Xanthomonas citri
(citrus canker)

Pictures

Picture	Title	Caption	Copyright
Title Symptoms Caption Symptoms of citrus canker on leaves. Copyright Elizabeth Asteraki/CABI SEARC	Symptoms	Symptoms of citrus canker on leaves.	Elizabeth Asteraki/CABI SEARC
Title Symptoms on leaf Caption Canker lesions develop as light yellow, raised, spongy eruptions on the surface of leaves. Copyright Masao Goto	Symptoms on leaf	Canker lesions develop as light yellow, raised, spongy eruptions on the surface of leaves.	Masao Goto
Title Symptoms on bark Caption Bark lesions from which X. campestris pv. citri was detected. Copyright Masao Goto	Symptoms on bark	Bark lesions from which X. campestris pv. citri was detected.	Masao Goto
Title Stem lesions Caption As the disease advances, lesions appear as corky dead tissue with a rough surface surrounded by a yellow halo. Copyright Masao Goto	Stem lesions	As the disease advances, lesions appear as corky dead tissue with a rough surface surrounded by a yellow halo.	Masao Goto
Title Symptoms on branch Caption Bacterial canker of citrus. Copyright ©CABI BioScience	Symptoms on branch	Bacterial canker of citrus.	©CABI BioScience
Title Lesions on fruit Caption Brown depressions appear in the central portion of lesions forming a crater-like appearance. Copyright Masao Goto	Lesions on fruit	Brown depressions appear in the central portion of lesions forming a crater-like appearance.	Masao Goto
Title TEM of bacterial cell Caption Electron micrograph of X. campestris pv. citri. Copyright Masao Goto	TEM of bacterial cell	Electron micrograph of X. campestris pv. citri.	Masao Goto
Title Stomatal infection Caption Light micrograph of lesion resulting from stomatal infection. Copyright Masao Goto	Stomatal infection	Light micrograph of lesion resulting from stomatal infection.	Masao Goto
Title Wound infection Caption Light micrograph of lesion resulting from wound infection. Copyright Masao Goto	Wound infection	Light micrograph of lesion resulting from wound infection.	Masao Goto
Title Wound healing Caption Light micrograph of normal wound healing. Copyright Masao Goto	Wound healing	Light micrograph of normal wound healing.	Masao Goto

Identity

Preferred Scientific Name

• Xanthomonas citri (Hasse 1915) Gabriel et al., 1989

Preferred Common Name

• citrus canker

Other Scientific Names

• Bacillus citri (Hasse) Holland 1920
• Bacterium citri (Hasse) Doidge 1916
• Phytomonas citri (Hasse) Bergey et al., 1923
• Pseudomonas citri Hasse 1915
• Xanthomonas axonopodis pv. aurantifolii Vauterin et al., 1995
• Xanthomonas axonopodis pv. citri (ex Hasse 1915) Vauterin et al., 1995
• Xanthomonas campestris pv. aurantifolii Gabriel et al., 1989
• Xanthomonas campestris pv. citri (Hasse 1915) Dye 1978
• Xanthomonas citri f.sp. aurantifolia Namekata & Oliveira 1972
• Xanthomonas citri ssp. citri Schaad et al. 2005
• Xanthomonas fuscans ssp. aurantifolii Schaad et al. 2005

International Common Names

• English: citrus bacterial canker
• Spanish: bacteriosis del limonero; cancro cítrico; cancrosis de los cítricos
• French: chancre bactérien des agrumes; chancre citrique

Local Common Names

• China: ganju kuiyang-bing
• Germany: Bakterienkrebs: Zitrus
• Japan: kankitsu kaiyo-byo
• Korea, Republic of: kamgyul gueyangbyung-byung

EPPO code

• XANTCI (Xanthomonas axonopodis pv. citri)

Summary of Invasiveness

X. citri is a bacterial pathogen that causes citrus canker - a disease which results in heavy economic losses to the citrus industry worldwide either in terms of damage to trees (particularly reduced fruit production), reduced access to export markets, or the costs of its prevention and control. Lesions appear on leaves, twigs and fruit which cause defoliation, premature fruit abscission and blemished fruit, and can eventually kill the tree. It is introduced to new areas through the movement of infected citrus fruits and seedlings, and inadvertent re-introduction is highly likely despite the quarantine restrictions that are in place in many countries. Locally, X. citri is rapidly disseminated by rainwater running over the surfaces of lesions and splashing onto uninfected shoots; spread is therefore greatest under conditions of hight temperature, heavy rainfall and strong winds. Some areas of the world have eradicated citrus canker, others have on-going eradication programmes, however, this pathogen remains a threat to all citrus-growing regions.  

Taxonomic Tree

• Domain: Bacteria
•     Phylum: Proteobacteria
•         Class: Gammaproteobacteria
•             Order: Xanthomonadales
•                 Family: Xanthomonadaceae
•                     Genus: Xanthomonas
•                         Species: Xanthomonas citri

Notes on Taxonomy and Nomenclature

Citrus canker, Asian canker and Oriental canker were names for the disease associated with the pathogenic species Xanthomonas citri, then with Xanthomonas campestris pv. citri. Subsequently, Citrus canker strains, Asian canker strains or Oriental canker strains were allocated as group A strains to X. campestris pv. citri, and four other pathogens, as group B strains (causing cancrosis B), group C strains (causing Mexican lime cancrosis), group D strains (causing citrus bacteriosis), and group E strains (causing citrus bacterial spot (Civerolo, 1985)) have been identified. Gabriel et al. (1989) combined the group B, C and D strains in Xanthomonas campestris pv. aurantifolii but failed to fulfil any of the standards required for formally naming pathovars. They also named group E strains as Xanthomonas campestris pv. citrumelo, but failed to show this pathogen differed from the previously named Xanthomonas campestris pv. alfalfae (Young et al., 1991). Vauterin et al. (1995) allocated the pathovar citri group A strains to Xanthomonas axonopodis pv. citri and used the defective names pv. aurantifolii and pv. citrumelo without amendment. Two groups of strains that are genetically similar to the group A strains, but have restricted host ranges were described as A* and A^W strains (Sun et al., 2004; Verniere et al., 1998).

