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Curtobacterium flaccumfaciens pv. flaccumfaciens
(bacterial wilt of dry beans)

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Datasheet

Curtobacterium flaccumfaciens pv. flaccumfaciens (bacterial wilt of dry beans)

Summary

  • Last modified
  • 10 December 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Curtobacterium flaccumfaciens pv. flaccumfaciens
  • Preferred Common Name
  • bacterial wilt of dry beans
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Actinobacteria [phylum]
  •     Class: Actinobacteria
  •       Subclass: Actinobacteridae
  •         Order: Actinomycetales
  • Summary of Invasiveness
  • Curtobacterium flaccumfaciens pv. flaccumfaciens, the causal agent of bacterial wilt of dry beans, is an economically important pathogen of edible legumes (i.e., common bean, soyabean, mungbean and cowpea) around the world. The d...

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Pictures

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PictureTitleCaptionCopyright
Curtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
TitleSymptoms
CaptionCurtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
Copyright©Dr Ebrahim Osdaghi; University of Tehran; Iran
Curtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
SymptomsCurtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.©Dr Ebrahim Osdaghi; University of Tehran; Iran
Curtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
TitleSymptoms
CaptionCurtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
Copyright©Dr Ebrahim Osdaghi; University of Tehran; Iran
Curtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
SymptomsCurtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.©Dr Ebrahim Osdaghi; University of Tehran; Iran
Curtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
TitleSymptoms
CaptionCurtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
Copyright©Dr Ebrahim Osdaghi; University of Tehran; Iran
Curtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.
SymptomsCurtobacterium flaccumfaciens (bacterial wilt of bean); Symptoms on leaves of bean caused by C. flaccumfaciens in field.©Dr Ebrahim Osdaghi; University of Tehran; Iran
Leaf necrosis in mung bean: spots progressively dry out and become bleached to a tan colour.
TitleSymptoms on mung bean
CaptionLeaf necrosis in mung bean: spots progressively dry out and become bleached to a tan colour.
CopyrightA. Diatloff
Leaf necrosis in mung bean: spots progressively dry out and become bleached to a tan colour.
Symptoms on mung beanLeaf necrosis in mung bean: spots progressively dry out and become bleached to a tan colour.A. Diatloff
Floret blighting in mung bean.
TitleSymptoms on mung bean floret
CaptionFloret blighting in mung bean.
CopyrightA. Diatloff
Floret blighting in mung bean.
Symptoms on mung bean floretFloret blighting in mung bean.A. Diatloff
C. flaccumfaciens pv. flaccumfaciens invading vascular elements, causing blockage of xylem vessel in mung bean.
TitleVascular blockage by bacteria - SEM
CaptionC. flaccumfaciens pv. flaccumfaciens invading vascular elements, causing blockage of xylem vessel in mung bean.
CopyrightA. Diatloff
C. flaccumfaciens pv. flaccumfaciens invading vascular elements, causing blockage of xylem vessel in mung bean.
Vascular blockage by bacteria - SEMC. flaccumfaciens pv. flaccumfaciens invading vascular elements, causing blockage of xylem vessel in mung bean.A. Diatloff

Identity

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Preferred Scientific Name

  • Curtobacterium flaccumfaciens pv. flaccumfaciens (Hedges 1922) Collins & Jones 1983

Preferred Common Name

  • bacterial wilt of dry beans

Other Scientific Names

  • Bacterium flaccumfaciens Hedges 1922
  • Corynebacterium flaccumfaciens pv. flaccumfaciens (Hedges 1922) Dowson 1942
  • Corynebacterium flaccumfaciens subsp. flaccumfaciens (Hedges 1922) Dowson 1942
  • Phytomonas flaccumfaciens (Hedges 1922) Bergey et al. 1923
  • Pseudomonas flaccumfaciens (Hedges 1922) Stevens 1925

International Common Names

  • English: bacterial tan spot; bacterial wilt; bean wilt
  • Spanish: bacteriosis vascular de la judía; marchitez bacteriana de la judía; marchitez bacteriana de la soja
  • French: bactériose vasculaire du haricot; flétrissement bactérien du haricot

Local Common Names

  • Germany: Bakterielle Welke: Bohne

EPPO code

  • CORBFL

Summary of Invasiveness

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Curtobacterium flaccumfaciens pv. flaccumfaciens, the causal agent of bacterial wilt of dry beans, is an economically important pathogen of edible legumes (i.e., common bean, soyabean, mungbean and cowpea) around the world. The disease occurs in many countries with a particular importance in regions characterized by dry and hot summers with extended drought. As a seedborne pathogen, C. flaccumfaciens pv. flaccumfaciens is included in the A2 (high risk) list of quarantine pathogens by the European and Mediterranean Plant Protection Organization (EPPO); hence, it is under strict quarantine control and zero tolerance in the dry bean industry in several countries. Bacterial wilt was first reported on common bean in South Dakota, USA, in 1922 and then spread into South America, Canada, Australia, Europe and more recently to western Asia (Iran) and Africa. Identification of the pathogen can be difficult owing to the presence of five different colony colour variants (i.e., yellow, orange, pink, purple and red) on culture media.

