> **RISK ASSESSMENT REPORT FOR *Xanthomonas axonopodis pv citri ON
> CITRUS FRUITS ***
>
> ***Elaborated by: Ings. Agrs. Pablo Cortese (Argentina), Jose Geraldo
> Baldini (Brazil), Ernesto Galliani (Paraguay), Ma. Inés Ares
> (Uruguay).***
>
> ***In consultation with : Dr. Ruy Pereira Leite (Brazil), Ing. Agr.
> Elina Zefferino (Uruguay).***
>
> ***Revised by: Citrus Canker Working Group ( IPPC,FAO)***

### COSAVE 2004 

**INDEX**

**STAGE I. INITIATION**

1.  **Reasons for the PRA initiation**

2.  **Taxonomic position of the pest**

**STAGE II. PROBABILITY OF INTRODUCTION**

**2.1 Probability of entry**

> **2.1.1 Geographical distribution at world level**
>
> **2.1.2 Situation of the area under PRA**
>
> **2.1.3 Main hosts**
>
> **2.1.4 Probable pathways of entry**

**2.2 Probability of establishment**

> **2.2.1 Hosts at risk in the PRA area**
>
> **2.2.2 Weather similarities between the area of origin and the area
> of destination**
>
> **2.2.3 Brief description of the pest biology**
>
> **2.2.4 Conditions of survival during handling, transportation and
> storing**
>
> **2.2.5 Possibility of transference to an appropriate host**

**2.3 Economic Impact Assessment**

> **2.3.1 Description of the damage to potential hosts in the PRA area**
>
> **2.3.2 Economic impacts where the pest is present**
>
> **2.3.3 Potential economic impact in the PRA area**

**2.4 Conclusion**

> **2.4.1 Estimate of probabilities of introduction and establishment**
>
> **2.4.2 Identified Level of Risk**

**MENTIONED BIBLIOGRAPHY**

**RISK ASSESSMENT REPORT FOR *[Xanthomonas axonopodis pv.
citri]{.underline}* (Xac) IN CITRUS FRUIT.**

**STAGE I. INITIATION**

**1.1 Reasons for the PRA initiation.**

At the COSAVE Region, with the exception of Chile, the other countries
(Argentina, Brazil Paraguay and Uruguay) have areas affected by citrus
canker, and among them, the main citrus fruit exporting countries at the
South Cone can be found.

Due to this reason, official institutions and their technical teams have
an experience of almost 30 years in the different technical aspects of
the management and control of the disease, and in export phytosanitary
certification systems. Additionally, this experience is complementary to
relevant information developed by USA, at domestic level or with
countries belonging to the COSAVE Region.

The objective of this assessment is to contribute with elements for the
risk management of the pest, in the citrus fruit trade, to facilitate
the reassessment of the phytosanitary measures required by those
importing countries in which the pest is of quarantine concern.

**1.2- Taxonomic position of the pest**

**Identity:**

**Name**: *Xanthomonas axonopodis pv. citri* (Hasse) Vauterin, et.al.
1995.

**Synonyms**: *Xanthomonas campestris* (Pammel) Dowson pv. citri
(Hasse).

*Pseudomonas citri* Hasse.

*Xanthomonas citri* (Hasse) Dowson

*Xanthomonas citri* (Hasse) Dowson f.dp. aurantifolia Namekata &
Oliveira.

*Xanthomonas campestris* (Pammel) Dowson pv. aurantifolii Gabriel, et
al. 1989.

**Taxonomic Position**: Bacterium: Gracilicutes.

**Common names**: Cancrosis de los cítricos (all strains), Cancrosis
Asiática (Tipo A), Cancrosis de la lima ácida y Cancrosis del limonero
gallego (Tipo C), Citrus canker, Bacterial canker of Citrus, Citrus
bacterial canker, Asiatic canker, canker A, canker B, canker C, canker
D, Citrus bacteriosis, Chancre bacterien des agrumes.