Group A (Asiatic or Oriental canker), group B (cancrosis B), group C (Mexican lime cancrosis), group D (citrus bacteriosis) and group E (citrus bacterial canker) are distinguished on the basis of host specificity and pathogen aggressiveness (Carrera, 1933; Namekata, 1971; Civerolo, 1985; Rodriguez et al., 1985). The restricted host ranges or weak pathogenicity of group B, group C, group D and group E strains has been widely recognized (Stall and Civerolo, 1991). The genotypic and phenotypic diversity has been demonstrated even among group A strains as aggressiveness to Citrus spp., serological reactions, and specific DNA fragments in PCR amplification (Verniere et al., 1998; Shintani et al., 2000). Although cultures of all the groups of strains exist in collections, the diseases caused by the group C and D no longer exist in nature.  The disease caused by group B may also no longer exist in nature because of the pathogen’s noncompetitiveness with the group A strains which were introduced into the areas previously occupied by the group B strains.  

There is no satisfactory formal nomenclature for these distinct pathogens. Any discussion of these pathogens should distinguish them either as groups of strains or by the common disease names. Unless otherwise stated, the discussion here refers to the group A, Asian or Oriental canker strain.

The current preferred name for this pathogen is Xanthomonas citri.

Description

Phenotypic Characteristics

X. citri is a Gram-negative, straight, rod-shaped bacterium measuring 1.5-2.0 x 0.5-0.75 µm. It is motile by means of a single, polar flagellum. It shares many physiological and biochemical properties with other members of the genus Xanthomonas. It is chemoorganotrophic and obligately aerobic with the oxidative metabolism of glucose. Colonies are formed on nutrient agar plates containing glucose and are creamy-yellow with copious slime. The yellow pigment is xanthomonadin. Catalase is positive, but Kovacs' oxidase is negative or weak; nitrate reduction is negative. Asparagine is not used as a sole source of carbon and nitrogen simultaneously; various carbohydrates and organic acids are used as a sole source of carbon. Hydrolysis of starch, casein, Tween 80 and aesculin is positive. Gelatine and pectate gel are liquefied. Growth requires methionine or cysteine and is inhibited by 0.02% triphenyltetrazolium chloride. Biovars may be distinguished by utilization of mannitol. For further information on the bacteriological properties of X. citri, see Goto (1992).

Strains of groups B, C and D have many properties in common with group A, the differences being detected by the utilization of only a few carbohydrates (Goto et al., 1980).

Molecular Characterization

Features of citrus-attacking xanthomonads including X. citri and the genus Xanthomonas as a whole, have been characterized at the molecular level for the development of quick and accurate methods for reclassification and identification. The procedures include DNA-DNA hybridization (Vauterin et al., 1995), genomic fingerprinting (Lazo et al., 1987), fatty acid profiling (Yang et al., 1993), SDS-PAGE (Vauterin et al., 1991) and isoenzyme profiles (Kubicek et al., 1989) and monoclonal antibodies (Alverez et al., 1991).

Bacteriophages

Phage-typing is applicable to X. citri with greater reliability than any other plant pathogenic bacterium investigated so far. Many strains of X. citri are lysogenic (Okabe, 1961). Two virulent phages, Cp1 and Cp2, can infect 98% of the strains isolated in Japan (Wakimoto 1967). Similar results were also obtained in Taiwan (Wu et al., 1993). The filamentous temperate phages and their molecular traits have been studied in detail (Kuo et al., 1994; Wu et al., 1996). Phage Cp3 is specific to the canker B strains (Goto et al., 1980). No phages specific to canker C and D strains have been isolated.

Distribution

The geographical distribution of X. citri differs for different types of citrus canker. Canker A (Asiatic canker) is found in Asia, South America, Oceania and the USA (Carrera, 1933); canker B (Cancrosis B) in South America (Carrera, 1933); canker C (Mexican lime cancrosis) in Brazil (Namekata, 1971); and canker D (citrus bacteriosis) in Mexico (Rodriguez et al., 1985).

Citrus canker is so common and prevalent in Asia and South America that it may also be present in countries and regions which are not listed in the table of geographical distribution.

In addition to the countries listed in the table of geographical distribution, citrus canker has also been reported in Arab countries (Ibrahim and Bayaa, 1989).

X. citri has been eradicated from New Zealand and Australia (IMI, 1996) including Thursday Island (Jones, 1991) and also from South Africa (IMI, 1996). An outbreak in Queensland, Australia, in 2004 was declared eradicated (IPPC, 2009). X. citri has been detected in Northern Territory (IPPC, 2018) and Western Australia (Commonwealth of Australia, 2018; DPIRD, 2018) and is under eradication.

A record for India (Uttar Pradesh) (IMI, 1996) cited in previous editions of the Compendium appears to be erroneous.

The present situation in the Ryukyu Archipelago can not be confirmed (CABI/EPPO, 2006).

EU Commission Decision 98/83 of 8 January 1998 recognizes Chile, Guam, Mexico and South Africa to be free from all strains of Xanthomonas campestris pathogenic to citrus.

See also CABI/EPPO (1998, No. 281).

Distribution Table

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.

Risk of Introduction

RISK CRITERIA CATEGORY

ECONOMIC IMPORTANCE High
DISTRIBUTION Worldwide except Europe
SEEDBORNE INCIDENCE Not recorded
SEED TRANSMITTED Not recorded
SEED TREATMENT None
INSECT TRANSMISSION None

OVERALL RISK Low

Habitat List

Hosts/Species Affected

The Citrus species listed in the table of hosts, and the following hybrids, are natural hosts of X. citri, with varying degrees of susceptibility to X. citri. In addition to host plant, susceptibility is also affected by the plant part affected, whether leaves, fruits or twigs. Reddy and Naidu (1986) reported canker lesions on roots but this has not been confirmed.