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Actinobacteria [phylum]
  •         Class: Actinobacteria
  •             Subclass: Actinobacteridae
  •                 Order: Actinomycetales
  •                     Suborder: Micrococcineae
  •                         Family: Microbacteriaceae
  •                             Genus: Curtobacterium
  •                                 Species: Curtobacterium flaccumfaciens pv. flaccumfaciens

Notes on Taxonomy and Nomenclature

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Bacterial wilt was first reported by Hedges (1922) on common bean in South Dakota, USA, and the causal agent was named as Bacterium flaccumfaciens (Hedges, 1922, 1926). Subsequently, Bergey et al. (1939) transferred the Gram-positive plant pathogenic bacteria into the genus Phytomonas, and renamed the wilt pathogen as Phytomonas flaccumfaciens. Then, Dowson (1942) transferred the Gram-positive coryneform plant pathogenic bacteria into the genus Corynebacterium (‘club’ bacterium) (Lehmann and Neumann, 1896) and the bacterial wilt pathogen was named as Corynebacterium flaccumfaciens (Hedges, 1922) Dowson 1942.

The taxonomic position of the phytopathogenic Corynebacterium was further clarified by Carlson and Vidaver (1982) and more recently by Collins and Jones (1983). Taxonomic studies using biochemical characteristics, DNA-DNA homology and cell wall composition on plant pathogenic members of Corynebacterium, resulted in the transfer of several species into the newly erected genus Curtobacterium (Carlson and Vidaver, 1982; Collins and Jones, 1983; Komagata and Suzuki, 1986) including Corynebacterium betae, Corynebacterium flaccumfaciens, Corynebacterium oortii and Corynebacterium poinsettiae. Subsequently, all the latter species were reclassified as pathovars of Curtobacterium flaccumfaciens (Collins and Jones, 1983, 1984). Hence, the bacterial wilt pathogen was classified as C. flaccumfaciens pv. flaccumfaciens. Recent investigations using data obtained by multilocus sequence analysis (MLSA) of five housekeeping genes, i.e., atpD, gyrB, ppk, recA and rpoB revealed that the pathovars of C. flaccumfaciens should be reclassified as stand-alone species (Osdaghi et al., 2018a, 2018b, 2020b; Gonçalves et al., 2019).

The term Curtobacterium is derived from a Latin word ‘cutus’ or ‘shortened’ to describe the short and rod-shaped nature of the bacterial cells (Yamada and Komagata, 1972) while the specific epithet ‘flaccumfaciens’ is a two-part term (flaccum+faciens) derived from the Latin words 'flaccus' meaning ‘flabby or flaccid’ and ‘faciens’ meaning ‘making’. Hence, the name of the pathogen describes the cell morphology and symptomology of the bacterium as ‘wilt-inducing, short, rod-shaped bacterium’ (Hedges, 1922; Harveson et al., 2015; Chen et al., 2020).

Description

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For several decades since the first description of the pathogen, C. flaccumfaciens pv. flaccumfaciens was known for possessing only yellow-pigmented colonies on culture media (Hedges, 1922). However, four additional colony variants of the pathogen have been described in different geographic areas. In the late 1950s, an orange-pigmented variant of was isolated from discoloured common bean seeds in Nebraska, USA, and named as Corynebacterium flaccumfaciens var. aurantiacum (Schuster and Christiansen, 1957). In 1968, another variant was isolated from white-seeded common bean in western Nebraska inducing a purple discoloration on seed coats, and the causal agent was described as Corynebacterium flaccumfaciens var. violaceum (Schuster and Sayre, 1967; Schuster et al., 1968). Two additional novel colour variants of C. flaccumfaciens pv. flaccumfaciens were identified from two geographically distinct areas. A pink-pigmented variant was isolated from orange-stained common bean seeds in western Nebraska, USA, in 2007 (Harveson and Vidaver, 2008) and in 2014, a red-pigmented variant was isolated in central Iran (Markazi province) from white-seeded common bean seed lots possessing deep orange discoloration (Osdaghi et al., 2016). Hence, C. flaccumfaciens pv. flaccumfaciens is well known for its multi-coloured colonies on culture media. The pathogen causes bacterial wilt and tan spot disease on edible dry beans of the family Fabaceae including common bean (Phaseolus vulgaris), cowpea (Vigna unguiculata), mungbean (Vigna radiata), soyabean (Glycine max), as well as a number of weed species.

C. flaccumfaciens pv. flaccumfaciens is an aerobic, Gram-positive, non-acid-fast, rod-shaped bacterium, occurring singly or paired, coryneform, 0.3-0.5 x 0.6-3 µm. It is non-capsulated, motile with 1-3 lateral or polar flagella. On nutrient broth yeast medium, slow growing, small (1-4 mm), flat colonies appear after 2-3 days. Colonies on yeast-extract peptone glucose agar (YPGA) medium are circular, smooth, flat or slightly convex, opaque and slightly viscid, with an entire margin. Colony growth on nutrient broth yeast extract (NBY) medium is slow and fluidal. The colony colour varies among yellow, orange, pink and red pigmentation (Collins and Jones, 1983; Harveson et al., 2015; Osdaghi and Lak 2015a, b; Osdaghi et al., 2016). Characteristic biochemical tests: acid but no gas is produced from glucose, maltose, lactose, sucrose, galactose, fructose, rhamnose, melibiose, mannose and glycerol; levan negative; catalase positive; gelatin is liquefied slowly (see Carlson and Vidaver, 1982). Apart from colony pigmentation, variants of C. flaccumfaciens pv. flaccumfaciens are indistinguishable based on biochemical and physiological characteristics (Osdaghi et al., 2016). Maximum temperature for growth is 37°C, while optimum growth occurs at 27-32°C. C. flaccumfaciens pv. flaccumfaciens cells are positive in the utilization of acetate, citric acid, fumarate, fumaric acid, gluconic acid, lactic acid and malic acid, and negative for the utilization of glyoxylic acid, propionate and α-Ketoglutaric acid (Evtushenko and Takeuchi, 2006). Furthermore, the pathogen is positive for H2S production, hydrolysis of aesculin and casein, as well as production of acid from adonitol, L-rhamnose and raffinose. The bacterial cell wall in C. flaccumfaciens pv. flaccumfaciens contains galactose, but lacks glucose and fucose. The G+C content of the pathogen was estimated to be 71.1% (Evtushenko and Takeuchi, 2006; Osdaghi et al., 2017). See also Hayward and Waterston (1965).

