Xanthomonas citri
(citrus canker)

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.  

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).

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

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).

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.

General

• Research model

Genetic importance

• Test organisms (for pests and diseases)

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.

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).

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.

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.

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).