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Citrus junos as a host of citrus bacterial canker

Abstract Following a request from the European Commission, the European Food Safety Authority (EFSA) Plant Health (PLH) Panel analysed a dossier submitted by the Japanese authorities in order to clarify the host status of Citrus junos with regard to Xanthomonas citri pv. citri and Xanthomonas citri pv. aurantifolii, causal agents of citrus bacterial canker, and to indicate whether C. junos fruit could represent a pathway for the introduction of citrus bacterial canker into the European Union. In a previous opinion in the year 2014, the EFSA PLH Panel concluded that commercial fresh citrus fruit is generally pathway and that no commercially important Citrus species or variety can be considered as immune to citrus bacterial canker. In the current assessment, the EFSA PLH Panel analysed the two scientific papers provided by the Japanese authorities, as well as 16 additional papers identified through a systematic literature review. The PLH Panel considered that the conclusions of its previous opinion remain valid and that convergent lines of evidence provide sufficient demonstration that C. junos is a host of X. citri pv. citri and X. citri pv. aurantifolii. Therefore, there is no reason to consider the C. junos fruit differently from other citrus species. Consequently, the assessment of the general citrus fruit pathway from the 2014 opinion still applies. Uncertainties on these conclusions are a result of the scarce scientific evidence published on this subject in addition to the methodological and reporting limitations of the published papers.

Background and Terms of Reference as provided by the requestor The European Food Safety Authority (EFSA) is requested, pursuant to Article 22(5.b) and Article 29 (1) of Regulation (EC) No 178/2002 1 , to provide a scientific opinion in the field of plant health.
The Japanese phytosanitary authorities consider that Citrus junos is not a host of Xanthomonas citri pv. citri and Xanthomonas citri pv. aurantifolii or citrus bacterial canker. Therefore, Japan has requested that C. junos fruits are excluded from the specific requirements listed in Point 16.2 of Annex IVAI of the Directive 2000/29/EC in relation to citrus bacterial canker. Japan has provided the Commission with two scientific papers on this issue, which are attached for consideration: • Koizumi M, 1979. Ultrastructural changes in susceptible and resistant plants of Citrus following artificial inoculation with Xanthomonas citri (Hasse) Dowson. Annals of the Phytopathological Society of Japan, 45, 635-644 (Appendix 1 of the request); • Koizumi M and Kuhara S, 1982. Evaluation of Citrus plants for resistance to bacterial canker disease in relation to the lesion extension. Bulletin of the Fruit Trees Research Station of Japan D, 4, 73-92 (Appendix 2 of the request) Therefore, EFSA is requested to prepare a scientific opinion to clarify the host status of C. junos with regard to X. citri pv. citri and X. citri pv. aurantifolii or citrus bacterial canker, and to indicate whether C. junos fruits could represent a pathway for the introduction of citrus bacterial canker into the Union.
EFSA have previously published several opinions related to citrus bacterial canker (EFSA, 2007;EFSA PLH Panel 2011, 2013, 2014. Commercial fresh fruit in general (for direct consumption or for industrial uses) is shown to be a pathway.
Directive 2000/29/EC considers 'Xanthomonas campestris (all strains pathogenic to Citrus)' in its present wording. Changes in taxonomy led to reclassification of that group of bacteria that are now separated as X. citri pv. citri and X. citri pv. aurantifolii. This does not change the conclusions of previously issued EFSA opinions in anyway because those taxonomic evolutions were already taken into consideration.
