2019).

Three pathotypes of strains have been distinguished among the bacterial spot causative agents: those exclusively infecting tomato (T races), those exclusively affecting pepper (P races), and those infecting both tomato and pepper. Several races have been identified based on the hypersensitive reaction (HR) triggered by effector proteins in Xanthomonas strains delivered via the type III secretion system into host cells and recognition by specific resistance proteins in tomato or pepper (Stall et al., 2009). Currently 11 pepper races and five tomato races have been documented (Bouzar et al., 1994; Stall et al., 2009; Adhikari et al., 2020; Jibrin et al., 2022). Pathogenic races are determined by the presence or absence of HR in the susceptible C. annuum cultivar Early Calwonder (ECW), its near-isogenic lines and Capsicum pubescens PI235047, or in different S. lycopersicum genetic lines. Nevertheless, future studies may reveal unknown races and potential novel dynamics in pathogen-host interaction.

A range of solanaceous and non-solanaceous plants, mainly weeds, have also been recorded as incidental hosts (Osdaghi et al., 2021).

Host list: Capsicum annuum, Capsicum baccatum, Capsicum chinense, Capsicum pubescens, Eucalyptus pellita, Ipomoea aquatica, Nicandra physalodes, Solanum americanum, Solanum lycopersicum, Tubocapsicum anomalum

Bacterial spot causative agents occur widely in tomato and pepper-growing areas, especially in tropical and subtropical regions with moderate or higher rainfall. The disease has primarily been observed in field crops but can also occur in greenhouses. The environmental conditions in Southern Europe are particularly favorable for disease expression in the field, given that the optimal growth temperature for xanthomonads is between 25 and 30°C (Holt, 1994).

The classification of the four lineages of bacterial spot xanthomonads has experienced several revisions due to the intricate taxonomic relationships within this group (see Notes on taxonomy and nomenclature). This has led to uncertainties regarding the specific species present in various geographical areas. As reported by Timilsina et al. (2015), shifts in the species composition of bacterial spot pathogens populations have occurred due to the global spread of dominant genotypes, and recombination between species has generated genetic diversity in these populations. Therefore, the global distribution and genetic diversity of bacterial spot xanthomonads are poorly understood. Strains belonging to X. euvesicatoria pv. euvesicatoria and X. vesicatoria were historically considered the dominant bacterial lineages with a worldwide distribution (Jones et al., 2004b). However, more recently, X. euvesicatoria pv. perforans and X. hortorum pv. gardneri were increasingly isolated in North and South America, the Middle East, East Africa, and regions bordering the Indian Ocean (Vancheva et al., 2021). Dramatic changes in the dominant lineages and population structure of bacterial spot in different local areas have been documented over the past few decades. For example, prior to 1991, X. euvesicatoria pv. euvesicatoria was the only species isolated from tomato in Florida (USA), while this taxon has been entirely replaced by X. euvesicatoria pv. perforans on this host since then (Klein-Gordon et al., 2021). Similar changes are also reported in Taiwan (Burlakoti et al., 2018).

The map includes only records where the Xanthomonas species has been identified. Articles mentioning 'Xanthomonas spp.’ or 'bacterial spot of tomato’ without mentioning the species are not included in the database. A map showing the records of Xanthomonas axonopodis pv. vesicatoria is available as an archive in EPPO Global Database.

EPPO Region: Italy (Sicilia), Türkiye
Africa: Comoros, Ethiopia, Mauritius, Seychelles, South Africa, Tanzania
Asia: China (Fujian), Indonesia (Sumatra), Iran, Korea, Republic, Taiwan, Thailand
North America: Canada (Ontario), Mexico, United States of America (Alabama, Florida, Georgia, Illinois, Indiana, Louisiana, Michigan, Mississippi, North Carolina, Ohio)
South America: Brazil (Bahia, Distrito Federal, Goias, Minas Gerais, Santa Catarina, Sao Paulo)
Oceania: Australia (Queensland)

The primary source of inoculum for bacterial spot xanthomonads are infected seeds and planting material (Potnis et al., 2015). Bacteria can survive from one season to another, mainly on tomato and pepper seeds, for at least 10 years (Bashan et al., 1982b). A positive correlation was observed between the inoculum concentration of the bacterium on pepper blossoms and the percentage of infested seeds (Dutta et al., 2013). These pathogens can also survive in infected debris and the soil to some extent, possibly in the rhizosphere of non-host plants (Bashan et al., 1982a). Diverse solanaceous and non-solanaceous weeds may be alternative hosts (Osdaghi et al., 2021).