Hybrids:

C. aurantiifolia x Microcitrus australasica (Faustrime), C. limon x M. australasica (Faustrimon), C. madurensis x M. australasica (Faustrimedin), C. sinensis x Poncirus trifoliata (Citrange), C. paradisi x P. trifoliata (Citrumelo) (Schoulties et al., 1987), C. aurantifolium x P. trifoliata (Citradia), C. nobilis x P. trifoliata (Citrandin), C. unshiu x P. trifoliata (Citrunshu), Citrange x P. trifoliata (Cicitrangle), C. adurensis x Citrange (Citrangedin), C. deliciosa x Citrange (Citrangarin), C. unshiu x Citrange (Citranguma), Fortunella margarita x Citrange (Citrangequat), F. japonica x C. aurantiifolia (Limequat), C. maxima x C. aurantiifolia (Limelo), C. madurensis x C. aurantiifolia (Bigaraldin), C. maxima x C. sinensis (Orangelo), F. margarita x C. sinensis (Orangequat), C. nobilis (Clementine) x C. maxima (Clemelo), C. nobilis (King of Siam) x C. maxima (Siamelo), C. unshiu x C. maxima (Satsumelo), C. deliciosa x C. maxima (Tangelo), C. nobilis (King of Siam) x C. sinensis (Siamor), C. deliciosa x C. madurensis (Calarin), C. unshiu x C. madurensis (Calashu). C. aurantiifolia x F. marginata is immune (Reddy, 1997).

Other than Citrus species and their hybrids, most plants, except P. trifoliata, are not sufficiently susceptible to X. citri under natural conditions to warrant attention as hosts of the bacterium. Although the potential of these plants as natural hosts seems to be negligible, further investigation is necessary because no confirmative host surveys have been undertaken since the 1920s. Species names within the genus Citrus also merit some attention due to their inconsistent use by authors.

Plants other than Citrus spp.:

Unless otherwise stated, the following plants refer to Peltier and Frederich (1920, 1924) who defined susceptibility on the basis of artificial inoculation in the greenhouse (G) and/or in the field (F): Aeglopsis chevalieri (G), Atalantia ceylonica (G), Atalantia citrioides (G), Atalantia disticha (G) (Lee, 1918), Chalcas exotica (G), Casimiroa edulis (G, F), Chaetospermum glutinosum (G, F), Clausena lansium (G), Citropsis schweinfurthii (G), Eremocitrus glauca (G, F), Evodia latifolia (G), Evodia ridleyei (G), Feronia limonia [Limonia acidissima] (G), Feroniella lucida (G, F), Feroniella crassifolia (G), Fortunella hindsii (G, F), Fortunella japonica (G, F), Fortunella margarita (G, F), Hesperethusa crenulata (G, F), Lansium domesticum (G), Melicope triphylla (G), Microcitrus australasica (G, F), Microcitrus australasica var. sanguinea (G, F), Microcitrus australis (G, F), Microcitrus garrowayi (G, F), Paramignya monophylla (G), Paramignya longipedunculata (G) (Lee, 1918), Poncirus trifoliata (G, F), Xanthoxylum clava-herculis [Zanthoxylum clava-herculis] (G, F), Xanthoxylum fagara [Zanthoxylum fagara] (G, F) (Jehle, 1917). Atalantia ceylanica, A. monophylla, Microcitrus australis, Feronia limonia and Severinia buxifolia are immune (Reddy, 1997). In India, goat weed (Ageratum conyzoides) is reported to be a host (Pabitra et al., 1997) but confirmation is needed.

The following plants have also been reported as susceptible to X. citri, however, the original descriptions were either not confirmed (U) or contradict those of other authors (C): Aegle malmelos (C), Balsamocitrus paniculata (U), Feroniella obligata (U), Matthiola incana var. annua (U) and Toddalia asiatica (C).

Of the primary hosts listed, yuzu is highly resistant (Goto, 1992) and calamondins, Cleopatra mandarin and Sunki mandarin are immune (Reddy, 1997). Both Fortunella japonica and F. margarita are highly resistant (Goto, 1992).

Host Plants and Other Plants Affected

Growth Stages

Symptoms

Canker lesions begin as light yellow, raised, spongy eruptions on the surface of leaves, twigs and fruits. The lesions continuously enlarge from pin-point size over several months and can be of many different sizes based on the age of the lesion. As the lesions enlarge, the spongy eruptions begin to collapse, and brown depressions appear in their central portion, forming a crater-like appearance. The edges of the lesions remain raised above the surface of host tissue and the area around the raised portion of the lesion may have a greasy appearance. The lesions become surrounded by characteristic yellow halos. Canker lesions retain the erupted and spongy appearance under dry conditions, such as in a greenhouse; whereas they quickly enlarge and turn to flat lesions with a water-soaked appearance with frequent rain. Canker lesions vary in maximum size from 5 to 10 mm, depending on the susceptibility of the host plant. The symptoms are similar on leaves, fruit and stems.

Canker lesions are histologically characterized by the development of a large number of hypertrophic cells and a small number of hyperplastic cells. At an early stage of infection, the cells increase in size and the nuclei and nucleoids stain more easily; there is also an increase in the amount of cytoplasm synchronized with rapid enlargement. However, these hypertrophied cells do not divide; cell division is only detected in the peripheral areas of lesions adjacent to healthy tissue.

The lesions of canker B, C and D are similar in appearance and histology to those of canker A (Goto, 1992).

Reddy and Naidu (1986) reported canker lesions on roots; however, this has not been confirmed.

List of Symptoms/Signs

Biology and Ecology

Citrus canker occurs in areas of the world where high rainfall and high temperatures co-exist. In those areas, citrus canker occurs on seedlings and young trees in which there are continuous flushes of shoots from spring through autumn. However, the disease becomes sporadic as trees reach full fruiting development when flushes of growth occur sporadically. Leaves and stems are susceptible to infection for only a short time period after flushes begin growth. If weather conditions are not favourable for infection during the susceptibility period disease will not develop (Stall et al., 1982). Fruit are susceptible for longer periods after set than are leaves and stems. Disease severity also depends on the susceptibility of the host plant species and cultivar (Goto, 1992).