In directive 2000/29/EC, the term 'fruit of Citrus' includes fruit from plant genera Citrus (to which C. junos belongs), Poncirus and Fortunella. That list shall be expanded to genera Microcitrus, Swinglea, Naringi and their hybrids (see later), as already indicated in the previous EFSA opinion (EFSA PLH Panel, 2014). In the present opinion, 'fruit of Citrus' means (except if specified differently) fruit from a plant belonging to the genera Citrus, Fortunella, Poncirus, Microcitrus, Swinglea, Naringi and their hybrids. Import into, and circulation within, the Community of fruit from all plants belonging to genera Citrus, Fortunella, Poncirus and their hybrids, is regulated by Directive 2000/29/EC, which prescribes measures to be applied by exporting countries in order to mitigate the risk of introduction into the European Union (EU) of X. citri pv. citri and X. citri pv. aurantifolii. The import of fruit from C. junos shall therefore be in accordance with regulation.
The current legislation is presented in Appendix A of this opinion. Given the request, in this opinion, the Plant Health (PLH) Panel considers only the fresh citrus fruit trade pathway (citrus fruit, commercial trade as assessed in the previous opinion under pathway I, (EFSA PLH Panel, 2014). Other pathways, including citrus fruit and/or leaves import by passenger traffic, referred as pathway II in the previous EFSA opinion (EFSA PLH Panel, 2014), are not taken into consideration.

2.
Data and methodologies

Data
Search strategies were undertaken in order to identify scientific literature on C. junos and citrus bacterial canker or Xanthomonas. It has been noted that the specific species C. junos might not be present in the title and/or abstract of the article but only in the full text. Therefore, two searches were combined in the main bibliographic databases: a tailored search to identify C. junos and Xanthomonas or citrus canker; a general search to identify studies including information of Citrus species and resistance or tolerance to Xanthomonas or citrus canker.
The following databases were searched (Table 1): Additional searches, limited to retrieve documents on C. junos and Xanthomonas or citrus canker, were run in Google Scholar via Publish or Perish version 4 software.
The searches were run on 7 March 2017. No language, date or document type restrictions were applied in the search strings. The search strategies were adapted according to the configuration of each resource of information. Full search strategies are listed in Appendix B.
The outputs from all the databases except AGRICOLA were exported to an Endnote x8 file and the duplicate results were removed. AGRICOLA outputs were sent via email and the results not yet identified in other databases were added manually into EndNote x8. The final number of results of the database searches after removing duplicates was 238.
The results of the searches in Google Scholar were exported in a different EndNote x8 file. The duplicate results of the different queries were removed; results already identified in the databases searches were also removed. The final number of unique results identified in Google Scholar after deduplication was 140.

Methodologies
The assessment was conducted in line with the principles described in the EFSA Guidance on transparency in the scientific aspects of risk assessment (EFSA, 2009). The present document is structured according to the Guidance on the structure and content of EFSA scientific opinions and statements (EFSA Scientific Committee, 2014).
For a thorough evaluation of C. junos as a possible host of X. citri pv. citri or X. citri pv. aurantifolii, as well as to indicate whether C. junos fruits could represent a pathway for citrus bacterial canker introduction into the Union, the Panel considered all the data and information provided by the Japanese authorities, the previous EFSA opinions on the topic (EFSA PLH Panel, 2014) and relevant literature.

3.
Assessment of C. junos as a host for X. citri pv. citri and X. citri pv. aurantifolii

Background information
Citrus junos Sieb ex Tanaka (Citrus ichangensis x Citrus reticulata var. austere), called Yuzu in Japanese, Yuja in Korean and Xiangch eng in Chinese, is a citrus species native to China (Ferguson and Grafton-Cardwell, 2014). It is mostly cultivated in South Korea and Japan where fresh fruits are used for juice, traditionally for preparing vinegar and seasoning. Yuzu essential oil is increasingly used in food, beverages, cosmetics, perfumery and aromatherapy (Sawamura and Lan-Phi, 2010). In Japan and China, several varieties are recorded and have been studied for the variation of the volatile constituents of their cold-pressed peel oil (Sawamura and Lan-Phi, 2010). There is also an emerging demand outside of Asia for yuzu fresh fruit.