Once introduced in an area, the spread of bacteria is primarily by rain-splash or overhead irrigation, with the handling of young plants also playing an important role (Goode & Sasser, 1980). Viable bacteria have been detected in aerosols over commercial fields, indicating a putative aerial dispersal (McInnes et al., 1988; Bernal & Berger, 1996 ). Leaves are infected through stomata, while fruits are infected through small wounds, such as abrasions, and insect punctures. Young leaves and fruits are more sensitive to infection and the bacteria can multiply epiphytically on young plants in the absence of symptoms. Thinning of directly seeded tomato seedlings (practice of selectively removing weaker seedlings to improve the health and productivity of the plants) is reported to promote spread of the disease, and it is recommended to thin in the afternoon, when plants are dry, and to use prophylactic hand washes (Pohronezny et al., 1990). The disease is favored by heavy rainfall, high humidity (Diab et al., 1982) and temperatures between 25°C and 30°C (EFSA, 2014).

Symptoms

All bacterial spot xanthomonads can induce a wide variety of symptoms on their host plants, including angular lesions that later become brown and necrotic on the leaves, fruits, petioles and stems. Some symptoms may be mistaken for those caused by other organisms (see below). Pathogen aggressiveness and the development of symptoms often depend on the host-pathogen combination, with X. euvesicatoria pv. euvesicatoria appearing to be significantly more aggressive on bell pepper than on tomato (Ignjatov et al., 2010).

Fruits of tomato show superficial corky spots or scabs, with water-soaked margins, oval or irregular in shape and with a diameter of around 2-10 mm. The ‘flecks’ caused by Pseudomonas syringae pv. tomato are distinctly smaller (diameter <1 mm), black, circular and elevated. Differences are also observed with symptoms of Clavibacter michiganensis on fruits, consisting of brown spots, slightly raised, and surrounded by a white halo (a distinctive 'bird's eye' appearance). Scabbing of fruit (but without water-soaking) may also be a symptom of the phytotoxicity of plant protection products. Bacterial spot xanthomonads fruit lesions in pepper are scab-like, raised and rapidly necrotising. Lesions on tomato or pepper leaves appear as irregular water-soaked areas, initially green and later becoming brown and necrotic. Speck lesions caused by P. syringae pv. tomato look similar in a first stage, but are surrounded by a more distinct yellow halo; lesions are often in streaks and the yellow haloes run together to give large chlorotic areas (Goode & Sasser, 1980). Severe infections in pepper cause defoliation, favoring sunscald of the fruits on hot and sunny days.

Bacterial spot xanthomonads can cause canker-like splits in stems, but their presence alone is not diagnostic as similar symptoms may also be caused by P. syringae pv. tomato, C. michiganensis and Alternaria solani. Pith necrosis has been associated with the presence of X. euvesicatoria pv. perforans, but this symptom could be confused with those of Pseudomonas mediterranea and Pseudomonas corrugata (Aiello et al., 2013).

Morphology

Xanthomonads causing bacterial spot of tomato and pepper are aerobic, mobile, Gram-negative rods, occurring singly or in pairs, 0.6 x 1.0-1.5 µm, with a single polar flagellum. Like other species of the genus, they produce characteristic yellow pigments (xanthomonadins). On general media, such as yeast-glucose-calcium carbonate agar (YGCA) or yeast peptone glucose agar (YPGA), colonies are mucoid-fluidal, convex, and yellow with entire edges. Unlike P. syringae pv. tomato, bacterial spot xanthomonads are non-fluorescent on King's B medium.

Detection and inspection methods

Symptoms of bacterial spot xanthomonads can be confused with those caused by other pathogens. Confirmation through diagnostic analysis is necessary when the presence of spot-causing bacteria is suspected. The EPPO Diagnostic protocol Standard PM 7/110 (2) (EPPO, 2023) offers comprehensive guidelines for the preliminary screening of plant material or seeds. The Standard includes isolation and molecular tests and, if required, confirmatory pathogenicity tests in susceptible cultivars of tomato and pepper plants. The EPPO Standard recommends multiplex real-time PCR (Strayer et al., 2016) and real-time PCR tests for specific identification of Xanthomonas species causing bacterial spot disease (Baldwin et al., 2023). Serological methods are not recommended in the Standard; few antibodies are commercially available for immunofluorescence and ELISA, and no validation data could be retrieved.

