X. citri pv. aurantifolii pathotype B has a limited host range and predominantly affects C. x aurantifolia (Mexican lime). Other natural hosts have also been reported, such as C. lemon and C. maxima (= C. grandis, pummelo) when planted near infected Mexican lime (Schubert et al., 2001) as well as C. aurantium (sour orange); C. limonia (Rangpur lime); C. limettioides (sweet lime). C. sinensis (sweet orange) is considered to be a rare host (Rossetti, 1977; EFSA, 2014, 2019). As is the case for pathotypes A* and A^w  of X. citri pv. citri pathotype B does not infect C. paradisi.

X. citri pv. aurantifolii pathotype C has a narrow host range, mainly affecting C. x aurantifolia (Mexican lime). The rootstock, 'Swingle' citrumelo (Poncirus trifoliata x Citrus paradisi) is considered to be a rare host (Jaciani et al., 2009; Jaciani, 2012; Fonseca et al., 2019a). Upon artificial inoculation pathotype C strains infected C. limonia (Rangpur lime), C. latifolia (Persian lime), C. limon (lemon), C. paradisi (grapefruit), and C. reshni (Cleopatra mandarin) (Malavolta et al., 1984a, 1984b, 1987; Jaciani, 2012).

In artificial inoculation studies conducted on many ornamental Rutaceae with X. citri pv. aurantifolii B (strain JJ59) and C (strain JV596) pathotypes, Licciardello et al. (2022) confirmed the pathogenicity of both strains on Atalantia buxifolia, A. ceylanica and A. disticha, Balsamocitrus dawei, Citrus myrtifolia, Eremocitrus glauca and Citrus (Microcitrus) australasica, and of single strains on Citrus (Microcitrus) australis (pathotype B strain) and Fortunella japonica (pathotype C strain).

The host range of X. citri pv. aurantifolii pathotypes B and C is summarized and compared to X. citri pv. citri pathotypes A, A* and A^w in Table 2 below.

Table 2 – Host range of X. citri pv. citri pathotypes A, A* and A^w and X. citri pv. aurantifolii pathotypes B and C. Adapted from Fonseca et al., 2019b and using data from Gottwald et al. (1988; 1991), Jaciani et al. (2012), Schoulties et al. (1987), Schubert et al. (2001), Sun et al. (2004) and Vernière et al. (1998).

The geographical distribution of X. citri pv. aurantifolii has been reported to be restricted to Argentina, Paraguay and Uruguay (pathotype B) and Brazil (pathotype C) (Rossetti, 1977; Behlau et al., 2020) in South America. However, its current distribution is rather uncertain due to the fact that both pathotypes B and C have gradually been replaced by the more virulent X. citri pv. citri A pathotypes. X. citri pv. aurantifolii has not been recorded in the field since 1990 for pathotype B and since 2009 for pathotype C, see below.

X. citri pv. aurantifolii pathotype B

Cancrosis B or South American citrus canker was first observed in North-Eastern Argentina in 1923 in two provinces (Corrientes and Entre Rios), and later in Uruguay in 1936 and Paraguay in 1940 (Fawcett & Bitancourt, 1949; Canteros et al., 1985; Jaciani, 2012; Canteros et al., 2017; Patané et al., 2019). These strains disappeared in Argentina during 1978-90 after the introduction of the more virulent A strains in 1974 (Canteros et al., 1985; Goto et al., 1980). As far as it could be traced, the last B strain isolated in Argentina dates back to 1990 (Fonseca et al., 2019a). A similar situation has been observed in Uruguay and Paraguay (Russi et al., 2013; Licciardello et al., 2022).

X. citri pv. aurantifolii pathotype C

Limoneiro gallega (also called Galego acid lime necrosis, Galician lemon canker or cancrosis C) was observed for the first time in 1963 on Mexican lime in São Paulo, Brazil. There are two groups of C strains: brown pigmented, less virulent and non-pigmented, slightly more virulent (Schaad et al., 2006; Jaciani, 2012). A strain of X. citri pv. aurantifolii, very similar to the original C strains, but only pathogenic to the ‘Swingle’ citrumelo rootstock (C. paradisi × Poncirus trifoliata) was described in Severina (São Paulo State). This particular strain induced fewer lesions without erumpent margins, even in young leaves severely infested by the citrus leafminer Phyllocnistis citrella, that usually increases incidence (Jaciani et al., 2009; Kapp, 2011; Constantin et al., 2016). Pathotype C strains remained restricted to São Paulo state and were last reported in 2009 on C. aurantifolia (Dall’Acqua, 2011; Jaciani, 2012; Fonseca et al. 2019a). The fact that C strains have disappeared, or are at least of very limited occurrence, may be also supported by the fact that when citrus canker was observed in Rio Grande do Norte (previously not known to be affected) on Citrus aurantifolia (main host of X. citri pv. aurantifolii) on the cultivar Galego, only X. citri pv. citri was isolated (Amancio et al., 2021).