Canker lesions are formed on the leaves, twigs and fruits of host plants. The occurrence of canker lesions on root systems in soil (Reddy and Naidu, 1986) is not confirmed. X. citri can also be isolated from discolored areas in bark on branches, limbs and trunks, however, it is not certain whether these are novel lesions resulting from direct infection or scars remaining from infection at an earlier stage of growth (Goto, 1992).

Molecular Aspects of Pathogenesis

Molecular recognition events eliciting a virulence response were reported for citrus canker. The protein from the expression of the pthA gene in the pathogen is secreted into the host cells through a functional type III secretion system. The pthA protein mobilizes to the nucleus of host cells and combines with DNA of the host cells. The transcription activation of host cells results in division, enlargement and death of hosts cells. One of the pthA homologues, Ap11 (avir/pthA-like), is thought to be a signal specific for canker formation. In this latter study, the signal protein is bound to trans-caffeoyl-coenzyme A 3-O-methyltransferase (CCoAMT) which catalyses the synthesis of a coenzyme for lignin formation, although the role of lignification in canker formation is open to question (Kanamori and Tsuyumu, 1998; Almeida and Tsuyumu, 2000).

Survival (Inoculum Sources)

X. citri survives in diseased plant tissues from season to season and is the primary inoculum source. It has been reported to survive as an epiphyte on host and non-host plants, and as a saprophyte on straw mulch or in soil. However, overwintering lesions, particularly those formed on angular shoots in the autumn, are the most important source of inoculum for the following season.

The overwintering bacterium forms lesions early in the following spring and a large number of bacteria disperse from these lesions. The bacterium can survive for long periods in discolored bark tissue of tree trunks, low scaffold limbs and lateral branches. 

Dissemination

X. citri is disseminated by rainwater running over the surfaces of lesions and splashing onto uninfected shoots. The concentration of bacteria is largely dependent on the age of the lesions with a maximum of a million cells/drop (Stall et al., 1980). Rainstorms such as typhoons and hurricanes encourage outbreaks of citrus canker where active sources of inoculum are available because strong winds can injure the leaves and twigs and force bacteria through the stomata. Although rainstorms can transport bacteria up to 100 m or more in small raindrops and/or aerosols, effective infection rarely occurs more than a few rows downwind (Goto, 1992). Overhead irrigation worsens the spatial and temporal development of the disease due to splash dispersal of the pathogen, and causes great concern in nurseries producing canker-free young trees (Pruvost et al., 1999).

Epidemiology

Epidemics of citrus canker on mature plants are characteristically sporadic; severe disease occurs every decade or so after the complete absence of the disease from the field. This implies that the disease is consistently present in fields as latent infections, but at an undetectable level; the absence of the disease from the field for at least 10 years is not sufficient to declare that the disease has been eradicated. Danos et al. (1984) studied the temporal and spatial spread of citrus canker within groves.

Seedborne Aspects

Pathway Causes

Pathway Vectors

Plant Trade

Impact Summary

Impact

Losses due to citrus canker primarily result from defoliation, premature fruit abscission and blemished fruit. It is not uncommon for almost 100% of the fruits and leaves of young, susceptible trees to be infected. Development and the achievement of full growth may be delayed in severely infected, young trees.

The impact of the disease has not been fully elucidated by the assessment of loss. The practical risk of transcontinental dissemination of citrus canker through lesions on marketable fruits requires investigation.

Economic Impact

Monetary losses occur due to yield losses and an increase in pesticide usage, and loss of markets because of regulatory laws.

Social Impact

The social impact of the disease includes an increased use of pesticides and loss of income.

Risk and Impact Factors

• Proved invasive outside its native range
• Abundant in its native range
• Highly adaptable to different environments
• Tolerant of shade
• Highly mobile locally
• Benefits from human association (i.e. it is a human commensal)
• Fast growing
• Has high reproductive potential
• Reproduces asexually
• Has high genetic variability

• Ecosystem change/ habitat alteration
• Host damage
• Negatively impacts agriculture
• Negatively impacts cultural/traditional practices
• Negatively impacts livelihoods
• Transportation disruption
• Damages animal/plant products
• Negatively impacts trade/international relations

• Pest and disease transmission
• Parasitism (incl. parasitoid)
• Pathogenic

• Highly likely to be transported internationally accidentally
• Highly likely to be transported internationally illegally
• Difficult/costly to control

Uses List

General

• Research model

Genetic importance

• Test organisms (for pests and diseases)

Diagnosis

Asiatic citrus canker is relatively easy to diagnose because of the characteristic symptoms of the disease. The pathogen may be isolated on nutrient agar (NA) or potato dextrose agar (PDA) at pH 6.8. Growth develops in 48 to 72 hours and colonies are creamy-yellow (on PDA) to straw-yellow (on NA). The identification of isolated bacteria can be confirmed by pathogenicity to grapefruit leaves or by the polymerase chain reaction (PCR) using specific primers (Goto, 1992). Differentiation of canker A strains from other groups can be made with confidence using the methods reported in molecular characterization.

The diagnosis of citrus canker using polymerase chain reaction (PCR) is accurate and rapid (Wang et al., 2004; Mavrodieva et al., 2004). Golmohammadi et al. (2007) and Yin et al. (2007) found real-time PCR to be more effective at detecting X. citri, and up to 100-1000 times as sensitive.

Detection and Inspection

Methods of detecting X. citri from natural habitats include leaf-infiltration, bacteriophage, fluorescent antibody and ELISA (Goto, 1992). The polymerase chain reaction and dot blot immunobinding assay (DIA) were developed for rapid, sensitive, and specific detection of the pathogen. The detectable limits were reported to be around 30 c.f.u./ml for the former and 1000 c.f.u./ml for the latter (Hartung et al., 1993, 1996; Wang et al., 1997; Miyoshi et al., 1998).

Similarities to Other Species/Conditions

Citrus bacterial spot, caused by group E strains (X. campestris pv. citrumelo) (Schoulties et al., 1987) and bacterial brown spot, caused by Pseudomonas syringae pv. syringae (Shigeta and Nakata, 1995) are distinguished from citrus canker by a distinctive water-soaked appearance along the margins of lesions and the absence of hypertrophic eruption. Canker B, C and D (Namekata, 1971) are distinguished by a narrow host range of Mexican lime and lemon under natural conditions.