**Notes about taxonomy**: Several changes on the taxonomic status of *X.
campestris* pv*. citri* have been proposed (Gabriel et al., 1989). This
includes the reassignment of some strains of pv. citri at species level,
such as X. citri and X. *campestris* pv*. aurantifolli.* Up to now,
these overviews have not been universally adopted and strains A, B, C
and D are still classified as *X. campestris* pv. *citri.* More
recently, Vauterin et al. (1995) have proposed new classifications
within the Xanthomonas genera. The new name *X. axonopodis* pv*. citri*
has been proposed for strain A, while *X. axonopodis* pv. *aurantifolli*
has been proposed for strains B, C and D. The name *X.axonopodis* pv*.
citrumelo* have been proposed, but they were not officially adopted for
the pathogen previously known as *X. campestris* pv. *citrumelo*
(Gabriel et al., 1989) or strain E of citrus canker identified in 1984
in citrus tree nurseries in Florida (USA) causing citrus bacterial spot.
In 1990 all the regulations regarding citrus bacterial spot or strain E
of *X. campestris* pv*. citri (X. campestris* pv*. citrumelo*) have been
withdrawn, based on scientific evidence and experience in Florida which
indicated that none of the strain types cause a harmful disease for
citrus or other fruit plants, **Graham and Gottwald (7)**.

**STAGE II -- PROBABILITY OF INTRODUCTION**

**2.1 Probability of entry.**

> **2.1.1 Geographical Distribution at world level**.
>
> Citrus canker has probably originated in the Asian southeast and it
> was subsequently spread throughout Asia and then Africa, Oceania and
> the Americas. The disease has been reported in the Indian Ocean
> Islands in Middle East. Strains causing a moderate type of disease,
> with a minor host range have been reported in South America (Canker B,
> Canker C). They have not been isolated from naturally infected trees
> since the 80´s.
>
> ASIA: Afghanistan, Andaman Islands, Bangladesh, Cambodia, People's
> Republic of China, Hong Kong, India, Indonesia, Iran, Japan (including
> Okinawa) Kampuchea, Democratic People's Republic of Korea, Laos,
> Malaysia, Maldives, Miasma (Burma), Nepal, Oman, Pakistan,
> Philippines, Ryuku Islands, Saudi Arabia, Singapore, Sri Lanka,
> Taiwan, Thailand, United Arab Emirates, Vietnam, Yemen.
>
> AFRICA: Comoro Islands, People's Republic of Congo, Cote d'Ivoire,
> Gabon, Madagascar, Mauritius,Mozambique (reported as eradicated),
> Reunion Island, Rodríguez Island, Seychelles Islands, Southafrica
> (Reported as Eradicated) and Zaire (status in Africa must be reviewed)
>
> NORTH AMERICA: Mexico (Only strain D, reported as eradicated), United
> States of America.
>
> SOUTH AMERICA: Argentina (Strain A, B eradicated), Brazil (Strain A,
> C), Paraguay (Strain A, B and C), Uruguay (Strain A, B eradicated).
>
> OCEANIA: Carolinas Islands, Christmas Islands, Cocos Islands, Fiji
> Islands, Guam, Marianas Islands, Micronesia, Papua New Guinea,
> Thursday Island (Eradicated in 1991), Reported as eradicated from the
> Australia and New Zealand commercial citrus areas, nevertheless, there
> are still occasional outbreaks.
>
> **2.1.2 Situation of the area under PRA.**
>
> The situation of the pest in the area under PRA is of quarantine
> importance.

3.  **Main hosts:**

> Known hosts are those of the Rutaceae family. Nevertheless, plants of
> Citrus genera are the hosts with higher economic importance. Natural
> infections are known to happen only in species, hybrids and cultivars
> of Citrus spp., *Poncirus trifoliata*, Fortunella spp. (*F. japonica*
> and *F. margarita), Severinia buxifolia* and *Swienglea glutinosa*.
> Nevertheless, other rutaceous members, including members of the
> Subfamilies Aurantiodeae, Rutoideae and Toddalioideae. A non rutaceous
> host, *Lansium domesticum* (Meliaceae) has been reported but this
> information was not confirmed. Canker B strains have a host range
> similar to Canker A strains, but affect certain hosts less severely
> (Stall and Civerolo, 1991). Canker C and D strains only affect Mexican
> lime (C. aurantifolia). The potential host range may include any wild
> or cultivated rutaceae plant developed in tropical and subtropical
> areas where the weather is appropriate for infection and development
> of the disease.