Although C. junos is considered to originate from China, Japan and South Korea are considered as the main C. junos producing areas. In 2014, yuzu acreage in Japan was evaluated as 2,216 ha (3% of the Japanese citrus acreage) (Omura and Shimada, 2016). Kim et al. (2015) report an area of 2,237 ha equivalent to a production of 19,127 metric tonnes in South Korea. Presently, at least one Japanese company is exporting C. junos fresh fruits to Europe (Sasu Olivier Derenne, online). There are some indications about EU importation of C. junos from California. C. junos fruits are also produced in Spain (Old, 2016;Stoffels, online).
There is no precise data on quantity of C. junos importation into the EU. In the import statistical data in EUROSTAT (online), only the main citrus species are individually reported (such as 'orange', 'mandarins', 'grapefruit', 'lemons', 'limes'); therefore, data on C. junos are not presented as such but are comprised within the term 'Citrus other'.
EFSA issued a scientific opinion on the risk to plant health of X. citri pv. citri and X. citri pv. aurantifolii for the EU territory in 2014 (EFSA PLH Panel, 2014). Previous EFSA opinions also considered citrus bacterial canker and the fruit pathway (EFSA, 2007;EFSA PLH Panel 2011, 2013. The latest opinion considered in detail the commercial fresh fruits pathway, with the following main conclusions (EFSA PLH Panel, 2014): • 'Xanthomonas citri pv. citri and X. citri pv. aurantifolii are likely to be associated with citrus fruit, with a medium uncertainty because of (i) incomplete data on the presence of X. citri pv. citri or X. citri pv. aurantifolii strains in the country at origin; (ii) the variation in cultivar susceptibility; (iii) the differences in the pest management measures set up according to the countries exporting citrus fruit; and (iv) differences in packinghouse operational procedures; • Xanthomonas citri pv. citri and X. citri pv. aurantifolii are very likely to survive during transport and storage of fruit, with a low uncertainty; • Xanthomonas citri pv. citri and X. citri pv. aurantifolii are very likely to survive the existing pest management procedures, with a low level of uncertainty; • the probability of transfer to a suitable host is unlikely, but with a high uncertainty because of (i) the paucity of literature and (ii) the lack of extensive information on transfer under natural conditions'.
Considering consequences of introduction of those bacteria into the Community, the previous EFSA opinion (EFSA PLH Panel, 2014) stated that: • 'all citrus-growing areas in the EU can be considered as the endangered area; • where citrus bacterial canker occurs, the quantity and quality of the fruit production is impaired owing to defoliation, premature fruit drop, dieback, blemishes on fruit, and general tree decline; • once introduced, citrus bacterial canker cannot be controlled without regulation, although those measures hardly permit to control the disease'.
Considering risk reduction options, with regard to the already implemented measures for the fruit pathway (including measures that may help to keep fruit free from bacteria in the field) and the request from Japan, the previous EFSA opinion (EFSA PLH Panel, 2014) reached the conclusions that: • 'the effectiveness of the prohibition of leaves and peduncles is rated as low, with a very high technical feasibility and a low uncertainty; • the prohibition of fruit from certain plant genotypes (which means the authorisation for others) appears not to be applicable; • the effectiveness of guarantying pest freedom of consignments through inspections and testing is rated as moderate, with moderate technical feasibility and medium uncertainty; • the effectiveness of measures taken while preparing the consignments in the country of origin (cleaning of harvesting material, separate facilities for fruit coming from known healthy fields, culling and cleaning of fruit, storage at cold temperatures, etc.) is rated as moderate, with very high technical feasibility and medium uncertainty; • the effectiveness of specific treatments of fruit to reduce pest prevalence in consignments is rated as moderate, with very high technical feasibility and low uncertainty; • the effectiveness of integrated pest management procedures in citrus growing fields and their environment is rated as moderate, with very high technical feasibility and low uncertainty; • the use of resistant or less susceptible varieties, as claimed by the Japanese authorities for C. junos (providing it would be proved that that species is resistant or less susceptible), is rated high to moderate, with a low technical feasibility and low uncertainty; • the effectiveness of limiting import to fruit originating from pest-free areas is rated as very high, with a high technical feasibility and medium uncertainty; • the effectiveness of limiting import to fruit originating from pest-free production places is rated as high, with a high technical feasibility and high uncertainty; • the effectiveness of systems approaches integrating individual risk reduction options is rated as moderate, with high technical feasibility and medium uncertainty'.