Care must be taken not to confuse X. citri with Pantoea agglomerans in culture, P. agglomerans often produces yellow colonies on isolation media.

Prevention and Control

Regulatory Control

Safeguards for exporting citrus fruits into the USA from Japan include: the establishment of isolated canker-free export areas; inspection of fruit by plant pathologists in both countries during harvesting and packing operations; pre-shipping surface sterilization with bactericidal dip; pre-shipping inspection using the bacteriophage method to ensure fruits are free of X. citri; and certification by the Japanese Plant Protection Service that fruits are free of X. citri (Goto, 1992).

Cultural Control

The disease has attracted widespread attention because of the serious efforts that have been made for eradication; these include destriction of citrus trees on a large scale and the implementation of strict international plant quarantine regulations against the pathogen (Stall and Civerolo, 1991; Goto, 1992).

The use of canker-free nursery plants is the first essential step in the management of citrus canker. Windbreaks established around citrus groves reduce disease. Pruning of angular shoots which hold canker lesions removes overseasoning inocula.  Periodic spraying with insecticides to control the leaf miner, Phyllocnistis citrella, reduces infection sites (Goto, 1992).

Biological Control

Interactions between X. citri and antagonistic bacteria including Bacillus subtilis (Pabitra et al., 1996), Pantoea agglomerans (Goto et al., 1979), Pseudomonas syringae (Ohta, 1983) and P. fluorescens (Unnamalai and Gnanamanickam, 1984) have been reported in vitro and in vivo. However, the practical usefulness of these bacteria in controlling the pathogen has not been proved.

Chemical Control

The disease cannot be controlled by chemicals after it has reached epidemic proportions. Therefore, the prevention of primary infection on spring shoots is emphasized; this is achieved by spraying copper compounds 10-14 days after the first shoots emerge in the spring (Stall et al., 1981). Reduction of disease on spring shoots reduces inocula for subsequent developing shoots.

Early Warning Systems

A forecasting system has been adopted in Japan. The number of overwintered lesions on angular shoots is determined and meteorological data such as temperature, precipitation and wind velocity are monitored from autumn through to early spring; these factors are responsible for the build-up of bacterial populations in citrus groves. Outbreaks of the disease can be predicted 1-2 months in advance (Goto, 1992).

References

1986. New pests recorded. Arab and Near East Plant Protection Newsletter, No. 3:17-18, 5-6

Alizadeh A, Rahimian H, 1990. Citrus canker in Kerman Province. Iranian Journal of Plant Pathology, 26(1-4):42 (En), 118 (Pe)

Almeida AG, Tsuyumu S, 2000. Cloning of a genomic DNA encoding caffeoyl-coenzyme A 3-O-methyltransferase of citrus. Journal of General Plant Pathology, 66(2):144-148; 11 ref.

Alvarez AM, Benedict AA, Mizumoto CY, Pollard LW, Civerolo EL, 1991. Analysis of Xanthomonas campestris pv. citri and X. c. citrumelo with monoclonal antibodies. Phytopathology, 81(8):857-865

APPPC, 1987. Insect pests of economic significance affecting major crops of the countries in Asia and the Pacific region. Technical Document No. 135. Bangkok, Thailand: Regional Office for Asia and the Pacific region (RAPA).

Bergey DH, Harrison FC, Breed RS, Hammer BW, Huntoon FM, 1923. Bergey's Manual of Determinative Bacteriology, 1st ed. Baltimore, USA: The Williams and Wilkins Co.

Bradbury JF, 1986. Guide to Plant Pathogenic Bacteria. Wallingford, UK: CAB International.

CABI/EPPO, 1998. Distribution maps of quarantine pests for Europe (edited by Smith IM, Charles LMF). Wallingford, UK: CAB International, xviii + 768 pp.

CABI/EPPO, 2006. Xanthomonas axonopodis pv. citri. Distribution Maps of Plant Diseases, No. 11. Wallingford, UK: CAB International.

CABI/EPPO, 2006. Xanthomonas axonopodis pv. citri. Distribution Maps of Plant Diseases, No. 11. Wallingford, UK: CAB International.

CABI/EPPO, 2014. Xanthomonas citri subsp. citri. [Distribution map]. Distribution Maps of Plant Diseases, No.October. Wallingford, UK: CABI, Map 11 (Edition 8).

Carrera C, 1933. Informe preliminar sobre una enfermedad nueva comprobada en los citrus de Bella Vista (Corrientes). Bol Mens Min Agric Nac Buenos Aires, 34:275-280.

Civerolo EL, 1985. Comparative characteristics of Xanthomonas campestris pv. citri variants. In: Abstracts on the genus Xanthomonas. Fallen Leaf Lake Conference, Fallen Leaf Lake, South Lake Tahoe, California, September 20-23, 1985, 24 pp.

Commonwealth of Australia, 2018. Current responses to outbreaks: Citrus canker. National Biosecurity Communication and Engagement Network. http://www.outbreak.gov.au/current-responses-to-outbreaks/citrus-canker.

Cook AA, 1988. Association of citrus canker pustules with leaf miner tunnels in North Yemen. Plant Disease, 72(6):546

Danós E, Berger RD, Stall RE, 1984. Temporal and spatial spread of citrus canker within groves. Phytopathology, 74(8):904-908.

Davis RI, Taylor RK, Rouse D, Flack M, Hailstones D, Jones LM, Rossel JB, Fanai C, Tsatsia F, Tsatsia H, 2015. First record of citrus canker, caused by Xanthomonas citri subsp. citri in Solomon Islands. Australasian Plant Disease Notes, 10(1):9. http://rd.springer.com/article/10.1007/s13314-014-0156-8/fulltext.html

Doidge EM, 1916. Citrus canker in South Africa. South African Fruit Grower, 3:265-268.

Dowson DW, 1939. On the systematic position and generic names of the Gram negative bacterial plant pathogens. Zentralblatt fur Bakteriologie, Parasitenkunde und Infektionskrankheiten, 2, 100:177-193.