The International Seed Health Initiative (ISHI) advises using a minimum of 10 000 tomato or pepper seeds for seed detection purposes to ensure effective screening (ISF, 2017). This approach, with subsamples capped at 10 000 seeds, aims to identify contamination levels as low as 0.03% with a 95% confidence interval. In instances where there is a high likelihood of saprophytic bacteria overshadowing the presence of Xanthomonas spp., opting for smaller subsample sizes, such as five sets of 2 000 seeds each, is recommended.

A procedure by which consignments of tomato seeds should be subjected to phytosanitary import inspection, including sampling and identification, is provided in EPPO Standard PM 3/80 (2) (EPPO, 2021).

Trade of infected seeds and plants for planting (transplants) are associated with long-distance dissemination of Xanthomonas spp. which are responsible of causing bacterial spot. Bacteria may escape from infected plants as exudates, and short-distance dispersal is then facilitated by splashing water, such as irrigation or rain. This becomes particularly concerning during transplant in greenhouse production when several thousands of transplants are growing closely together, as well as in the field, especially in the case of sprinkler irrigation. Short-distance-spread of bacteria is also possible through contaminated tools (EFSA, 2014).

Economic impact

Bacterial spot xanthomonads are widespread and are considered significant pathogens of tomato and pepper in field-grown crops in warm-temperate and tropical countries, especially under overhead irrigation. They can also occur in greenhouses. Fruit yield losses are most substantial when infection occurs early, as observed in tomato in USA, and pepper in Israel (Dougherty, 1978; Bashan et al., 1985). Damage to the leaves tends to expose fruits to the sun, increasing the risk of sunscald. Although fruit lesions are often only superficial, they result in loss of marketability.

Bacterial spot has been recognized as a severe disease accompanied by significant damages in production in countries of the EPPO region, such as Serbia (Ignjatov et al., 2010; Vlajić et al., 2017), Bulgaria and the Republic of North Macedonia (Kizheva et al., 2011), or Türkiye (Aysan & Sahin, 2003). Although no recent data are available on economic losses caused by these pathogens in the European Union (EU), infections resulting in up to 30 % losses have been reported (EFSA, 2014). Yield losses of up to 66% have been reported in the USA (Pohronezny & Volin, 1983). Tomato yield loss estimated to be 7 413 USD per ha have been reported in Florida (USA) (Vallad et al., 2013). Furthermore, outbreaks in 2009-2010 in 2000 ha of processing tomatoes in Northwest Ohio and Southeast Michigan resulted in total losses of up to 7.8 USD million (Ma et al., 2011).

Control

Due to the seedborne nature of bacterial spot xanthomonads, management of the disease has been a major challenge since its original description. As no effective methods or chemical control agents are available for infected crops, disease control requires the adoption of integrated management measures, primarily focused on prevention and exclusion. Pathogen-free seeds and transplants are crucial to avoid the introduction and spread of bacteria. Tomato seed extraction from fruits using appropriate fermentative or acid treatments to reduce xanthomonads population is required in the EU (Anonymous, 2019). For both tomato and pepper seeds, hot water soak, dry heat therapy or selected chemicals have been recommended (EFSA, 2014).

Once infection occurs, control of disease in the field is particularly difficult. Cultural practices, such as four-year crop rotations, are recommended. Avoiding the handling of wet plant material and minimizing free moisture on foliage helps prevent disease development and spread. The application of protective chemicals or biological treatments is advised to reduce the severity and spread during transplant production.