Some other risk reduction options, not implemented in EU regulation and not included into the request from the Commission for this opinion, were nevertheless evaluated: • 'the effectiveness of restriction on distribution of fruit within the EU is rated as high, with low technical feasibility and low uncertainty; • the effectiveness of restriction on end use of fruit is rated as high, with high (for nonendangered areas) or low (for endangered areas) technical feasibility, as a result of difficulties in implementation, with low uncertainty'.
Relying on those conclusions from the previous EFSA opinion (EFSA PLH Panel, 2014), fresh fruit of Citrus sp. was clearly considered as a pathway for X. citri pv. citri and X. citri pv. aurantifolii.

Assessment of data provided by the Japanese authorities
To support their request to exclude C. junos from the specific requirements listed in Point 16.2 of Annex IV Part A Section I of the Directive 2000/29/EC in relation to citrus bacterial canker, the Japanese phytosanitory authorities provided two papers by Koizumi (1979), and Koizumi and Kuhara (1982).
The two studies refer to previous work published by Koizumi, in a subsequent way. First, Koizumi developed a way of assessing the bacterial multiplication using serial dilutions of lesions and pin-prick inoculation on a susceptible host (Koizumi, 1971). In C. junos, the bacterial multiplication in attached, pin-pricked inoculated, leaves was evaluated under controlled conditions (glasshouse) at 21°C, to reach levels of 10 6 cells per lesion, as determined by the needle-prick inoculation of tenfold dilutions from lesion crushes (Koizumi, 1976). Water-soaked lesions appeared 7 days post-inoculation on C. junos, whereas they were recorded 5 days post-inoculation in hosts that are more susceptible. Finally, the level of bacterial multiplication was also evaluated over a 4-month period using either the needle-prick inoculation method (Koizumi, 1971(Koizumi, , 1977 or an indirect detection/enumeration technique based on CP1 citriphage multiplication from lesion extracts (Koizumi et al., 1966;Koizumi, 1969aKoizumi, ,b, 1972. Indirect X. citri pv. citri population size estimates by this citriphage technique from symptoms on yuzu were similar to those on other resistant hosts; for example, Ponkan mandarin (C. reticulata) or calamondin (Citrus madurensis) (Koizumi and Kuhara, 1982).
The paper by Koizumi (1979) is based on macroscopical and ultrastructural observations following leaf infiltration (2-year-old Citrus spp. potted plants) by a hypodermic syringae of a high concentration of inoculum (10 9 cells/mL) of the virulent isolate QN7501 of X. citri (name of the bacterium at the time this paper was publishedsee Section 1.2), performed under controlled conditions at 20°C.
The author states that: 'In the resistant C. junos leaves, ultrastructural changes were similar to those observed on the susceptible host until 3 days after inoculation. Four days after inoculation, however, the liberated fibrils became concentrated around the bacterial cell and filled the intercellular spaces. These enveloped bacteria became electron-dense indicating deterioration of the cells. By 6 days after inoculation, the spaces between separated plasmalemma and the cell wall were filled with numerous granules mixed with small vesicles and the cytoplasm was markedly electron-dense. This was associated with necrosis or a hypersensitive reaction'. The authors stress also the fact that less hypertrophy and translucence were observed on the symptoms of Yuzu plants compared to the Natsudaidai susceptible ones.
Although the paper does not provide the reader with detailed information on the inoculation conditions (no indication about the precise line or variety of C. junos used, nor about any different night-day regime), it is reported that the experiments were conducted at 20°C, whereas the optimum temperature for X. citri is between 25°C and 30°C (Dalla Pria et al., 2006).