DPIRD, 2018. Biosecurity alert: Citrus canker. Department of Primary Industries and Regional Development (DPIRD). May 25, 2018. https://www.agric.wa.gov.au/citruscanker2018.

Duan YP, Castaneda A, Zhao G, Erdos G, Gabriel DW, 1999. Expression of a single, host-specific, bacterial pathogenicity gene in plant cells elicits division, enlargement, and cell death. Molecular Plant-Microbe Interactions, 12(6):556-560; 26 ref.

Dye DW, 1978. Genus IX. Xanthomonas Dowson 1939. In: Young JM, Dye DW, Bradbury JF, Panagopoulos CG, Robbs CF, eds. A proposed nomenclature and classification for plant pathogenic bacteria. New Zealand Journal of Agricultural Research, 21:153-177.

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Gabriel DW, Kingsley MT, Hunter JE, Gottwald T, 1989. Reinstatement of Xanthomonas citri (ex Hasse) and X. phaseoli (ex Smith) to species and reclassification of all X. campestris pv. citri strains. International Journal of Systematic Bacteriology, 39(1):14-22

Golmohammadi M, Cubero J, Peñalver JM, Quesada JM, López MM, Llop P, 2007. Diagnosis of Xanthomonas axonopodis pv. citri, causal agent of citrus canker, in commercial fruits by isolation and PCR-based methods. Journal of Applied Microbiology, 103(6):2309-2315. http://www.blackwell-synergy.com/loi/jam

Goto M, 1992. Citrus canker. In: Kumer J, Chaube HS, Singh US, Mukhopadhyay AN, eds. Plant Diseases of International Importance, Vol. III, Diseases of Fruit Crops. New Jersey, USA: Prentice Hall.

Goto M, Tadauchi Y, Okabe N, 1979. Interaction between Xanthomonas citri and Erwinia herbicola in vitro and in vivo. Annals of the Phytopathological Society of Japan, 45(5):618-624

Goto M, Takahashi T, Messina MA, 1980. A comparative study of the strains of Xanthomonas campestris pv. citri isolated from citrus canker in Japan and cancrosis B in Argentina. Annals of the Phytopathological Society of Japan, 46(3):329-338

Grygiel P, Seny-Couty A, Hassani FA, Boyer C, Boyer K, Vernière C, Pruvost O, Hamza AA, 2014. First report of Xanthomonas citri pv. citri pathotype a causing Asiatic citrus canker in Grande Comore and Anjouan. Plant Disease, 98(12):1739-1740. http://apsjournals.apsnet.org/loi/pdis

Hartung JS, Daniel JF, Pruvost OP, 1993. Detection of Xanthomonas campestris pv. citri by the polymerase chain reaction method. Applied and Environmental Microbiology, 59:1143-1148.

Hartung JS, Pruvost OP, Villemot I, Alvarez A, 1996. Rapid and sensitive colorimetric detection of Xanthomonas axonopodis pv. citri by immunocapture and a nested-polymerase chain reaction assay. Phytopathology, 86(1):95-101; 38 ref.

Hasse CH, 1915. Pseudomonas citri, the cause of citrus canker. Journal of Agricultural Research, 4:97-100.

Hoarau J, Boyer C, Vital K, Chesneau T, Vernière C, Roux-Cuvelier M, Pruvost O, Moreau A, Hostachy B, Yahaya N, Abdoul-Karime AL, 2013. First report of Xanthomonas citri pv. citri - a causing Asiatic citrus canker in Mayotte. Plant Disease, 97(7):989. http://apsjournals.apsnet.org/loi/pdis

Holland DF, 1920. V. Generic index of the commoner forms of bacteria. In: Winslow CEA, Broadhurst J, Buchanan RE, Krumwiede Jr. C, Rogers LA, Smith GH, eds. The families and genera of the bacteria. Journal of Bacteriology, 5:191-229.

Ibrahim G, Bayaa B, 1989. Fungal, bacterial and nematological problems of citrus, grape and stone fruits in Arab countries. Arab Journal of Plant Protection, 7(2):190-197

IPPC, 2008. Update on citrus canker eradication program in Emerald, Queensland. IPPC Official Pest Report, No. AU-12/1. Rome, Italy: FAO. https://www.ippc.int/IPP/En/default

IPPC, 2009. Eradication of citrus canker from Australia. IPPC Official Pest Report, No. AU-18/1. Rome, Italy: FAO. https://www.ippc.int/IPP/En/default

IPPC, 2015. Eradication of citrus canker from Australia. IPPC Official Pest Report, No. AUS-18/2. Rome, Italy: FAO. https://www.ippc.int/

IPPC, 2018. Xanthomonas citri subsp citri (Citrus canker) in Northern Territory. IPPC Official Pest Report, No. GB-4/2. Rome, Italy: FAO. https://www.ippc.int/

Jehle RA, 1917. Susceptibility of non-citrus plants to Bacterium citri. Phytopathology, 7:339-344.

Jones DR, 1991. Successful eradication of citrus canker from Thursday Island. Australasian Plant Pathology, 20(3):89-91

Juhasz CC, Leduc A, Boyer C, Guérin F, Vernière C, Pruvost O, Wonni I, Ouedraogo L, 2013. First report of Xanthomonas citri pv. citri causing Asiatic citrus canker in Burkina Faso. Plant Disease, 97(12):1653. http://apsjournals.apsnet.org/loi/pdis

Kanamori H, Tsuyumu S, 1998. Comparison of nucleotide sequences of canker-forming and non-canker-forming pthA homologues in Xanthomonas campestris pv. citri. Annals of the Phytopathological Society of Japan, 64(5):462-470; 17 ref.