Distribution

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Bacterial wilt was first described in South Dakota, USA, in 1922 (Hedges, 1922). In addition to the USA, the disease was reported in Canada and Mexico in 1955 (Patrick, 1955; Yerkes and Crispin, 1956). However, its presence in Mexico has not been confirmed (EPPO/CABI, 1997). The disease was restricted to North America until being observed on mungbean and cowpea plants in Australia in the late 1980s (Wood and Easdown, 1990). The disease has also continued to spread southward into South America, reaching Colombia in 1982 (Torres et al., 1982) and Venezuela in 1990 (EPPO, 2011). Then, Maringoni and Rosa (1997) reported the disease on common bean plants in São Paulo State, Brazil in 1995. Since the beginning of the 21st Century, bacterial wilt has sporadically been reported in some European countries (EPPO, 2011). For instance, the disease was found affecting common bean in south-eastern Spain in 2005 (González et al., 2005). Subsequently, C. flaccumfaciens pv. flaccumfaciens was isolated from soyabean plants in Germany in 2012 (Sammer and Reiher, 2012). The disease was also reported, but not substantiated, in two distinct areas of Russia (EPPO, 2011). The pathogen was not officially reported in Asia until 2013 when a widespread occurrence of the disease was found in Iran in both common bean and cowpea fields from different provinces (Osdaghi et al., 2015a, b). Unofficial occurrences of the pathogen have also been recorded in Albania, Belgium, Bulgaria, France, Greece, Hungary, Romania, Switzerland, Tunisia, Turkey and former Yugoslavia (EPPO, 1994; Ishimaru et al., 2005). Although the pathogen has previously been observed infecting common bean in Africa (i.e., Kenya, Mauritius, South Africa and Tunisia; EPPO, 2011), it was not officially documented from Africa until 2019 when it was reported on soyabean plants in Zambia (Pawlowski and Hartman, 2019).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 17 Feb 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

KenyaAbsent, Eradicated1968
MauritiusPresent
TunisiaPresent, Localized
ZambiaPresent, Localized2019

Asia

IranPresent, Widespread2014
TurkeyPresent, Few occurrences

Europe

AlbaniaAbsent, Unconfirmed presence record(s)
BelgiumAbsent, Formerly present
BulgariaAbsent, Formerly present
FranceAbsent, Invalid presence record(s)
GermanyAbsent, Eradicated
GreeceAbsent, Formerly present
HungaryAbsent, Formerly present1982
ItalyAbsent, Confirmed absent by survey
NetherlandsAbsent, Confirmed absent by survey
PolandAbsent, Formerly present
PortugalAbsent, Confirmed absent by survey
RomaniaAbsent, Formerly present
RussiaPresent, Localized1976
-Russian Far EastPresent, Localized
-Southern RussiaPresent, Localized
SerbiaAbsent, Formerly present
Serbia and MontenegroAbsent, Formerly present
SpainAbsent, Eradicated
SwitzerlandAbsent, Invalid presence record(s)
UkraineAbsent, Formerly present

North America

CanadaPresent, Localized
-AlbertaPresent
-ManitobaPresent
-OntarioPresent
-QuebecPresentOriginal citation: CFIA, personal communication, 2009
-SaskatchewanPresent
MexicoAbsent, Unconfirmed presence record(s)
United StatesPresent, Localized1920
-ColoradoPresent
-ConnecticutPresent
-IdahoPresent
-IowaPresent
-MichiganPresent
-MontanaPresent
-NebraskaPresent
-North DakotaPresent
-OhioPresent
-OregonPresent
-VirginiaPresent
-WisconsinPresent
-WyomingPresent

Oceania

AustraliaPresent, Localized
-New South WalesPresent
-QueenslandPresent
-South AustraliaPresent, Few occurrences
-VictoriaPresent

South America

BrazilPresent, Localized1995
-Distrito FederalPresent
-GoiasPresent
-Mato Grosso do SulPresent
-Minas GeraisPresent
-ParanaPresent
-Santa CatarinaPresent
-Sao PauloPresent1995
ColombiaPresent
VenezuelaPresent