The experiment was performed with a single isolate (QN5701), for which no detailed information is available. Kitagawa et al. (1992) provide with the information that the strain was isolated from the Kuchinotsu fruit tree research station (Nagasaki prefecture) from sweet orange (Citrus sinensis).
Finally, the symptoms described by Koizumi (tissue hypertrophy and watersoaking) appear to be rather different from those observed following a true hypersensitive reaction on non-host plants as stated by Dunger et al. (2005).
In the second paper provided by the Japanese authorities, Koizumi and Kuhara (1982) investigated the susceptibility of citrus lines following (i) outdoor artificial inoculations (C. junos included) and (ii) natural infections in field conditions (C. junos not included). The authors classified C. junos as class F (lowest susceptibility) together with calamondin on the basis of a lack of bacteriophage CP1 multiplication (used as an estimator of the density of Xanthomonas cells present in the lesion) from lesions produced from inoculations on C. junos. The authors did not clearly report the morphology of the lesions assayed from C. junos but mention lesions sized between 0.6 and 0.8 mm 2 on potted plants placed in the field. The reported field studies were performed between 1968 and 1970. The authors provide a table classifying the different resistance levels, probably also based on the former paper by Koizumi (1978), which itself is based on field observations made by three different observers in 1973 at Kuchinotsu Fruit Tree Research Station, when the disease was 'severely prevalent'.

Assessment of additional literature data
Based on an extensive literature search, 16 additional peer-reviewed papers provide data on C. junos as a host for citrus bacterial canker. Most of these papers focus on X. citri pv. citri, except for two papers dealing with X. citri pv. aurantifolii (Goto et al., 1980;Malavolta et al., 1984).
An overview of additional literature data is provided in Table 2. From the review of these additional papers, the PLH Panel emphasises that: • Citrus junos inoculated with X. citri pv. citri exhibits typical canker-like lesions, although the extent of watersoaking, tissue hypertrophy and lesion increase in size was less than those observed on susceptible cultivars. Population sizes in leaf lesions as high as 1 9 10 6 X. citri pv. citri per lesion were detected, although this experiment was conducted at a temperature suboptimal for X. citri pv. citri multiplication (Koizumi, 1976). Similarly, natural infections of C. junos in production groves were reported from Japan and X. citri pv. citri strains were readily isolated from these lesions (Obata, 1974). C. junos is therefore considered to be a host of X. citri pv. citri (low uncertainty).
• Although very little literature is available (which leads to high uncertainty), C. junos can be considered as a putative host of X. citri pv. aurantifolii. Two major groups of strains (i.e. referred to as pathotypes B and C) have been reported within this pathovar (EFSA PLH Panel, 2014). Goto et al. (1980)  • Analysed papers suggest that C. junos exhibits partial resistance but no immunity to X. citri pv.
citri. A single exception listed yuzu as highly susceptible to X. citri pv. citri (Amaral et al., 2010) but assignation of the assayed cultivar to C. junos was considered doubtful (personal communication, 10 March 2017, Dr S ergio Alves de Carvalho, Centro de Citricultura Sylvio Moreira -Instituto Agronômico, Cordeir opolis, SP, Brazil; replying to a specific query with regard to susceptibility rating of yuzu to Xanthomonas citri subsp. citri).
• Most papers investigating the susceptibility of C. junos to X. citri pv. citri used a single, genetically uncharacterised strain for pathogenicity assays. The genetic structure of X. citri pv. citri in C. junos production areas is not precisely known. Shiotani et al. (2007) showed the occurrence of genetic and pathological diversity among Japanese strains of X. citri pv. citri in relation to their TALE (transcription activator-like effector) gene content, yielding a differential susceptibility of some strains to some pummelo (C. maxima) cultivars. C. junos has, to our knowledge, not been challenged with strains representative of such a diversity. In addition to the distinct experimental procedures used for characterising levels of susceptibility of citrus lines to X. citri pv. citri, the lack of fully congruent conclusions (Table 2) may be a result of such pathological diversity.