Kubicek QB, Civerolo EL, Bonde MR, Hartung JS, Peterson GL, 1989. Isozyme analysis of Xanthomonas campestris pv. citri. Phytopathology, 79(3):297-300

Kuo TT, Chiang CC, Chen SY, Lin JH, Kuo JL, 1994. A long lytic cycle in filamentous phage Cf1tv infecting Xanthomonas campestris pv. citri. Archives of Virology, 135(3-4):253-264

Lazo GR, Roffey R, Gabriel DW, 1987. Pathovars of Xanthomonas campestris are distinguishable by restriction fragment-length polymorphism. International Journal of Systematic Bacteriology, 37(3):214-221

Leduc A, Vernière C, Boyer C, Vital K, Pruvost O, Niang Y, Rey JY, 2011. First report of Xanthomonas citri pv. citri pathotype A causing Asiatic citrus canker on grapefruit and Mexican lime in Senegal. Plant Disease, 95(10):1311. http://apsjournals.apsnet.org/loi/pdis

Lee HA, 1918. Further data on the susceptibility of rutaceous plants to citrus-canker. Journal of Agricultural Research, 15:661-665.

Lim G, 1988. Plant diseases in Singapore. Singapore Journal of Primary Industries, 16(2, Supplement):12-29

Lou BH, Deng CL, Song YQ, Zhao XL, Wang MZ, Li XL, 2013. First report of Xanthomonas citri subsp. Citri pathotype a causing citrus canker on Nanfeng tangerine in Guangxi Province, China. Journal of Plant Pathology, 95(3):664. http://sipav.org/main/jpp/index.php/jpp/article/view/2977

Mavrodieva V, Levy L, Gabriel DW, 2004. Improved sampling methods for real-time polymerase chain reaction diagnosis of citrus canker from field samples. Phytopathology, 94(1):61-68.

Mirzaee MR, 2015. Citrus bacterial canker pustules are associated with leafminer galleries in Iran. Journal of Plant Pathology, 97(1):213. http://sipav.org/main/jpp/index.php/jpp/article/view/3274

Miyoshi T, Sawada H, Tachibana Y, Matsuda I, 1998. Detection of Xanthomonas campestris pv. citri by PCR using primers from the spacer region between the 16S and 23S rRNA genes. Annals of the Phytopathological Society of Japan, 64(4):249-254; 15 ref.

Mkervali VG, 1980. Diseases of citrus trees. Zashchita Rastenii, No.8:46-47

Namekata T, 1971. Estudos comparativos entre Xanthomonas citri (Hasse) Dow., agente causal do 'Cancro Citrico' e Xanthomonas citri (Hasse) Dow, NF, sp. aurantifolia, agente causal da 'Cancrose do Limoeiro Galego'. Tese apresentada a Escola Superior de Agricultura 'Luiz de Queiroz' para a obencao do Titulo de doutor em Agronomia.

NAPPO, 2013. Phytosanitary Alert System: Detection of Citrus Canker (Xanthomonas axonopodis pv. citri) in Louisiana. NAPPO. http://www.pestalert.org/oprDetail.cfm?oprID=550

NAPPO, 2014. Phytosanitary Alert System: Citrus Canker (Xanthomonas spp.) quarantine established in Louisiana. NAPPO. http://www.pestalert.org/oprDetail.cfm?oprID=576

NAPPO, 2016. Phytosanitary Alert System: Citrus Canker (Xanthomonas spp.) - APHIS establishes a quarantine in portions of Cameron County, Texas. NAPPO. http://www.pestalert.org/oprDetail.cfm?oprID=672

Ohta T, 1983. Interaction in vitro and in vivo between Xanthomonas camprestris pv. citri and antagonistic Pseudomonas sp. Annals of the Phytopathological Society of Japan, 49:308-315.

Okabe N, 1961. Studies on the lysogenic strains of Xanthomonas citri (Hasse) Dowson. Special Publication of College of Agriculture, Taiwan University, 10:61-73.

Pabitra Kalita, Bora LC, Bhagabati KN, 1996. Phylloplane microflora of citrus and their role in management of citrus canker. Indian Phytopathology, 49(3):234-237; 14 ref.

Pabitra Kalita, Bora LC, Bhagabati KN, 1997. Goat weed - a host of citrus canker (Xanthomonas campestris pv. citri). Journal of Mycology and Plant Pathology, 27(1):96-97; 3 ref.

Peltier GL, Frederich WJ, 1920. Relative susceptibility to citrus-canker of different species and hybrids of the genus Citrus, including the wild relatives. Journal of Agricultural Research, 19:339-362.

Peltier GL, Frederich WJ, 1924. Further studies on the relative susceptibility to citrus canker of different species and hybrids of the genus Citrus, including the wild relatives. Journal of Agricultural Research, 28:227-239.

Pruvost O, Gottwald TR, Brocherieux C, 1999. The effect of irrigation practices on the spatio-temporal increase of Asiatic citrus canker in simulated nursery plots in Reunion Island. European Journal of Plant Pathology, 105(1):23-37; 38 ref.

Ray, J. D., Taylor, R. K., Griffin, R. L., James, R. S., Dale, C., Ximines, A., Jones, L. M., 2017. Confirmation of Xanthomonas citri subsp. citri causing citrus canker in Timor-Leste. Australasian Plant Disease Notes 12(44). DOI 10.1007/s13314-017-0259-0.

Reddy MRS, 1997. Sources of resistance to bacterial canker in citrus. Journal of Mycology and Plant Pathology, 27:80-81.

Reddy MRS, Naidu PH, 1986. Bacterial canker on roots of acidlime (Citrus aurantifolia) a new report. Indian Phytopathology, 39(4):588-590

Rodriguez G S, Garza L JG, Stapleton JJ, Civerolo EL, 1985. Citrus bacteriosis in Mexico. Plant Disease, 69(9):808-810

Roistacher CN, Civerolo EL, 1989. Citrus bacterial canker disease of lime trees in the Maldive Islands. Plant Disease, 73(4):363-367

Schaad NC, Postnikova E, Lacy GH, Sechler A, Agarkova I, Stromberg PE, Stromberg VK, Vidavar AK, 2005. Emended classification of xanthomonad pathogens on citrus. Syst. Appl. Microbiol, 29:690-695.

Schotman CYL, 1989. Plant pests of quarantine importance to the Caribbean. RLAC-PROVEG, No. 21:80 pp.