## Host susceptibility

> Only species of Citrus and Poncirus genera are susceptible under
> natural conditions as to be important in the Citrus canker epidemic
> development. Among Citrus varieties, Citrus canker is more severe on
> grapefruits, some orange varieties such as Hamlin, Pineapple and
> Navel, Mexican limes and lemons (12). However some varieties of
> mandarins, oranges and limes are less susceptible and can be
> commercially produced in areas where Citrus canker is endemic (12).
> Among these varieties are: Dancy, Ponkan, Tankan and Satsuma
> mandarins; Valencia, Pera, Folha, Murcha, Jaffa, Salustiana, Shamouti
> and Cadenera oranges, and Tahiti lime (12, 13)
>
> **2.1.4 Probable pathways of entry**: This assessment only analyzes
> citrus fruits to be traded.

**2.2 Probability of establishment.**

> **2.2.1 Hosts in risk in the PRA Area**: Species of the Citrus,
> Poncirus and Fortunella genera.
>
> **2.2.2 Weather similarities between the area of origin and the area
> of destination.**
>
> As this analysis is carried out for different free areas in which the
> weather details are not known, weather conditions favorable for the
> disease are analyzed.
>
> According to **Canteros (3) and Leite (12)**, weather conditions
> favorable for the disease are copious and persistent rains during
> growing season, specially in spring and summer and strong winds (wind
> speed higher than 8 m/s) when raining and high temperatures, but
> generally not above 35°C (12). Citrus canker takes place since ancient
> times and reaches high intensity in zones of the world where the rain
> season happens together with the more intense growing season. Even in
> favorable zones the disease may vary widely when environmental
> conditions change. For example, in Japan the higher infections are
> produced at the same time as typhoons, which lashes planted areas in
> some seasons.
>
> Weather factors which promote the different stages of the disease are
> temperature from 20 to 35°C and humidity with regards to bacteria
> multiplication in already produced lesions, humidity, rains and
> simultaneous winds for spreading and invasion, high humidity for
> establishment and temperatures of 20 to 35°C for the development of a
> new lesion. Optimum temperature for Citrus canker development is 30º C
> (12)
>
> Adverse effects for this phase are: temperatures above 35º C or under
> 13º C and low humidity for multiplication in old canker lesions,
> dryness for dispersion and invasion, low humidity for establishment
> and low temperature for young lesion development
>
> According to **Peltier & Frederick (15)**, the disease is more severe
> in regions where temperature and humidity (rains) monthly averages
> increase and decrease during the year. On the contrary, the disease is
> less severe where high temperatures come together with low rains.
>
> According to **Serizawa et. al. (19) and Graham et al. (8)**, high
> relative humidity is a dispersion factor for the bacteria. If the wind
> speed is higher than 8m/sec. the disease will be more severe, as it
> will have the necessary pressure for penetration of the bacteria
> through the stomata.
>
> **Koizumi (10)**, has analyzed the behavior of canker in 10 varieties
> of citrus and verified that the period of incubation of the bacteria
> decreased with the increasing of temperature. Then, there was no
> relationship between the incubation period and resistance. This author
> also verified that optimal temperatures for canker development in
> field conditions are between 25 and 30°C.
>
> **Stall et al. (20),** in studies carried out in Argentina, verified
> that the internal population of *X. axonopodis* pv. *citri* in canker
> lesions are between 10 ^6^ and 10 ^7^ cfu/ml. in the seasons in which
> the higher temperatures comes together with rains, while during winter
> months bacteria population decreased from 10 ^2^ to 10 ^4^ cfu/ml.
> Even the age of the lesions does not significantly affect the
> bacterial population during the warmer months.
>
> On the other side, using a rainfall simulation device, **Pruvost et
> al. (16)**, verified that in Mexican Lime canker leaf lesions,
> submitted to tropical environment, populations of *X. axonopodis* pv.
> *citri* did not strongly decrease in old lesions (6-10 months).
>
> **2.2.3 Brief description of the pest biology.**
>
> The sources of primary inoculum for spring infections are lesions in
> branches and leaves as a consequence of the previous autumn infections
> and in which the pathogen survives during winter. The bacteria survive
> in lesions in leaves, branches and fruits developed during spring.
> Seasonal lesions are the source of bacteria for secondary infections.
>
> In spring and at the beginning of the summer, with humid and warm
> weather and in the presence of free water, the bacteria that survived
> winter, exude from lesions. The bacteria infect leaves and young
> branches in actively growing tissue. The infection takes place through
> natural openings (stoma pores and lenticels) and injuries. The
> bacteria multiplies in intercellular spaces, while the host cells
> divide producing abnormal proliferation of cells to cause canker type
> lesions.