History of Introduction and Spread

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Bacterial wilt was first observed and described in South Dakota, USA, in 1922 (Hedges, 1922). The disease was then reported from Canada and Mexico in 1955 (Patrick, 1955; Yerkes and Crispin, 1956). It was restricted to North America until being observed on mungbean and cowpea plants in Australia in the late 1980s (Wood and Easdown, 1990). The disease has also continued to spread southward into South America, reaching Colombia in 1982 (Torres et al., 1982) and Venezuela in 1990 (EPPO, 2011). Then, Maringoni and Rosa (1997) reported the disease on common bean plants in São Paulo State, Brazil in 1995. Over the past two decades, the disease has sporadically been reported in some European countries, although economic yield losses on dry beans have not been documented (EPPO, 2011). For instance, the disease was found affecting common bean in south-eastern Spain in 2005, while the geographic distribution of the pathogen within Spain was not included in the report (González et al., 2005). Subsequently, C. flaccumfaciens pv. flaccumfaciens was isolated from soyabean plants in Germany in 2012 (Sammer and Reiher, 2012). The disease was also reported, but not substantiated, from two distinct areas of Russia (EPPO, 2011). The pathogen was not officially reported from Asia until 2013 when a widespread occurrence of the disease was found in Iran in both common bean and cowpea fields from different provinces (Osdaghi et al., 2015a, b). Subsequently, a red-pigmented variant of the pathogen was isolated from common bean seeds in central Iran (Osdaghi et al., 2016). Unofficial occurrences of the pathogen have also been recorded in Albania, Belgium, Bulgaria, France, Greece, Hungary, Romania, Switzerland, Tunisia, Turkey and former Yugoslavia (EPPO, 1994; Ishimaru et al., 2005). Although the pathogen has previously been observed infecting common bean in Africa (i.e., Kenya, Mauritius, South Africa and Tunisia; EPPO, 2011), it was not officially documented from Africa until 2019, when it was reported infecting soyabean plants in Zambia (Pawlowski and Hartman, 2019).

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Zambia 2019 Horticulture (pathway cause) No No Pawlowski and Hartman (2019)
Iran 2013 Horticulture (pathway cause) Yes No Osdaghi et al. (2015)
Germany 2012 Horticulture (pathway cause) No No Sammer and Reiher (2012)
Spain 2005 Horticulture (pathway cause) No No González et al. (2005)

Risk of Introduction

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Risk Criteria Category

Economic Importance Moderate to high depending on the region and host crop
Distribution North and South America, Western Asia, Australia
Seedborne Incidence Moderate
Seed Transmitted Yes
Seed Treatment None

Overall Risk Moderate to high

Notes on phytosanitary risk

Although C. flaccumfaciens pv. flaccumfaciens is widespread geographically, imported seed is often subject to declaration of disease status. Exporters of common bean, soyabean and mungbean are often required to certify their exports free from disease to enable entry into other countries. 

Hosts/Species Affected

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Apart from common bean (Phaseolus vulgaris), the natural host list of C. flaccumfaciens pv. flaccumfaciens includes adzuki bean (Vigna angularis), black gram (Vigna mungo), cowpea (Vigna unguiculata), hyacinth bean (Lablab purpureus), lima bean (Phaseolus lunatus), mungbean (Vigna radiata), pea (Pisum sativum), scarlet runner bean (Phaseolus coccineus), soyabean (Glycine max), yardlong bean (Vigna unguiculata subsp. sesquipedalis) and Zornia glabra (Dunleavy, 1983; Chavarro et al., 1985; Ishimaru et al., 2005; Harveson and Vidaver, 2007; Osdaghi, 2014; Osdaghi et al., 2015b).

Growth Stages

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Flowering stage, Fruiting stage, Seedling stage, Vegetative growing stage

Symptoms

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The main symptoms are observed on seedlings emerged from infected seeds at the cotyledon and/or the second trifoliate leaf stage. However, the vegetative growing stage, flowering stage and fruiting stage are also susceptible to the disease (Osdaghi et al., 2020).

Field symptoms of bacterial wilt include a series of interveinal chlorotic and necrotic areas on leaves accompanied by overall plant wilt, leading to plant mortality (Harveson et al., 2011; Harveson et al., 2015). The symptoms first appear as chlorotic areas leading to foliar wilting and necrosis on leaves surrounded by a yellow halo. Subsequent symptoms are leaf wilting during periods of warm and dry weather or periods of moisture stress, due to the pathogen’s presence within the vascular system which interferes with normal water movement from the roots into the foliage (Huang et al., 2009; Harveson et al., 2015).

C. flaccumfaciens pv. flaccumfaciens is primarily a vascular invader that causes vascular browning. In common bean and Zornia spp., plant parts (or the entire plant) wilt and seedling death is common. In soyabean, cowpea and mungbean, leaf chlorosis with spotting and sometimes flower blighting occurs, but there is no wilting. Necrotic spots may appear on the early shield leaves, or, more commonly, on the trifoliate leaves. Spots progressively dry out, become bleached to a tan colour and tear in winds, thus giving the leaf a ragged appearance. Plants infected when young remain chlorotic and stunted. Symptoms are accentuated by moisture stress (see Conde and Diatloff, 1991). Seed discoloration is a common symptom in bacterial wilt disease (Schwartz et al., 2005; Huang et al., 2009). If infected plants survive to produce mature seeds, they are often discoloured as a result of bacterial infection and colonization, particularly in white-seeded cultivars (Hagedorn and Inglis, 1986; Ishimaru et al., 2005; Schwartz et al., 2005).

