Xanthomonas citri pv. fuscans(XANTFF)
EPPO Datasheet: Xanthomonas citri pv. fuscans
This datasheet covers the two bacterial species and pathovars that are associated with the common bacterial blight of bean: Xanthomonas phaseoli pv. phaseoli (XANTPH) and X. citri pv. fuscans (XANTFF).
IDENTITY
Authority: (Schaad et al.) Constantin et al.
Taxonomic position: Bacteria: Proteobacteria: Gammaproteobacteria: Lysobacterales: Lysobacteraceae
Other scientific names: Pseudomonas phaseoli var. fuscans (Burkholder) Stapp, Xanthomonas fuscans subsp. fuscans Schaad et al., Xanthomonas phaseoli var. fuscans (Burkholder) Starr & Burkholder
Common names in English: bacterial blight of bean, bacterial leaf pustule of bean, common blight of bean, fuscous blight of bean
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Notes on taxonomy and nomenclature
The causal agent of common bacterial blight of bean was first identified in 1897 as Bacillus phaseoli (Smith, 1897). Variant strains isolated in 1924 by Burkholder produced a brown pigment on tyrosine-containing medium and were thus described as fuscous strains (Burkholder, 1930). Different revisions of the taxonomy led the fuscous and non-fuscous strains to be grouped under the names Xanthomonas phaseoli (Corey & Starr, 1957), then X. campestris pv. phaseoli (Dye et al., 1980), and then X. axonopodis pv. phaseoli (Vauterin et al., 1995). Molecular divergence between fuscous and non-fuscous strains led to the proposition of a taxonomic distinction between the two, leading to the fuscous strains being renamed as X. fuscans subsp. fuscans, while the non-fuscous strains conserved the name X. axonopodis pv. phaseoli (Schaad et al., 2005). Later on, heterogeneity within X. axonopodis pv. phaseoli was revealed based on AFLP analysis, leading to the description of three non-fuscous genetic lineages: GL1, GL2, and GL3 (Alavi et al., 2008). Lineages GL2 and GL3 were, however, genetically distant from GL1 and grouped with the fuscous strains from X. fuscans subsp. fuscans. The four lineages of bacterial pathogens responsible for common bacterial blight of bean are currently distributed across two species within the Xanthomonas genus. Lineage GL1 corresponds to X. phaseoli pv. phaseoli, while the other three lineages (GL2, GL3, and fuscans) group under the name X. citri pv. fuscans (Constantin et al., 2016).
EU Categorization: RNQP (Annex IV)
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EPPO Code: XANTFF
HOSTS 2023-01-25
Besides common bean (Phaseolus vulgaris), which is the main host of X. phaseoli pv. phaseoli and X. citri pv. fuscans, natural infections have been reported on diverse other legume species (see host list, Bradbury, 1986; Gilbertson et al., 1992). Additional hosts were reported after artificial inoculation. X. phaseoli pv. phaseoli was also reported from asymptomatic Digitaria scalarum and Senna hirsuta (Opio et al., 1996).
Host list: Phaseolus vulgarisGEOGRAPHICAL DISTRIBUTION 2023-01-25
Common bacterial blight of bean is widely distributed over 100 countries across the five inhabited continents. The disease was reported in most regions where common bean is cultivated except in dry tropical areas. Although one can hypothesize that the bacteria originated from the same centre of diversity as their wild host P. vulgaris (from Mexico to Northern Argentina), the native range of the disease is unknown. This is due in part to the lack of geographic structuring of the strains, which may result from continuous movements of bacteria between regions through the global seed market (Mahuku et al., 2006). Because most commonly used detection methods do not differentiate between X. phaseoli pv. phaseoli and X. citri pv. fuscans (Grimault et al., 2014), it is still difficult to assess if the disease presence in a country is due to one species, the other or both.
EPPO Region: Belgium, Bulgaria, Italy (mainland), Spain (mainland), TürkiyeAfrica: Ethiopia, Kenya, Lesotho, Malawi, South Africa, Tanzania, Uganda
Asia: China (Beijing, Hebei, Heilongjiang, Neimenggu, Shanxi), India (Himachal Pradesh), Iran
North America: Canada (Alberta, Manitoba, Ontario), Mexico, United States of America (Michigan, Nebraska)
Central America and Caribbean: Guatemala, Puerto Rico
South America: Brazil (Distrito Federal, Goias, Mato Grosso, Minas Gerais, Parana, Rio Grande do Sul, Sao Paulo), Colombia
BIOLOGY 2023-01-25
The main source of inoculum is infected seed. Bacteria can reside on both sides of the seed coat and on the surface of the embryo (Darrasse et al., 2018; Zaumeyer, 1930), allowing overwintering and up to 30 years survival (Saettler, 1989). One seed in a lot of 10 000 to 30 000 is sufficient to cause a disease outbreak (Darrasse et al., 2007; Opio et al., 1993; Sutton & Wallen, 1970; Zaumeyer & Thomas, 1957). In tropical and subtropical areas, survival on weeds and crop residues represents an important source for bacterial dissemination (Fininsa & Tefera, 2001; Fininsa & Yuen, 2002; Santana, 1991). Epiphytic life is possible on various alternative hosts and weeds (Angeles-Ramos et al., 1991; Cafati & Saettler, 1980; Gent et al., 2005; Karavina et al., 2011).