Citrus leaves are susceptible to the canker infection for a period of
only 14 to 21 days approximately near the moment they reach their
maximum expansion. Fruits may be susceptible for a period of 60 to 90
days after petal drop. Lesions do not affect the internal quality of the
fruit.

> Rainwater collected from the foliage with lesions have between 10^5^
> and 10^8^ cfu/ml. Thus rain with wind is the main way of spreading of
> the bacteria and winds above 8 m/s help the penetration of the agent
> through stomata or injuries caused by storms and insects.
>
> Among the last ones, the citrus leaf miner (*Phyllocnistis citrella)*
> may be highlighted as it produces galleries on the leaves and when it
> breaks the cuticle it exposes the mesophyll to the infection caused by
> the bacteria, even in the more resistant varieties. **Jesus et al.
> (9)** has verified that the damages caused by the miner larvae on the
> leaves facilitate infection in a period of 0 to 4 days. On the other
> hand, with mechanical injuries, this period was of 0 to 2 days
> (possibly due to a quicker leaf healing).

**2.2.4 Conditions of survival during handling, transportation and
storing.**

> The bacteria survive for variable periods of time, associated to
> citrus symptomatic leaves, more than one year, in debris of affected
> plant tissues, a few months and in the soil for a few days or weeks,
> depending on soil and weather conditions (temperature and relative
> humidity). Gottwald, Graham and Shubert (6)
>
> In addition to this, it can survive on undergrowth of weed foliage
> during short periods.
>
> Timmer, Gottwald and Zitko (22) verified that the bacteria do not
> multiply on the asymptomatic leaves surface and the number of live
> bacteria on the surface of this leaves decrease very quickly, even
> when they had favorable conditions for their development. Culturable
> populations of 50.000 cfu/ml decrease to 5 cfu/ml in 50 hours on the
> surface of the leaves of Pineapple orange.
>
> Populations of Xac. in leaves and fruits without symptoms are
> generally low, even in highly infected lots and almost always
> undetectable in farms with low disease intensity. Rybacck and Canteros
> (18), Timmer, Gottwald and Zitko (23) have found evidences that the
> Xac can not remain on host plants or non host in absence of symptoms
> for long periods of time. This verifies the fact that the Xac residual
> epiphyte population does not contribute to the leaf infection.
> Bacteria remaining on the leaves after rain can only survive some
> days, but they cannot multiply on the foliage surface and the number
> of live bacteria quickly decreases (12, 13). As Xac is not multiplied
> on the leaf surface, it is considered as a casual epiphyte instead of
> resident, and, therefore, it is not an important source of inoculum.
>
> For the analysis of this point there is a division between Xac
> survival in lesions and in epiphytic form.

\- Survival of Xac in lesions:

> According to Gottwald, Graham and Shubert (6), the bacteria survives
> from one growing season to the following in lesions formed, mainly,
> during its last stage. The bacteria remain viable because there are
> host live cells near it. Lesions in branches can keep the bacteria
> alive for several years. Living bacteria have been isolated in lesions
> of 5 to 7 years of age form Mexican lime trunks affected by Wellington
> strains in Florida.