• Most papers investigating the susceptibility of C. junos to X. citri pv. citri used a single, uncharacterised C. junos accession for pathogenicity assays. A single study (Deng et al., 2010), investigating the susceptibility level of five Chinese C. junos accessions, suggested that levels of partial resistance are cultivar-dependent.
Studies presenting a pathological characterisation based on a single host cultivar/strain interaction cannot be viewed as a final proof of resistance of C. junos. Based on available literature review, the PLH Panel concludes that the studies reviewed herein suggest an immunity of C. junos solely towards X. citri pv. aurantifolii pathotype C and rather suggest that C. junos is partially resistant to X. citri pv. citri. Based on the levels of partial resistance provided in table 4 of the scientific opinion on the risk to plant health of Xanthomonas citri pv. citri and Xanthomonas citri pv. aurantifolii for the EU territory (EFSA PLH Panel, 2014), C. junos may be classified as being resistant to highly resistant. This is because the only study assessing several yuzu cultivars suggests cultivar-dependent levels of partial resistance in C. junos. Such citrus cultivars/species that are classified as resistant or highly resistant are known to display natural infections when exposed to high inoculum pressure (e.g. the presence of highly diseased plants in the vicinity).

Uncertainties
The literature available on C. junos as a host for citrus bacterial canker is very limited (Table 2). Often, the data provided are given for a single uncharacterised C. junos accession (Table 2), although different accessions are well known and characterised (Rahman et al., 2001). A single study (Deng et al., 2010), investigating the susceptibility level of five Chinese C. junos accessions, suggested that levels of partial resistance are cultivar-dependent. Additionally, Citrus spp. are often grafted in www.efsa.europa.eu/efsajournal commercial orchards and rootstock. Such a practice can significantly modify the susceptibility of the grafted cultivar to the aboveground pest (Bruessow et al., 2010;Agut et al., 2014Agut et al., , 2016, including X. citri pv. citri, for which a higher disease severity was observed for rootstock associations conferring a higher tree vigour (Agostini et al., 1985).
Most papers investigating the susceptibility of C. junos to X. citri pv. citri used a single, genetically uncharacterised strain for pathogenicity assays.
Additional pathogenicity data would be useful for confirming the non-host status of X. citri pv. aurantifolii pathotype C suggested by Malavolta et al. (1984).
There is also a lack of quantitative data on the bacterial population size in citrus bacterial canker lesions found on C. junos, both from naturally occurring infections or following inoculations. Only five papers report quantitative assessment over the 16 available, and often by the use of indirect assessment methodologies (using phage population as quantitative estimator, immunoassay, indirect needle-prick inoculation of serial dilutions obtained from lesion crush), which are considered as being less suitable for the estimation of small bacterial population. The use of bacteriophages for estimating the bacterial cell densities was established in the 1960s in Japan. Such an indirect enumeration technique only provides an approximate estimation of X. citri pv. citri population densities. Obata (1974) stated that, over multiplication cycles, X. citri pv. citri subpopulations can switch towards a citriphage-resistant phenotype, further questioning the reliability of this technique for quantification of population densities.
No data assessing the susceptibility level of C. junos fruits are presently available. There is also a lack of data on C. junos production outside South Korea and Japan.

Conclusions
In answer to a request of the European Commission, the EFSA PLH Panel performed an analysis of the two scientific papers submitted by the Japanese authorities and of additional relevant scientific literature, aiming to reach a conclusion on the host status of C. junos to X. citri pv. citri and X. citri pv. aurantifolii. Taking into account the current lack of data on C. junos fruit as a pathway, the PLH Panel also checked that the conclusions of its previous opinion (EFSA PLH Panel, 2014) remain valid and up to date regarding fruit as a pathway and the ongoing update of Directive 2000/29/EC. The Panel acknowledges the difficulty in providing compelling evidence for non-susceptibility of a particular plant species to infection with a pathogenic organism.