The distribution map below is rather uncertain, as no outbreaks of X. citri pv. aurantifolii have been reported in citrus orchards in South America since the 2000s. Absence has been confirmed in Argentina and Uruguay but not (yet) in São Paulo (Brazil) and Paraguay.

Biological data available in literature predominantly pertains to X. citri pv. citri, though it is generally considered that the life cycles of both X. citri pv. citri and X. citri pv. aurantifolii are largely similar (EFSA, 2014, 2019). Extensive descriptions of the biology (including pathogenesis) of X. citri pv. citri can be found in Gottwald et al. (2002); Ference et al. (2018); Caicedo and Villamizar (2021) Naqvi et al. (2022) and this has been summarized in the EPPO datasheet on X. citri pv.citri (EPPO, 2023a). Concerning X. citri pv. aurantifolii, it can thus be assumed that infection takes place through natural openings (stomata) and wounds created by grove maintenance operations, insects (e.g. Phyllocnistis citrella), or adverse climatic conditions (wind, storms). The bacterium most likely survives in canker lesions, which represent the most biologically significant inoculum source. Splash dispersal of the bacterium caused by rain or irrigation occurs over short distances and allows movement of the inoculum between adult trees or between plants in nurseries.

One of the reasons behind the disappearance of the X. citri pv. aurantifolii pathotype B strains (less virulent) after the introduction of the virulent X. citri pv. citri A strains into the affected areas, might be linked to the production of inhibitory compounds, as was demonstrated in vitro. Such compounds could be bacteriocins, although they have not been identified as such (Gochez, 2014; Canteros et al., 2017).

X. citri pv. aurantifolii pathotype C elicits a hypersensitivity response (HR) in specific citrus species, such as sweet orange and lemon (Brunings & Gabriel, 2003; Cernadas et al., 2008). Pathotype C has a narrow host range, unlike pathotype B strains which do not cause this HR and have a broader host range. An avirulence gene, avrGf2, was discovered in a pathotype C strain, responsible for eliciting a HR in grapefruit (C. x paradisi). This avrGf2 gene is related to avrGf1 found in X. citri pv. citri pathotype A^w strains, which also cause a HR in grapefruit. X. citri pv. aurantifolii pathotype B strains contain a transposon in avrGf2, rendering it non-functional. This may explain the broader host range of B strains (Gochez, 2014; Gochez et al., 2008, 2015 and 2017). Additional effector genes that differentiate X. citri pv. citri pathotype A and X. citri pv. aurantifolii pathotype B and C strains have been extensively described by Hajri et al. (2009); Moreira et al. (2010); Escalon et al. (2013); Ference et al. (2018) and Fonseca et al. (2019a). In summary, X. citri pv. aurantifolii pathotypes B and C lack several key genes important for pathogenesis when compared to X. citri pv. citri A pathotype. The higher virulence exhibited by X. citri pv. citri pathotype A strains, as well as their dominance in the field, can be explained by the presence and composition of the Type I and IV Secretion Systems and the Type IV pilus system (Dunger et al., 2014). This in comparison with the lower virulence of the X. citri pv. aurantifolii pathotype B and C strains, (Fonseca et al., 2019a).

Both pathotypes B and C of X. citri pv. aurantifolii differed when their genomes were compared with those of X. citri pv. citri pathotype A strains. For instance, the absence of the rpfN gene, critical for biofilm formation, in X. citri pv. aurantifolii pathotype B might account for its slow growth rate, also related to a low xanthan gum production and its dependence on glutamate in culture media as a carbon source. This is similar to the slow growth of another citrus pathogen, Xylella fastidiosa, which also lacks the rpfN gene (Moreira et al., 2010).

Correct identification of citrus bacterial canker pathogens and related pathogens causing Citrus bacterial spot is critical. Incorrect identification in the USA prompted the removal of thousands of productive citrus trees that were infected only with citrus bacterial spot, a mild disease caused by the related (now largely deregulated) X. euvesicatoria subsp. citrumelonis (formerly X. axonopodis pv. citrumelo, X. alfalfa pv. citrumelonis) Schaad et al. (2006).

Extensive description of symptoms on diverse hosts can also be found in Civerolo (1984); Goto (1992); Gottwald et al. (2002) and Graham et al. (2004).