Schoulties CL, Civerolo EL, Miller JW, Stall RE, Krass CJ, Poe SR, DuCharme EP, 1987. Citrus canker in Florida. Plant Disease, 71(5):388-395

Shigeta S, Nakata E, 1995. Bacterial brown spot of citrus caused by Pseudomonas syringae pv. syringae van Hall 1902. Annals of the Phytopathological Society of Japan, 61(2):150-157

Shiotani H, Ozaki K, Tsuyumu S, 2000. Specific interactions between Xanthomonas axonopodis pv. citri and pummelos. Phytopathology, in press.

Shivas RG, 1987. Citrus canker (Xanthomonas campestris pv. citri) and banana leaf rust (Uredo musp) at Christmas Island, Indian Ocean. Australasian Plant Pathology, 16(2):38-39

Stall RE, Civerolo EL, 1991. Research relating to the recent outbreak of citrus canker in Florida. Annual Review of Phytopathology, 29:399-420

Stall RE, Marco GM, Echenique BICde, 1982. Importance of mesophyll in mature-leaf resistance to cancrosis of citrus. Phytopathology, 72(8):1097-1100.

Stall RE, Miller JW, Marco GM, Canteros BI, 1981. International Society Citriculture Proceedings 1981, 1. 414-417.

Stall RE, Miller JW, Marco GM, Echenique BICde, 1980, publ. 1981. Population dynamics of Xanthomonas citri causing cancrosis of citrus in Argentina. Proceedings of the Florida State Horticultural Society, 93:10-14.

Stapleton JJ, Garza-Lopez JG, 1988. Epidemiology of a citrus leaf-spot disease in Colima, Mexico. Phytopathology, 78(4):440-443

Sun XA, Stall RE, Jones JB, Cubero J, Gottwald TR, Graham JH, Dixon WN, Schubert TS, Chaloux PH, Stromberg VK, Lacy GH, Sutton BD, 2004. Detection and characterization of a new strain of citrus canker bacteria from Key/Mexican lime and alemow in South Florida. Plant Disease, 88(11):1179-1188. http://www.apsnet.org

Unnamalai N, Gnanamanickam SS, 1984. Pseudomonas fluorescens is an antagonist to Xanthomonas citri (Hasse) Dye, the incitant of citrus canker. Current Science, India, 53(13):703-704

Vauterin L, Hoste B, Kersters K, Swings J, 1995. Reclassification of Xanthomonas. International Journal of Systematic Bacteriology, 45(3):472-489

Vauterin L, Swings J, Kersters K, 1991. Grouping of Xanthomonas campestris pathovars by SDS PAGE of proteins. Journal of General Microbiology, 137:1677-1687.

Verniere C, 1992. Bacterial canker of citrus (Xanthomonas campestris pv. citri). Epidemiological and ecological study on the island of Reunion. Fruits (Paris), 47(4):541-542

VerniFre C, Hartung JS, Pruvost OP, Civerolo EL, Alvarez AM, Maestri P, Luisetti J, 1998. Characterization of phenotypically distinct strains of Xanthomonas axonopodis pv. citri from Southwest Asia. European Journal of Plant Pathology, 104(5):477-487; 44 ref.

Wakimoto S, 1967. Some characteristics of citrus canker bacteria. Xanthomonas citri (Hasse) Dowson, and the related phages isolated from Japan. Annals of the Phytopathological Society of Japan, 33:301-310.

Wang ZhongKang, Luo HuaiHai, Shu ZhengYi, 1997. Application of DIA (dot immunobinding assay) for rapid detection of Xanthomonas axonopodis pv. citri. Journal of Southwest Agricultural University, 19(6):529-532; 7 ref.

Wang ZhongKang, Sun XianYun, Xia YuXian, Zhou ChangYong, Yin YouPing, 2004. Rapid detection of citrus bacterial canker disease (Xanthomonas axonopodis pv. citri) with polymerase chain reaction (PCR). Acta Phytopathologica Sinica, 34(1):14-20.

Wu WC, Chen TT, Wang YR, 1996. Characterization of five filamentous phages from Xanthomonas campestris pv. citri. Plant Pathology Bulletin, 5:1-14.

Wu WC, Lee ST, Kuo HF, Wang LY, 1993. Use of phages for identifying the citrus canker bacterium Xanthomonas campestris pv. citri in Taiwan. Plant Pathology, 42(3):389-395

Yang P, Vauterin L, Vancanneyt M, Swings J, Kersters K, 1993. Application of fatty acid methyl esters for the taxonomic analysis of the genus Xanthomonas. Systematic and Applied Microbiology, 16(1):47-71

Yik CP, 1988. Plant disease research and service, Primary Production Department. Singapore Journal of Primary Industries, 16(2, Supplement):30-37

Yin YouPing, Huang GuanJun, Zhao Yun, Liu Hong, Wang ZhongKang, 2007. Establishment and application of real time fluorescent PCR approaches for detection of Xanthomonas axonopodis pv. citri. Acta Phytophylacica Sinica, 34(6):607-613. http://www.wanfangdata.com.cn

Young JM, Bradbury JF, Gardan L, Gvozdyak RI, Stead DE, Takikawa Y, Vidaver AK, 1991. Comment on the reinstatement of Xanthomonas citri (ex Hasse 1915) Gabriel et al. 1989 and X. phaseoli (ex Smith 1897) Gabriel et al. 1989: indication of the need for minimal standards for the genus Xanthomonas. International Journal of Systematic Bacteriology, 41(1):172-177

Young JM, Saddler GS, Takikawa Y, Boer SHde, Vauterin L, Gardan L, Gvozdyak RI, Stead DE, 1996. Names of plant pathogenic bacteria 1864-1995. Review of Plant Pathology, 75(9):721-763; 10 pp. of ref.

Zombré C, Sankara P, Ouédraogo SL, Wonni I, Pruvost O, Boyer C, Vernière C, Adandonon A, Vayssières JF, Ahohuendo BC, 2015. First report of Xanthomonas citri pv. mangiferaeindicae causing Mango bacterial canker on Mangifera indica L. in Benin. Plant Disease, 99(12):1854. http://apsjournals.apsnet.org/loi/pdis

Distribution Maps