The Panel recognises that the available lines of evidence, although not fully demonstrative on their own, complement and reinforce each other. Therefore, in reaching its conclusions, the Panel systematically considered all information available, as well as the associated uncertainties and the possible synergies between the different lines of evidence.
From the two papers provided by the Japanese authorities and the 16 additional ones obtained from the literature review, the PLH Panel notes that: • C. junos artificially inoculated with X. citri pv. citri exhibits typical canker-like lesions, although the extent of watersoaking, tissue hypertrophy and lesion increase in size was less than on susceptible cultivars; • natural infections of C. junos were reported from Japan in production groves in the 1970s (although the precise locations in Japan have not been provided) and X. citri pv. citri strains had been isolated from those lesions; • the analysed scientific papers suggest that C. junos exhibits partial resistance but not immunity to X. citri pv. citri; • based on limited scientific papers, C. junos can also be considered a putative host of X. citri pv. aurantifolii.
The Panel also emphasises the limited literature available, and especially that: • most scientific papers investigating the susceptibility of C. junos used single genetically uncharacterised bacterial strain for inoculations; • the genetic structure of the population of X. citri pv. citri in the C. junos productions zones is not precisely known. Up to now, C. junos has not been challenged with strains representative of the X. citri diversity; • a single scientific paper investigating the susceptibility level of five Chinese C. junos accessions suggested cultivar-dependent partial resistance levels among these.
From this, the PLH Panel considers that the conclusions of its previous opinion remain valid and that convergent lines of evidence provide sufficient demonstration that C. junos is a host of X. citri pv. citri and X. citri pv. aurantifolii.
Therefore, there is no reason to consider the C. junos fruit differently from other citrus species; consequently, the assessment of the general citrus fruit pathway from the 2014 opinion still applies.
Documentation provided to EFSA 1) Request to provide a scientific opinion on the risk of Citrus junos fruits for the introduction of citrus canker. SANTE.GI/GVC/as (2016)  a) the fruits originate in a country recognised as being free from X. campestris (all strains pathogenic to Citrus), in accordance with the procedure referred to in Article 18 (2) or b) the fruits originate in an area recognised as being free from X. campestris (all strains pathogenic to Citrus), in accordance with the procedure referred to in Article 18(2) and mentioned on the certificates referred to in Articles 7 or 8 of that Directive, or c) either, in accordance with an official control and examination regime, no symptoms of X. campestris (all strains pathogenic to Citrus) have been observed in the field of production and in its immediate vicinity since the beginning of the last cycle of vegetation and none of the fruits harvested in the field of production has shown symptoms of X. campestris (all strains pathogenic to Citrus), and the fruits have been subjected to treatment such as sodium orthophenylphenate, mentioned on the certificates referred to in Articles 7 or 8 of Directive 2000/29/EC, and the fruits have been packed at premises or dispatching centres registered for this purpose, or any certification system, recognised as equivalent to the above provisions in accordance with the procedure referred to in Article 18(2) of Directive 2000/29/EC, has been complied with.
Fruit of Citrus, Fortunella, Poncirus and their hybrids, are then considered in Point 3, Section I, Part B of Annex V of Directive 2000/29/EC (version in force), as plant products originating in territories other than the Community, which are potential carriers of harmful organisms of relevance for the entire Community, and which must be subject to a plant health inspection before being moved within the Community, in the country of origin or the consignor country, before being permitted to enter the Community.
Apart from Directive 2000/29/EC, Commission Decision 2006/473/EC recognises certain third countries and certain areas of third countries as being free from X. campestris (all strains pathogenic to Citrus). Japan is listed neither in Article 1, nor in Article 2 of that decision, dealing with X. citri pv. citri or X. citri pv. aurantifolii, and cannot therefore be considered as partly or entirely free from those bacteria.