List of Symptoms/Signs

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SignLife StagesType
Fruit / abnormal shape
Fruit / discoloration
Fruit / lesions: on pods
Fruit / ooze
Leaves / abnormal colours
Leaves / necrotic areas
Leaves / wilting
Roots / cortex with lesions
Seeds / discolorations
Stems / discoloration of bark
Stems / internal discoloration
Stems / internal red necrosis
Stems / stunting or rosetting
Stems / wilt
Whole plant / dwarfing
Whole plant / seedling blight

Biology and Ecology

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C. flaccumfaciens pv. flaccumfaciens is seedborne, with poor survival in soil. It overwinters in plant debris and in weeds. Contaminated seeds provide the initial source of infection, which becomes systemic in the xylem. Mechanical injury of roots by infections from the root-knot nematode Meloidogyne incognita, was shown to provide a mechanism for introducing the pathogen into host plants (Schuster 1959). Bacteria may also enter through wounds on roots and above-ground plant parts and, in contrast to other common bacterial pathogens, infrequently through stomata. Secondary infections occur through wounds following rain and hail storms. Disease is favoured by temperatures above 30°C. Moisture stress induces wilting in common bean and Zornia spp.

Survival of C. flaccumfaciens pv. flaccumfaciens in intact soil under field conditions varies between 34 and 80 days as a function of temperature and moisture (Gonçalves et al., 2018). Infested common bean debris and straw are important in C. flaccumfaciens pv. flaccumfaciens overwintering. Bacteria in infested dry straw on the soil surface survive far better (up to 22 months) than in debris buried 20 cm in the soil (Schuster and Coyne, 1974). Non-leguminous plant species were shown to harbour the pathogen for overwintering (Schuster, 1970; Saettler, 1991). Gonçalves et al. (2017) showed that under Brazilian field conditions, C. flaccumfaciens pv. flaccumfaciens colonizes barley, black oat, oilseed rape, ryegrass, wheat and white oat where these plant species are cultivated during winter in rotation with common bean. It is recommended that common bean cultivation in succession with barley, black oat, oilseed rape, ryegrass, wheat and white oat must be avoided in areas with a history of the disease. The pathogen endophytically colonizes stems of wheat plants inoculated by wounding or spraying techniques (Silva Júnior et al., 2012). Harveson et al. (2015) isolated bean-pathogenic orange and yellow strains of C. flaccumfaciens pv. flaccumfaciens from black chaff-infected wheat plants. Black chaff is a bacterial disease on small grain cereals caused by different pathovars of Xanthomonas translucens. Dry bean-pathogenic strains of C. flaccumfaciens pv. flaccumfaciens were also isolated from symptomless aubergine, pepper and tomato plants in Iran (Osdaghi et al., 2018a).

Climate

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ClimateStatusDescriptionRemark
A - Tropical/Megathermal climate Tolerated Average temp. of coolest month > 18°C, > 1500mm precipitation annually
Af - Tropical rainforest climate Tolerated > 60mm precipitation per month
Am - Tropical monsoon climate Tolerated Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
As - Tropical savanna climate with dry summer Tolerated < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
Aw - Tropical wet and dry savanna climate Tolerated < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
B - Dry (arid and semi-arid) Preferred < 860mm precipitation annually
BS - Steppe climate Tolerated > 430mm and < 860mm annual precipitation
BW - Desert climate Tolerated < 430mm annual precipitation
C - Temperate/Mesothermal climate Preferred Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Tolerated Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)
Cf - Warm temperate climate, wet all year Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Ds - Continental climate with dry summer Tolerated Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)

Air Temperature

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Parameter Lower limit Upper limit
Mean annual temperature (ºC) 37
Mean maximum temperature of hottest month (ºC) 32

Seedborne Aspects

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Incidence

Contaminated seeds are considered to be the main method of introducing bacterial wilt inoculum into areas with no history of the disease (Zaumeyer and Thomas, 1957; Saettler and Perry, 1972). The level of seed transmission was reported to range from six to 70 percent in different assays, however, transmissibility of the pathogen via seeds depends on the host plant and time of infection (Wood and Easdown, 1990; Camara et al., 2009). Up to 10% of commercial mungbean seeds were found to be infected by C. flaccumfaciens pv. flaccumfaciens after surface sterilization with NaOCl (Tripepi and George, 1991). The pathogen has been shown to be present in soyabean seeds collected in 14 US states and in Ontario, Canada (Dunleavy, 1988). It is also seedborne in common bean (Schuster and Smith, 1983) and cowpea (Vigna unguiculata) seeds (Arcila and Trujillo, 1990). Masses of C. flaccumfaciens pv. flaccumfaciens were localized in testa cells of seeds of Zornia spp. (Chavarro et al., 1985).

Effect on Seed Quality

C. flaccumfaciens pv. flaccumfaciens is included in the A2 (high risk) list of quarantine pathogens by EPPO; hence, it is under strict quarantine control and zero tolerance in dry bean industry in several countries (EPPO, 2011). Economic losses caused by bacterial wilt disease are attributed not only to a substantial decrease in the net crop yield (i.e., number of pods per plants and number of mature seeds per pod) but also to a significant decrease in marketability of the product where visual appearance, shape and size of the seeds are determinative factors in pricing (Huang et al., 2009). C. flaccumfaciens pv. flaccumfaciens causes yellow or purple discoloration on common bean seeds but does not affect germination (Schuster and Sayre, 1967). However, the sprouting quality of mungbean can be affected (Conde and Diatloff, 1991) and seed infection by C. flaccumfaciens resulted in low germination of seeds of Zornia spp. (Chavarro et al., 1985). In visual inspections of dry bean fields it should be noted that seeds may become infected even when pods look healthy (Harveson et al., 2006). When bacterial wilt occurs on older plants, disease and symptom development proceed more slowly and are less severe. The percentage of common bean seeds possessing bacterial wilt symptoms in a given field (i.e., yellow, orange, pink or purple discoloration of the seed coat) was reported to vary between 0 and 25% in seed-producing fields in Canada and research plots in Nebraska, USA (Huang et al., 2003, 2004; Harveson et al., 2006, 2015).