-   Survival of Xac in epiphyte form:

> All studies listed below refer to culturable populations of Xac,
> however a recent report by Cubero & Graham, establishes that
> Xanthomona associated with Citrus can enter a viable but non
> culturable state. The biological significance of this state is
> presently unknown.
>
> On inert surfaces (metals, plastics, clothes and processed woods,
> among others) it was verified that Xac dies between 24 and 72 hours
> Gottwald et al. (6), depending on the environmental conditions, mainly
> humidity: when the surfaces are dried the bacteria dye.
>
> In non host plants it may survive for several weeks in natural
> conditions and, according to the information of Japan and Brazil, the
> survival of Xac was verified up to 8 months at root zones of some
> weeds located under diseased trees that had been eradicated (there are
> no other quotations that may confirm these results). Gottwald et al
> (6). More recent studies showed that Xac can not survive on crop
> residues, weeds or soil for long periods (12). This quick decrease of
> Xac population is due to the fact that the bacteria has not the
> capacity to survive out of citrus canker lesions (12).
>
> Koizumi and Kuhara (11) indicated that fruits are susceptible for long
> periods, from green (small) to maturation. Mature fruits can be
> infected, but their lesions do not develop.
>
> On fruits without symptoms, Belasque and Rodriguez Neto (1) externally
> sprayed with a suspension of bacteria (10 x 6 cells/ml) and preserved
> them at room temperature at the laboratory. It was verified that the
> bacteria population decreased from 10 x 5 cells/ml in time zero to 10
> x 2 cells/ml in 24 hours and 10 x 1 cells/ml at the third day. There
> was no possibility of recovering inoculated bacteria after five days.
>
> It is useful to mention that several studies that refer to this point,
> such as Obata et al. (14), Stapleton, J.J. (21), Canteros et al. (4),
> analyze the efficiency of disinfections treatments for fruits without
> symptoms and their results are directly linked to the possibility of
> spreading of the disease and its establishment in a free zone.
>
> Verdier et. al. in recent studies non publish yet, evaluating post
> harvest treatments in symptomless fruit, artificially inoculated and
> naturally exposed, found that average bacterial population from
> inoculated fruit was 2 x 10^3^ cfu/ml, being 4 cfu/ml after post
> harvest treatments. In naturally exposed fruit the bacterial
> population was 40 cfu/ml, being 0,054 cfu/ml after post harvest
> treatments.
>
> 2.2.5 Possibility of transference to an appropriate host.
>
> Pest long distance dissemination mainly takes place through movement
> of infected plant propagative material, such as buds, rootstocks or
> nursery plants. There are no confirmed proof of spreading through
> seeds. Although it is possible to think that the pest can move long
> distances with infected fruits, there is no proof of an infection
> started as a consequence of the introduction of affected fruit to the
> market.

As from the last information of Xac detection in the world, and of
reinfections in countries with the disease eradicated or in areas
considered as free it is mentioned that:

> Infections in several Arab countries (Yemen, Saudi Arabia, Iran,
> United Arab Emirates, etc) are related to the introduction of infected
> plants from India and Pakistan, countries where the disease is
> endemic.
>
> In countries such as Australia or New Zealand which have shown some
> reinfection events, they have not been related to the introduction of
> affected fruit. The same has happened in Florida State (USA) even when
> this country has an important database of interceptions of symptomatic
> fruits in airports and ports.

**2.3 Economic Impact Assessment.**

> **2.3.1 Description of the damage to potential hosts in the PRA
> area.**
>
> Primary symptoms of Xac are spots on leaves and branches and damage in
> the fruit skin. Under favorable infection conditions in susceptible
> hosts there is a defoliation and premature fall of the fruits.

Dead of terminal branches in highly susceptible hosts may happen in
highly favorable conditions for the development of the disease. The
internal quality of the infected fruit, which ripens on the trees, is
not affected. However, the market value of the fruit with lesions is
reduced.