The most common approach for managing bacterial spot pathogens is the preventive application of copper-based bactericides, but their success is limited as bacterial resistance to such chemicals has appeared worldwide (Lamichhane et al., 2018). Additionally, in the EU a new legislation limits the use of copper compounds (Anonymous, 2018). Several biological control approaches have been studied, including bacteriophages (Jones et al., 2012; Balogh et al., 2018; Gašić et al., 2018; Ríos-Sandoval et al., 2020), plant growth-promoting rhizobacterium (Naue et al., 2014; Liu et al., 2018) and antagonistic bacteria. Integration of biological control agents, such as tailocins (phage-tail-like bacteriocins produced by Pseudomonas fluorescens SF4c (Príncipe et al., 2018) and Bacillus velezensis GF267 (de Paula Kuyat Mates et al., 2019), and SARS inducers (harpin and acibenzolar-S-methyl) enhances the effectiveness of bacterial spot management (Obradovic et al., 2005; Abo-Elyours & El-Hendawy, 2008). The application of bacteriophages alone or in combination with biocontrol agents or copper hydroxide reduces disease incidence.

Efforts have been made to develop tomato and pepper lines with resistance to bacterial spot xanthomonads, and sources of resistance have been identified and incorporated into breeding programs and varieties (Stall et al., 2009). However, the persistence of resistance can change rapidly due to the evolving geographical distribution of the pathogen and the rapid emergence of new pathogenic variants (Potnis et al., 2015).

Phytosanitary risk

Xanthomonas spp. are important bacterial pathogens that affect tomato and pepper production. Environmental conditions in Southern Europe are particularly favorable for bacterial spot expression in the field, as the optimal growth temperature for xanthomonads is between 25°C and 30°C, but the disease also occurs in greenhouses (EFSA, 2014).

Long-distance spread of Xanthomonas spp. causing bacterial spot of tomato and pepper, is commonly related to the movement of infected seeds and planting material (transplants). Once introduced into a production area, such as a cultivation plot or a greenhouse, the pathogens disperse easily, and short-distance dispersal is facilitated by splashing water (from irrigation and rain) or contaminated tools (EFSA, 2014).

As the main means of spread of bacterial spot xanthomonads are with seeds and plants for planting, the use of healthy seed and plantlets are a key phytosanitary measure (Picard et al., 2018).

Currently Xanthomonas euvesicatoria pv. euvesicatoria, Xanthomonas euvesicatoria pv. perforans, Xanthomonas hortorum pv. gardneri and Xanthomonas vesicatoria are classified as regulated non-quarantine pests (RNQP) in many EPPO countries, including those within the EU (Anonymous, 2019), and measures to prevent their presence on seeds and planting material are mandatory. The EU measures are as follows: the presence of these bacteria is not allowed in propagating material of ornamental plants or other plants for planting intended for ornamental purposes, vegetable seeds, and vegetable propagating and planting material other than seeds (threshold level 0%) (Anonymous, 2019 Annex IV, Parts D, F, and I). For tomato seeds, an appropriate extraction method for bacterial elimination is required (there is no indication whether or not pepper seeds should be treated). Tomato and pepper seeds should originate in areas known to be free from these pathogens where no symptoms of bacterial spot have been observed during the complete cycle of vegetation of the plants at site of production. Alternatively, seeds should have been subjected to official testing on a representative sample using appropriate methods and have been found free of the pathogens (Anonymous, 2019 Annex V, Parts C, E, and H).

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This datasheet was extensively revised in 2024 by Ana Palacio-Bielsa (CITA, Centro de Investigación y Tecnología Agroalimentaria de Aragón, Spain / Instituto Agroalimentario de Aragón - IA2 (CITA-Universidad de Zaragoza, Spain), Jaime Cubero (INIA/CSIC, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria/Consejo Superior De Investigaciones Científicas, Spain) and Jerson Garita-Cambronero (ANOVE, Asociación Nacional de Obtentores Vegetales, Spain / ITACyL, Instituto Tecnológico Agrario de Castilla y León, Spain). Their valuable contribution is gratefully acknowledged.

EPPO (2024) Xanthomonas euvesicatoria pv. perforans. 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 1988 and revised in the two editions of 'Quarantine Pests for Europe’ in 1992 and 1997, as well as in 2024. 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 (2^nd edition). CABI, Wallingford (GB).

EPPO (1988) Data sheets on quarantine organisms No. 157, Xanthomonas campestris pv. vesicatoria. EPPO Bulletin 18, 521-526. https://onlinelibrary.wiley.com/doi/epdf/10.1111/j.1365-2338.1988.tb00409.x