Seed Transmission

C. flaccumfaciens pv. flaccumfaciens is primarily transmitted by contaminated seeds that carry the pathogen both externally and internally. It can also be found on overwintering bean straw (Schuster and Smith, 1983). Artificially inoculated mungbean seeds gave 6-12% transmission of C. flaccumfaciens pv. flaccumfaciens (Wood and Easdown, 1990). The bacteria may also be transmitted to mungbean via Ipomoea species: infected plants act as alternative weed hosts (Conde and Diatloff, 1991). Localized spread by irrigation water may also occur (Hedges, 1926). The rate of transmission in common bean seeds is reported to be higher than in other hosts of the pathogen. For instance, susceptible and resistant soyabean cultivars showed 0-1% and zero seed transmission, respectively; while up to 70% seed transmission was reported in susceptible common bean cultivars in greenhouse experiments (Camara et al., 2009; Soares et al., 2018). Bacterial tan spot lesions developed on soyabean seedlings grown in sterile soil in growth chambers from surface-sterilized seeds. Transmission rates averaged 13.5% and 7.0% for susceptible cultivars grown at 25°C and 30°C, respectively. No lesions were detected on seedlings grown at 10, 15, 20 or 35°C (Dunleavy, 1986).

Seed Treatments

Seed inspections during intra- and international transportation of dry beans should be employed to avoid the distribution of the pathogen to new areas with no history of the disease (EPPO, 2011). There are no effective seed treatments against C. flaccumfaciens pv. flaccumfaciens. Copper and antibiotics were ineffective (Tripepi and George, 1991) as were experimental heat treatments at 52°C for 20 h and 85°C for 5 h (Zaumeyer and Thomas, 1957).

Harding et al. (2007) concluded that resistance to chemicals is attributed to the capacity of the bacterial wilt pathogen in biofilm production. Recently, Harveson (2019) reported the results of a 7-year (2010-2016) field study (13 site years) investigating the performance of newly available antimicrobial chemicals for managing the four major bacterial diseases of dry beans (i.e., common blight, halo blight, brown spot and wilt). These novel products were compared with two conventional copper‐based products, copper hydroxide and copper sulfate, in Nebraska, USA, and several showed great promise for reducing losses due to these diseases. Treatments with hydrogen peroxide and peroxyacetic acid and ecoAgra 300 (plant-based fatty acids) consistently produced higher seed yields than the other treatments compared to the controls while not reducing disease incidence. These products do not appear to be curative, but act as protectants by slowing or prohibiting disease progress. Better results in all seasons were achieved from severely affected fields, than those from fields with low levels of disease (Harveson, 2019).

Soares and Maringoni (2002) evaluated the use of acibenzolar-S-methyl and its effect on the germination and vigour of common bean seeds and the induction of resistance to bacterial wilt. Results indicated that the seed treatment was phytotoxic to seeds, reducing the number of normal plants that developed in germination and vigour tests. Acibenzolar-S-methyl did not efficiently induce resistance to bacterial wilt when applied either as a seed treatment or as a spray. Ryley et al. (2010) suggested that the use of clean seed from a certified source and resistant cultivars are equally important in the management of bacterial wilt (tan spot) on mungbean in Australia, while crop rotation played a minor role.

Antibiotic seed treatment can reduce surface contamination of seeds. For instance, slurry seed treatments using Streptomycin Agri-Strep 500 were shown to be effective to combat C. flaccumfaciens pv. flaccumfaciens infection on common bean seeds (Schwartz, 2007). Soaking the seeds in Agrimaicin 500 solution, containing copper sulphate and oxytetracycline, eliminated the bacterium from naturally infected seeds; however, it was not effective on the artificially inoculated seeds using 108 c.f.u./ml suspension of the pathogen (Estefani et al., 2007).

Seed Health Tests

Grow-out test (Dunleavy, 1986; USDA National Seed Health System Standard Method, www.seedhealth.org).

1. Surface-sterilize the suspected dry bean seeds and plant in sterile soil.
2. Grow seeds at 30°C under growth-chamber conditions until characteristic leaf symptoms are visible. Refer to EPPO (2011) for further details.

Serological tests (Calzolari et al., 1987)

Although a number of serological techniques were developed for detection of C. flaccumfaciens pv. flaccumfaciens, they are unable to differentiate non-pathogenic lineages of C. flaccumfaciens from the pathogenic members (Calzolari et al., 1987; Diatloff et al., 1993; McDonald and Wong, 2000). Immunofluorescence staining was successful in the detection of C. flaccumfaciens pv. flaccumfaciens to a concentration of 1.23 × 107, which corresponded to 1.82 × 104 fluorescent cells per ml of soaked seed leachate (Calzolari et al., 1987). Immunofluorescence tests using a polyclonal antibody produced against C. flaccumfaciens pv. flaccumfaciens strain NCPPB 559 lacked adequate sensitivity and did not react with all tested C. flaccumfaciens pv. flaccumfaciens strains (Calzolari et al., 1987; McDonald and Wong, 2000), while a monoclonal antibody developed by Diatloff et al. (1993) was able to detect the pathogen from symptomless mungbean plants.