Symptoms

The symptomatology of X. citri pv. aurantifolii is similar to that of X. citri pv. citri. These bacteria causing citrus canker infect all aerial parts of their hosts. When the disease is severe, defoliation and early fruit drop can occur, but no tree death has been reported.

[On leaves, lesions first appear on the lower leaf surface as pin-point oily spots due to water-soaking of the tissue. Later the lesions become visible on both epidermal surfaces as slightly raised pustules or blister-like eruptions. As lesions develop, they increase in size, the epidermis ruptures and the lesions become erumpent, spongy or corky. The pustules then darken and thicken into light tan-brown corky lesions, which are rough to the touch. Eventually, their centre becomes crater-like. Diagnostic symptoms are tissue hyperplasia resulting in cankers sometimes with water-soaked margins and yellow halos surrounding the lesions. Lesions with an atypical morphology (flat or blister-like spots) can be sometimes observed, especially in the case of late fruit infections or lesions on some resistant cultivars. In most hosts wilting is a common symptom of infection. The youngest leaves usually wilt first, with symptoms initially appearing at the warmest time of day. Wilting may be visible in only one stem, on one side of a plant or even sectoral in part of a leaf, depending where vascular infections occur (e.g., if they are restricted to sectors of stems and/or leaf petioles). Leaves may become bronzed or chlorotic and epinasty may occur. Wilting of the whole plant may follow rapidly if environmental conditions are favourable for pathogen growth. As the disease develops, a brown discoloration of the xylem vessels in the stem may be observed above the soil line and adventitious roots may develop. A creamy, slimy mass of bacteria exudes from vascular bundles when the stem is cut.]

[On twigs, the symptoms are similar: raised corky lesions initially surrounded by an oily or water-soaked margin. The lesions are generally irregularly shaped and may be sunken. Pustules may coalesce but chlorosis does not typically surround twig lesions. On removal of the corky layer, dark brown lesions are visible in the healthy green bark tissue. On highly susceptible citrus cultivars, diseased twigs can eventually show dieback symptoms.

Lesions on fruits can appear when they are still small and green and are similar to those on leaves, but tend to have more elevated margins and a sunken centre. These craters do not penetrate deep into the rind. Yellow chlorotic halos may or may not be present. Harvestable infected fruit have a reduced value or can be unmarketable depending on the severity of infection].

Symptoms of citrus canker on fruits may be confused with those of citrus scab (Elsinoe fawcetti), Phaeoramularia leaf and fruit spot disease (Phaeoramularia angolensis) or greasy spot (Mycosphaerella citri); Civerolo, 1984; Timmer et al., 2000; EFSA, 2014, 2019). Lesions caused by X. citri pv. aurantifolii appear slower and are generally smaller than those caused by X. citri pv. citri (A strains) (Goto et al., 1980; EFSA, 2014 and 2019; CABI, 2023).

Morphology

[X. citri pv. aurantifolii is morphologically similar to X. citri pv. citri. Bacterial cells are Gram-negative rods with a single polar flagellum, non-fluorescent, typically with no diffusible pigment produced on agar media (very rare exceptions of brownish-reddish pigment production occur). After ≥ 3 days of incubation at 28°C, colonies on agar plates are circular, convex, mucoid, shiny and yellow. Very occasionally, strains altered in xanthomonadin pigment production (and therefore cream-white to pale yellow) can be observed].

Strains of X. citri pv. aurantifolii produce single colonies on agar plates usually after 4-6 days. Occasionally pathotype C strains produce a brown diffusible pigment (Jaciani, 2012). In comparison colonies of X. citri pv. citri and X. euvesicatoria pv. citrumelonis grow more rapidly and usually appear after 2-3 days and 1-2 days, respectively (Schaad et al., 2005, 2006).

Detection, identification and inspection methods

Canteros et al. (1985) developed an elective medium for isolation and cultivation of X. citri pv. aurantifolii pathotype B strains. This elective media should contain Difo purified agar as base, as other agars failed to give satisfactory growth.

Serological tests using polyclonal or monoclonal antibodies have been previously developed and can detect both X. citri pv. citri and X. citri pv. aurantifolii (Namekata & Oliveira, 1972; Civerolo & Fan, 1982; Alvarez et al., 1991). However, monoclonal antibodies raised against X. citri pv. citri failed to react with some pathotype A* strains (Vernière et al., 1998) and could cross-react with unrelated xanthomonads (Alvarez et al., 1991). Moreover, enzyme-linked immunosorbent assays (ELISAs) are inadequate for detecting low bacterial populations but could be used for symptomatic material (EFSA, 2014, 2019).