In general, and depending on the varieties, grapefruits, limes and
*Poncirus trifoliata* are highly susceptible; sour orange, lemon and
sweet orange are moderately susceptible. Mandarins are moderately
resistant. But some mandarins and hybrids mandarins are high susceptible
to citrus canker, such as Fremont, Kara and Umatilla (13)

2.  **Economic impacts where the pest is present.**

When citrus canker is severe on very susceptible varieties, under highly
favorable conditions for the development of the disease (without an
adequate phytosanitary management) defoliation and fall of the fruit are
mentioned. There is a lost in commercial quality due to changes in the
external aspect of the affected fruit.

> The most important economic loss happens because of quarantine
> restrictions imposed to citrus fruit international trade, for fruits
> coming from areas where the disease occurs.

3.  **Potential economic impact in the PRA area.**

> If the pest is effectively established in citrus commercial production
> areas the economic impact will depend on the phytosanitary measures
> implemented at the beginning of the epidemic and on their success. The
> presence of the citrus leaf miner, and the occurrence of favorable
> environmental conditions are important factors which may affect the
> effectiveness of the first control actions.
>
> If an endemic situation is reached, impacts will be the same as those
> mentioned above.

**2.4 Conclusion**

> **2.4.1 Estimate of probabilities of introduction and establishment.**
>
> For the analysis of this estimate several statistical procedures which
> may allow to achieve an estimated value of introduction and
> establishment, all of them based on the probability calculation where
> each stage is considered independently may be used.
>
> This document uses information based on the Citrus Canker Risk
> Analysis carried out by a possible importer country for a country of
> the region and the risk assessment for *Erwinia amylovora* in
> commercialization of apple fruit carried out by **Roberts et at.
> (17)**, due to the fact that it is a bacteria with possible
> transmission by fruit, subject to international trade.

If the before mentioned citrus canker risk analysis assessment is
considered, the assessment will be carried out through:

**- Estimate probability of entry.**

The number of symptomatic and asymptomatic harvested fruit in one season
was considered, taking into account export volumes with two definite
probabilities:

a)  If the bacterium survives in the infected fruit after post harvest
    treatment.

b)  If the bacterium is capable of living after transport from the port
    to the destination.

**- Estimate probability of establishment.**

The number of symptomatic and asymptomatic fruit, which may enter into
the destination country during a year, was considered, calculating the
following probabilities:

a)  If the exported fruit enters into a citrus growing region in the
    country of destination.

b)  The possibility of the viable bacteria getting in contact with a
    Citrus tree.

c)  If the host is receptive at the contact moment.

d)  If environmental conditions are favorable for infection development.

e)  If it is possible that as from the moment of contact between the
    bacterium and the host, an infection is produced.

> For this study, the results obtained with regard to **the possibility
> of entrance vary between 0 and 2000 fruits/year with a media of near
> 20 fruits**.
>
> Regarding **the possibility of establishment, it is concluded that it
> may happen 1 outbreak in 3.000 years.**
>
> In the study carried out by **Roberts**, a model taking into account
> the number of exported fruits per year was used, based on the
> following probabilities:

a)  If the exported fruit is infected or contaminated.

b)  If the bacteria survives to storing, transportation and culling.

c)  If the fruit may be in touch with the host.

d)  If the host is in a receptive state

e)  If the bacteria is transferred to the hosts and the infection is
    produced.

The results, according to the assessed scenarios, were the following:

> Scenario 1: It takes into account the restrictions imposed by Japan to
> New Zealand and USA, and the average obtained is **1 outbreak every
> 38,462 years.**
>
> Scenario 2: Considers some of the requirements of the previous
> scenario, and in the **places of production there may happen a 1 % or
> less of trees affected by the disease and the media obtained is 1
> outbreak every 35,971 years**.
>
> Scenario 3: Without any phytosanitary measures and the obtained
> average is **1 outbreak every 11,364 years**.