Two methods have been compared for detecting C. flaccumfaciens pv. flaccumfaciens in commercial common bean seed lots. Experimentally contaminated seeds were homogenized and a standard extraction and concentration procedure used. The final pellets were used for immunofluorescence staining and indirect isolation through seedlings. The staining sensitivity threshold was 12,300,000, corresponding to 18,200 fluorescent cells per millilitre of final concentrate. The indirect isolation sensitivity threshold was 1,230,000, producing 43% symptomatic plants and 53% positive re-isolation.

Pathovar Specific PCR Primers

Two PCR tests for the detection of C. flaccumfaciens pv. flaccumfaciens in bean seeds are described in the literature (Guimaraes et al., 2001; Tegli et al., 2002). A highly sensitive and rapid PCR assay for the detection of C. flaccumfaciens pv. flaccumfaciens in common bean seeds was developed by Tegli et al. (2002). A pair of PCR primers (CffFOR2-CffREV4), targeting the sequence of a cloned DNA fragment of 550 bp amplified in repetitive-sequence-based-PCR (Rep-PCR) experiments, were designed and shown to specifically amplify a 306-bp DNA fragment using C. flaccumfaciens pv. flaccumfaciens DNA as template. Moreover, this PCR protocol successfully detected C. flaccumfaciens pv. flaccumfaciens in naturally infected bean seeds in 36 h. Using these primers in combination with Bio-PCR and centrifugally concentrated seed extract allows the detection of one artificially contaminated common bean seed among 999 healthy seeds (Deuner et al., 2012). The primer pair CffFOR2/CffREV4 did not direct the amplification of the expected 306 bp fragment in various non-pathogenic C. flaccumfaciens strains isolated from tomato and aubergine (Osdaghi et al., 2018a). Tegli et al. (2017) provided a detail-oriented step-by-step protocol for detection of C. flaccumfaciens pv. flaccumfaciens in dry bean seeds using both general and semi-selective culture media as well as conventional PCR.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Botanical gardens and zoos Yes Yes
Breeding and propagation Yes Yes
Crop production Yes Yes
Food Yes Yes
Forage Yes Yes
Garden waste disposal Yes Yes
Horticulture Yes Yes
Industrial purposes Yes Yes
Intentional release Yes Yes
Live food or feed trade Yes Yes
Ornamental purposes Yes Yes
People sharing resources Yes Yes
Research Yes Yes
Seed tradevery important Yes Yes Osdaghi et al. 2020

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Clothing, footwear and possessionsTransfer of seeds. Yes Yes Osdaghi et al. (2020)
MailTransfer of seeds. Yes Yes Osdaghi et al. (2020)
Consumables Yes Yes
Germplasmvery important Yes Yes
Plants or parts of plantsimportant Yes Yes

Plant Trade

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

Impact Summary

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CategoryImpact
Economic/livelihood Negative
Environment (generally) Negative

Impact

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Currently, economic yield losses due to bacterial wilt disease have been recorded in Brazil, Canada, eastern Australia, Iran, and the central high plains of the USA, where it causes death of seedlings and yield loss in surviving plants. It is becoming a serious, but sporadic, pathogen of soyabean, cowpea and mungbean in the USA, Iran and Australia. Sporadic yield losses of up to 19% in soyabean have been recorded in the USA (Dunleavy, 1978; Dunleavy et al., 1983; Dunleavy, 1984). Pasture establishment of the legume Zornia spp. is seriously affected in Colombia. Economic losses due to bacterial wilt disease are attributed not only to substantial decrease in the net crop yield (i.e., number of pods per plant and number of mature seeds per pod) but also to a significant decrease in marketability of the product where visual appearance, shape and size of the seeds are determinative factors in pricing (Huang et al., 2009). Hence, in visual inspections of dry bean fields it should be noted that seeds may become infected even when pods look healthy (Harveson et al., 2006).

Risk and Impact Factors

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Invasiveness
  • Invasive in its native range
  • Proved invasive outside its native range
  • Has a broad native range
  • Highly adaptable to different environments
  • Fast growing
  • Reproduces asexually
  • Has high genetic variability
Impact outcomes
  • Host damage
  • Modification of nutrient regime
  • Negatively impacts agriculture
  • Transportation disruption
  • Negatively impacts trade/international relations
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Highly likely to be transported internationally deliberately
  • Highly likely to be transported internationally illegally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Uses List

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General

  • Laboratory use
  • Research model

Diagnosis

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The bacterial wilt pathogen can readily be isolated from all above-ground parts of dry beans, but leaves, stems and seeds are the most suitable. Isolation of C. flaccumfaciens pv. flaccumfaciens from either seed lots or symptomatic plant tissues can be performed by cutting the marginal tissues of the visible lesions on leaves and grounding them in sterile distilled water (SDW). Spread a loopful of the resulting suspension on NBY (5 g glucose, 2 g K2HPO4, 0.5 g KH2PO4, 0.25 g MgSO4, 8 g nutrient broth, 2 g yeast extract and 15 g agar dissolved in 1 L SDW) or YPGA (10 g glucose, 5 g peptone, 5 g yeast extract and 15 g agar dissolved in 1 L SDW) media (EPPO, 1994, 2011). The bacterium grows also on a broad range of media, including Kelman’s medium, nutrient agar, MSC medium and King’s medium B (Tegli et al., 2017). Several methods for isolation can be employed. Margins of leaf lesions can be abraded or punctured with a dissecting needle, and streaked onto medium plates (Harveson et al., 2006; Harveson et al., 2015). Another technique involves squeezing the sap out of petioles attached to symptomatic tissues and blotting onto medium, followed by streaking with a sterilized inoculating loop (Harveson, 2013). For dried leaf samples, leaf tissues can be ground in SDW, shaken for 1-2 h to release the bacterial cells into the water, and a loopful of the resulting suspension can then be spread onto YPGA or NBY media. Another method of isolation can be utilized by placing dried tissues in humidity chambers for 12-24 hours. If present, bacteria will ooze out of necrotic tissues and can be streaked onto media (Harveson et al., 2015). Finally, the bacterium can also be isolated from infected, discoloured or even symptomless seeds. Discoloured seeds are soaked overnight in SDW and the eluent is streaked onto plates (Harveson and Schwartz, 2007). After streaking on the media surface, fluidal colony growth will be observed on the culture media after incubation at 25-27°C for 48-72 h.