Primary infection usually starts with an epiphytic phase facilitated by aggregation in biofilms where bacterial populations grow and stabilize (Jacques et al., 2005; Weller & Saettler, 1980). After growing on the leaf surface, bacteria enter the host tissues through openings such as stomata, hydathodes, or wounds (Rudolph, 1993; Zaumeyer, 1930). Within the host tissues, bacteria multiply exponentially and may express their pathogenicity when inoculated at ~106 bacterial cells per cm2 or above (Weller & Saettler, 1980). Bacterial progression leads to colonization of the vascular tissues, which can lead to plant wilting in the most severe cases (Vidaver, 1993). In temperate areas, colonization of the plant is often asymptomatic but can still lead to efficient vertical transmission of the bacteria (Darrasse et al., 2007; Weller & Saettler, 1980). Disease spread, incidence and severity are favored under warm temperatures (28-32°C) and above 80% relative humidity (Weller & Saettler, 1980).
DETECTION AND IDENTIFICATION 2023-01-25
Symptoms
All aerial parts of bean plants (seedling, leaf, stem, pod, and seed) can present symptoms caused by X. phaseoli pv. phaseoli or X. citri pv. fuscans (Gilbertson et al., 1992; Zaumeyer, 1930). Symptoms on pods and/or leaves are very similar to those caused by Pseudomonas savastanoi pv. phaseolicola, the causative agent of halo blight, and it is seldom possible from visual examination to be certain which of these pathogens is present.
On leaves, symptoms appear as water-soaked spots usually starting from hydathodes and evolving into dry and brown necrotic lesions surrounded by a narrow yellow halo (Chupp & Sherf, 1960). These spots may merge, resulting in a burnt appearance, with possible defoliation and death of the plant. In case of systemic infection, a reddish-brown discoloration of the veins with water-soaking of adjoining interveinal areas may be observed. Infected stems present reddish longitudinal streaks.
On pods, symptoms appear as water-soaked spots, later evolving into dark red-brown lesions, slightly depressed circular spots, and possible bacterial ooze. Shrinking and death of pods may occur in the case of severe infection.
On seeds, symptoms appear as butter yellow spots that turn brown and are localized according to the infection pathway: on the hilum area in case of vascular transmission, at the micropyle in case of floral infection, and on the entire surface of the seed coat in case of infection by contact (Darrasse et al., 2010; Maude, 1997). In severe cases, the seed may be shriveled, affecting germination rate and vigour (Darrasse et al., 2018).
When grown from infected seed, seedlings are usually asymptomatic if infected with relatively low population numbers (Darrasse et al., 2007). In more severe infections, seedlings can present water-soaked symptoms on the stem, cotyledons and/or primary leaves (Gilbertson et al., 1992; Zaumeyer & Thomas, 1957). Angular, water-soaked areas frequently occur on the opposite sides of the primary leaves, indicating that the initial infection occurred while they were still folded together (Zaumeyer, 1930). Lesions on the stems of young seedlings begin as small water-soaked spots that gradually enlarge and sometimes become sunken. Plants often exhibit a characteristic wilting during the heat of the day, with recovery of turgidity at night (Zaumeyer, 1930). In some cases, seedlings may present injured or entirely destroyed growing tips (Gilbertson et al., 1992; Zaumeyer & Thomas, 1957). If these plants do not die, buds may arise in the axils of the cotyledons and produce dwarfed plants with few pods.
Morphology
X. phaseoli pv. phaseoli and X. citri pv. fuscans are motile, aerobic, Gram-negative rod-shaped bacteria of 0.4-0.9 x 0.6-2.6 µm, with a single polar flagellum. Agar colonies are convex, yellow and wet-shining. A brown, diffusible pigment is produced by strains from the fuscans lineage when grown on tyrosine-containing media.
Detection and inspection methods
Detection on seeds include isolation of the bacterium followed by in planta pathogenicity assays and/or molecular detection by PCR, as validated by the International Seed Testing Association (Audy et al., 1994; Grimault et al., 2014). Commercial ELISA kits are also available, as well as LAMP-PCR primers (de Paiva et al., 2020).