Discriminative physiological and biochemical tests for have been described by Goto et al. (1980), Vernière et al. (1991 and 1993) and Schaad et al. (2005, 2006). Strains of X. citri pv. citri are susceptible to bacteriophage CP1 and CP2 whereas those of X. citri pv. aurantifolii are not (Goto et al., 1980; Schaad et al., 2006, citing the thesis of Namekata, 1971).

Multilocus sequence analysis (MLSA), using e.g., atpD, dnaK and fusA genes can reliably differentiate between X. citri pv. citri and X. citri pv. aurantifolii pathotype B and C (Bui Thi Ngoc et al., 2010; Dall’Acqua, 2011). Conventional PCR and real-time PCR primers that discriminate between X. citri pv. citri and X. citri pv. aurantifolii pathotype B and C have been described by Cubero & Graham (2002, 2005); Delcourt et al. (2013); Yu et al. (2012, 2017); Fonseca et al. (2019b); Robène et al. (2020); Yasuhara-Bell et al. (2023).

Strains of X. citri pv. citri are susceptible to bacteriophage CP1 and CP2 whereas those of X. citri pv. aurantifolii are not (Goto et al., 1980; Schaad et al., 2006, citing the thesis of Namekata (1971). Destefano & Rodrigues (2002) found that pigment producing C strains did not differ in 16S-23S intergenic region sequences and in pathogenicity, however in other studies (Nociti et al., 2006; Jaciani et al., 2012) pigment producing strains were less virulent on C. x aurantifolia than non-pigmented strains and they could be discriminated by ERIC-PCR (Jaciani et al., 2012).

Details about presumptive diagnosis with rapid tests, detection and identification methods (including methods for extraction of bacterial cells and DNA), biochemical, serological and molecular and pathogenicity tests (using inoculation of bean plantlets or hilum injury/seed inoculation) for latent and symptomatic infected material, flow chart, culture media, chemicals and reference material) are provided in the EPPO Standard PM 7/44 Xanthomonas citri pv. citri and Xanthomonas citri pv.  aurantifolii (EPPO, 2023b) and IPPC Diagnostic protocol DP 6 (IPPC, 2016).

As is the case for X. citri pv. citri, X. citri pv.  aurantifolii can be spread by the movement of contaminated plant propagative material, agricultural equipment, or clothes used for grove/nursery maintenance operations (Graham et al., 2004). Seven significant introduction pathways were identified and evaluated by the EFSA Plant Health Panel (EFSA, 2014, 2019):

1. Citrus fruit, commercial trade
2. Citrus fruit and/or leaves import by passenger traffic
3. Citrus plants for planting, commercial trade
4. Citrus plants for planting import by passenger traffic
5. Ornamental rutaceous plants for planting, commercial trade
6. Ornamental rutaceous plants for planting import by passenger traffic
7. Citrus and rutaceous leaves and twigs, commercial trade

Economic impact

Together with ‘Candidatus Liberibacter spp.’ (the causal agents of citrus huanglongbing) and Citrus tristeza virus, citrus canker is one of the main phytosanitary threats for citrus industries worldwide. Citrus canker has had and still has serious direct and indirect economic impacts. Direct impacts included alteration of fruit quality and yield (due to early fruit drop), the severity of the effect being influenced by the host species, the bacterial strain and the environmental conditions. Indirect impacts include restricted access to fruit export markets and undesirable consequences of chemical treatments.

However, due to its generally low virulence and restricted host range, easy control by copper containing bactericides and the replacement of X. citri pv. aurantifolii by the more virulent strains of X. citri pv. citri in South America, the current impact of X. citri pv. aurantifolii in areas where it might still be present is currently very low, if not nil. In Argentina, where B strains occurred for 40 years only in a small area with little impact, disappearing and replaced by pathotype A strains around 1990 (Goto et al., 1980; Canteros et al., 1985; Jaciani et al., 2009; Kapp, 2011; Jaciani, 2012; Canteros et al., 2017). Nociti et al. (2006) described the occurrence of pathotype C as restricted to a few municipalities in the state of São Paulo, Brazil only, without causing significant economic damage.