**2.4.2 Identified Level of Risk.**

> According to what has been analyzed with regard to the information of
> this risk assessment, the conclusion is that the level of risk of this
> pest in the citrus fruit trade **is very low.**
>
> **Canteros (3)** says that the probable risk of spreading of this
> disease through a fruit without symptoms, exported for final
> consumption, **is practically non existent**.

Civerolo (5) mentions that:

-   Up to the date it has not been proved that Xac latent populations
    may produce symptoms in harvested fruits.

-   There is no report proving the beginning of an epidemic due to
    asymptomatic commercial fruit.

-   An effective management of the citrus canker may mitigate the risk
    of spreading of Xac through commercial fruit.

-   Citrus fruit commercially produced through an integrated measure
    system has a very low risk of spreading of citrus canker.

Although there is a very low risk for introduction of citrus canker
through fruit transportation pathway, from places that are not free from
the pest, it is important to establish risk management options to meet
the appropriate level of protection of importing countries where Xac is
considered a quarantine pest. This is based on the lack of evidence that
an epidemics can be initiated through the movement of Citrus fresh fruit
from countries where the disease occur or by the introduction of
symptomatic or asymtomatic fruits from infected areas.

MENTIONED BIBLIOGRAPHY

> 1\. BELASQUE Jr.J.;RODRIGUEZ NETO, J. Sobrevivencia da bactéria
> causadora do cancro cítrico (Xanthomonas axonopodis pv. citri) em
> frutos de laranja nao infectados com a doença. Summa Phytopathologica,
> 26 (1): 128 (Resumo 153).
>
> 2\. BROWN, W.G., and SCHUBERT, T.S. 1987. Use of Xanthomonas
> campestris p.v. citri to evaluate surface disinfectants for canker
> quarantine treatment of citrus fruit. Plant Disease. 71: 319-323.
>
> 3\. CANTEROS, B. I. 1997. Justificación del Sistema de Lotes de
> Sanidad Controlada para la Producción de Fruta en Argentina con Riesgo
> Mínimo para la infección de Cancrosis de los Países Citrícolas de la
> Unión Europea. Curso de Actualización para profesionales. EEA INTA
> Bella Vista. 2002, pg. 211-213
>
> 4\. CANTEROS, B.I. NARANJO,M., RYBAK, M. 2000. Production of Fruits
> Free of Xanthomonas axonopodis pv.citri in Selected Plots, in Areas of
> Endemic Canker in Argentina. Proceddings International Society
> Citriculture. Orlando. Florida. USA. 2000.
>
> 5\. CIVEROLO, E. 1997. XXI NAPPO Annual Meeting en Seattle,
> Washington, USA.
>
> 6\. GOTTWALD, T.R.; GRAHAM, J.M. and SCHUBERT, T.S. 2002. Citrus
> Canker: The pathogen and Its Impact.
>
> 7\. GRAHAM, J.H. and GOTTWALD, T.R., 1991. Research Perspectives on
> Eradication of Citrus Bacterial Disease in Florida. Plan Disease 12
> 1991, 1193-1200 pp.
>
> 8\. GRAHAM, J.H.; GOTTWALD, T.R.; RILEY, T.D., ACHOR, D. 1992.
> Penetration through stomata and growth of strains of Xanthomonas
> campestris in citrus cultivars varying in susceptibility to bacterial
> diseases. Phytopathology, 82: 1319-1325, 1992.
>
> 9\. JESUS Jr., W. C.; BERGAMIN FILHO, A., BELASQUE JR.,
> J.C.CHRISTIANO, R.S.C.; AMORIN, l; RODIGUES NETO, J. 2003. Age of
> mechanical and leaf miner wounds on incidence and severity of citrus
> canker. 8^th^.Int.Congr. Pl. Pathol., Christchurch, NZ, 2-7 feb/2003
> (Abstr. 2.5).
>
> 10\. KOIZUMI, M. 1976. The incubation period of citrus canker in
> relation to temperature. Bull Fruit Trees Res. Sta., series B,
> 3:33-46.
>
> 11\. KOIZUMI, M.; KUHARA, S.1982. Evaluation of citrus plants for
> resistance to bacterial canker disease in relation to the lesion
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