PATHWAYS FOR MOVEMENT 2023-01-25
Sources of primary inoculum are infected seeds, infected weeds or volunteers. The bacteria further spread naturally over relatively short distances within or between fields. The only means of long-distance dispersal is by human transport of infected bean seed (Zaumeyer & Thomas, 1957). Secondary spread in the field mainly occurs by direct contact between infected plants, wind-blown rain or splashing. Dissemination of bacteria can also be caused by transportation via farm workers, or agricultural equipment (Belete & Bastas, 2017; Saettler, 1991). The role of bean-feeding insects as vectors is still understudied, but has been reported for a long time (Sackett, 1905; Zaumeyer & Thomas, 1957). Potential insect vectors include Chalcodermus ebeninus, Empoasca sp., Nezara viridula, Cerotoma ruficornis, and Diaprepes abbreviata (Kaiser & Vakili, 1978).
PEST SIGNIFICANCE 2023-01-25
Economic impact
Common bacterial blight is a major disease impacting common bean production (Broughton et al., 2003). Yield losses up to 45% were reported in susceptible genotypes (Saettler, 1989; Wallen & Jackson, 1975; Yoshii et al., 1975). Common bacterial blight agents directly reduce the area of photosynthetic tissues impacting yield of pods and seeds. Symptomatic edible fresh pods and edible seeds become unsaleable. Additional economic losses are due to the time and costs involved in controlling the disease. Common bacterial blight is a major threat for seed quality, as the bacterium is seed-transmitted. Infected seed lots, even in the absence of symptoms, cannot be sold in many countries, in particular where the disease does not occur-or has a limited distribution.
Control
A cornerstone of common bacterial blight management is pathogen detection on seed lots and regulation (see “Phytosanitary measures”). The most efficient management strategy is to use pathogen-free seeds, by producing seeds in specified areas either free of the bacteria (de Boisgrollier, 1993) or whose climatic conditions are non- conducive for the disease (Gilbertson et al., 1992) and checking the absence of the pathogens. Cultural practices are essential to control the disease. If watering is necessary, furrow irrigation should be used rather than overhead irrigation, which mimics rainfall and promotes secondary spread of the bacteria (Akhavan et al., 2013). Burial of residues is an effective way to reduce the survival of the bacteria (Chávez & Granada, 1988; Wimalajeewa & Nancarrow, 1980). Regular cleaning of harvesting equipment and seed containers is a means to limit primary infection, as bacteria can survive in dust or dirt on contaminated equipment (Belete & Bastas, 2017). Likewise, it is recommended to eliminate weeds, infected beans, and other potential hosts (Gilbertson et al., 1990; Saettler et al., 1986). Epidemics can effectively be reduced through employing long crop-rotations of 3 years or more to limit the risk of contamination by pathogens surviving on alternate hosts and volunteers (Schwartz et al., 2005). Resistant bean varieties have been developed for the American market (Osorno et al., 2016, 2020; Urrea et al., 2019; Viteri et al., 2014). However, breeding resistance to common bacterial blight is complex as it has variable heritability and level of expression depending on the environment, the genetic background, or the epidemic pressure (Miklas et al., 2006; Singh & Schwartz, 2010). In addition, different genetic systems appear to control resistance in pods and leaves, and resistance may not be effective against the high diversity of pathogenic strains responsible for common bacterial blight (Aggour et al., 1989; Duncan et al., 2011).
Phytosanitary risk
Common bean is widely cropped throughout the EPPO region, and the major threat posed by common bacterial blight concerns seed quality, impacting both the seed industry and edible seed production. Depending on weather conditions and the level of seed inoculum management, the risk in terms of yield and quality losses is moderate to high. EFSA (2014) considered that the climatic conditions are widely favourable for the disease development in Europe, except in the northern EU countries and that the impact of the disease is limited in the EU due to the existing regulations against these pathogens.
PHYTOSANITARY MEASURES 2023-01-25
As contaminated seeds are the main dispersal pathway for X. phaseoli pv. phaseoli and X. citri pv. fuscans, phytosanitary (quarantine) measures can be implemented to reduce the risk of long-distance dissemination of these pathogens. It can be recommended that consignments of bean seeds should have been produced from pest-free areas, or from pest-free places of production. Seed material imported from areas where the disease is known to occur should be certified for disease freedom via field inspections and laboratory testing.
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ACKNOWLEDGEMENTS 2023-01-25
This datasheet was extensively revised in 2023 by Nicolas WG Chen and Marie-Agnès Jacques, IRHS, FR. Their valuable contribution is gratefully acknowledged.
How to cite this datasheet?
Datasheet history 2023-01-25
This datasheet was first published in the EPPO Bulletin in 1978 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2023. 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 (1st and 2nd edition). CABI, Wallingford (GB).
EPPO (1978) EPPO Data Sheet on Quarantine Organisms no 61: Xanthomonas phaseoli subsp. fuscans. EPPO Bulletin 13(1), 58-61. https://doi.org/10.1111/j.1365-2338.1978.tb02771.x