Control

As explained in the EPPO datasheet on X. citri pv. citri (EPPO, 2023a), the control strategy against citrus canker is based on integrated pest management (IPM), which aims to reduce the rate of infection and spread of the disease, and attempt to keep it below economically damaging levels. IPM combines several control options such as (i) the production of healthy citrus nursery plants for new grove establishment through certified programs, (ii) the recurrent physical elimination of inoculum sources, (iii) the avoidance of grove/nursey maintenance operations when the plant canopy is wet, (iv) the use of cultural practices minimizing infection and spread including general prophylactic measures applied to citrus production sites during grove/nursery maintenance operations, rootstocks controlling high tree vigour, drip irrigation, efficient windbreaks, preventive application of bactericides timed at host susceptibility peaks (most often using copper-based compounds), disinfection of agricultural equipment and (v) the use of partially resistant citrus lines or molecules inducing plant defence. The integrated approach described above, was and is primarily achieved for X. citri pv. citri but it would manage and control X. citri pv. aurantifolii (Leite & Mohan, 1990; Dewdney & Johnson, 2023). B strains can effectively be controlled by copper containing bactericides (Canteros et al., 2017).

For a comprehensive understanding of the various control measures and possibilities in managing citrus canker, recent publications by Gottwald et al. (2002), Das (2003), de Carvalho et al. (2015), and Ference et al. (2018) and EFSA (2014, 2019) offer valuable insights.

Phytosanitary risk

Bacteria associated with citrus canker were estimated to be likely to establish and spread in the European Union if reaching susceptible hosts (EFSA, 2014; 2019). Citrus canker is a risk for the EPPO region where citrus is widely commercially cultivated and largely available in public and private non-commercial areas. Once established in a region, its spread would be difficult to control. Therefore, the best risk reduction options to be taken are the ones aiming to maintain its absence.

Long-distance spread of citrus canker can occur through the movement of diseased, latently infected or contaminated propagating material (e.g., budwood, rootstock, seedlings and budded trees, and also as its trade is increasing ornamental host plants) and fruits (Graham et al., 2004; Golmohammadi et al., 2007; EFSA, 2014, 2019).

Asiatic bacterial canker, particularly caused by X. citri pv. citri pathotype A, presents the most significant risk for the European region, primarily concentrated around the Mediterranean Basin. This risk is considerably higher compared to the risk posed by X. citri pv. aurantifolii. Pathotype B strains have not been observed since 1990 and cause only a mild disease and the pathotype C strains, not observed after 2009, are even of a lesser concern, because C. aurantifolia is hardly cultivated in the Mediterranean region (EFSA, 2014, 2019). It is worth noting that the citrus leaf miner Phyllocnystis citrella, that can exacerbate the disease and facilitate its spread, is widely distributed in the citrus-producing areas of the Mediterranean Basin. Nonetheless there is at present no citrus bacterial canker reported in the EPPO region, and precautionary phytosanitary measures should be implemented for all forms of X. citri as outlined in this datasheet (Timpanaro et al., 2020, 2021). This proactive approach aims to prevent and mitigate potential outbreaks of citrus bacterial canker within the EPPO region.

It has been shown that once transferred to a suitable host, citrus canker can only be controlled with strong phytosanitary measures. Eradication has been attempted against X. citri pv. citri with different results, it was successful in Australia, unsuccessful in the USA for example (Gottwald et al., 2001). Eradication seems a feasible option for the less aggressive X. citri pv. aurantifolii, should the latter be introduced into new areas. As a general remark, successful eradication requires efficient surveillance systems as well as quick and appropriate management measures on diseased and exposed trees.

Considering the severity of citrus canker, EPPO countries are recommended to prohibit the importation of citrus plants for planting and cut branches from areas or countries where the disease occurs. For the EU, the current phytosanitary measures (EU Regulation 2019/2072, 2019) are targeting both X. citri pv. citri and X. citri pv. aurantifolii. In summary, these measures include a prohibition to import plants for planting of Citrus, Fortunella and Poncirus from third countries. Plants for planting of Citrus, Naringi and Swinglea can only be imported from pest-free third countries or pest-free areas. Imports of fruit are also subject to restrictions, such as fruit should be free from peduncles and leaves and should originate pest-free third countries, pest-free areas or pest-free places of production. These measures have been described in more details in the EPPO datasheet on X. citri pv. citri (EPPO, 2023a).

[National regulatory control systems are recommended to EPPO countries for the surveillance, early detection and eradication of citrus canker, and for containment measures to prevent spread during eradication. Efficient and regular surveillance actions are recommended as they are key in enabling early detection and prompt implementation of eradication measures. In citrus-growing areas, inspectors, industry experts and workers should be trained to recognize citrus canker symptoms and host plants. Countries should have access to laboratories with trained diagnosticians, experienced and competent in the identification of the pathogen according the EPPO PM 7/44 Diagnostic Protocol (EPPO, 2023b)].

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This datasheet was extensively revised in 2024 by Dr Jaap D. Janse, independent consultant, bacteriologist. His valuable contribution is gratefully acknowledged.

This datasheet was first published online in 2023. It is maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.