To confirm whether a suspected plant is infected with the bacterial wilt pathogen, excise a piece of discoloured vascular tissue, or a discoloured seed, or the necrotic margin of the infected leaf tissue and comminute in sterile water. Streak bacterial suspension onto a glass slide and carry out Gram-staining. If Gram-positive, coryneform bacteria are detected in the suspension in large numbers and the plants show typical symptoms of wilt or spotting, a presumptive diagnosis can be made. For further confirmation, a loopful of the resulting suspension can be streaked onto yeast extract (7 g/litre) peptone (7 g/litre) glucose (7 g/litre) agar (18 g/litre) (YPGA) medium. The plates should be incubated at 27-30°C for 4-5 days. The appearance of yellow, orange or red-pigmented bacterial colonies is an approval of infection of the plant in question. Diagnosis as C. flaccumfaciens pv. flaccumfaciens can be confirmed by either specific PCR primers as described by Tegli et al. (2002) or stem-prick inoculation with bacteria into common bean (Phaseolus vulgaris), which is a suitable test plant for the various host isolates (for a detailed description, see Osdaghi et al. (2020) and Tegli et al. (2017)).

Detection and Inspection

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In growing crops, C. flaccumfaciens pv. flaccumfaciens can be detected as leaf chlorosis and large, tan-coloured spotting with or without wilting. Infected common bean seeds may be discoloured yellow, orange or purple, but discoloration does not occur on soyabean, cowpea or mungbean, which are symptomless carriers.

Similarities to Other Species/Conditions

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Bacterial wilt symptoms may be confused with those caused by the common bacterial blight pathogen, Xanthomonas axonopodis pv. phaseoli in areas where both pathogens occur in the same field (Harveson et al., 2011). Bacterial wilt lesions occur between veins, often accompanied by wilting and death of severely infected plants. Whereas, wilting and plant death are less likely to occur in common bacterial blight and other bacterial diseases, i.e., halo blight and brown spot caused by Pseudomonas savastanoi pv. phaseolicola and P. syringae pv. syringae, respectively (Schwartz et al., 2005; Harveson and Schwartz, 2007), although neither of these pathogens is systemic. Isolation in a laboratory would be necessary to distinguish these pathogens.

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

No effective chemical control is available against C. flaccumfaciens pv. flaccumfaciens, although secondary spread can be retarded by bactericidal sprays of copper fungicide. Weeds, volunteer plants and plant debris that act as reservoirs of infection should be eliminated.

Heat treatment does not eliminate the pathogen from seeds; there are no established seed treatments. Development of resistant cultivars is the most practical method for managing bacterial wilt disease in terms of cost effectiveness and durability over time. Common bean cultivars and varieties differ in their reaction to the pathogen, and resistant or tolerant varieties should be planted, if available, in the areas where the disease is established (Hsieh et al., 2005; Urrea and Harveson, 2014). Furthermore, considering the differences among C. flaccumfaciens pv. flaccumfaciens colony variants in their virulence and aggressiveness, a given cultivar/line should be evaluated for its resistance against different variants of the pathogen (Huang et al., 2007; Conner et al., 2008; Urrea and Harveson, 2014).

As for the biological control methods, Corrêa et al. (2014) applied a combination of Bacillus cereus and Pseudomonas fluorescens strains to reduce the severity of bacterial wilt by seed inoculation using the antagonistic bacterial suspension. Bacterial wilt reduction ranged from 42 to 76% (Martins et al., 2013). Environmental temperature (20 vs. 30°C) interferes with the colonization of plants with the pathogen and antagonist, while the suppression of bacterial wilt using the B. cereus strain ALB629 was similar in the two temperatures (Martins et al., 2014). Furthermore, soaking common bean seeds in a suspension (3×108 c.f.u./ml) of Pantoea agglomerans resulted in thorough endophytic colonization of the entire bean seedling from root to apical stem 7 days post inoculation and resulted in the reduction of bacterial wilt severity in greenhouse conditions (Hsieh et al., 2005). The application of P. agglomerans as a soil drench 24 h post planting was effective in suppressing bacterial wilt, but not as effective as seed treatment (Hsieh et al., 2005). Furthermore, seed treatment using Rhizobium leguminosarum reduced bacterial wilt and common bacterial blight diseases in greenhouse conditions (Huang et al., 2007b). Bacteriophages have also been proposed for the control of the bacterial wilt pathogen but no detailed information is available in this regard (Klement 1957).

References

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Contributors

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29/08/20 Reviewed by:

Ebrahim Osdaghi, Department of Plant Protection, University of Tehran, Karaj 31587-77871, Iran.

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