• Bacterial Citrus Canker

Plant Pathology Circular No. 377 Fl. Dept. of Agriculture & Cons. Svcs.
May/June 1996 (fifth revision January 2003) Division of Plant Industry
Bacterial Citrus Canker1
T. S. Schubert2 and X. Sun3
INTRODUCTION: Citrus canker (CC), caused by the bacterial pathogen Xanthomonas axonopodis Starr & Garces emend.
Vauterin, et al. pv. citri (Hasse) Dye (Xac) [syn. Xanthomonas campestris pv. citri (Hasse) Dye], is a serious disease of most
commercial citrus varieties and some citrus relatives. The pathogen causes necrotic lesions on leaves, stems and fruit. Severe
infections can cause defoliation, badly blemished fruit, premature fruit drop, twig dieback and general tree decline.
Considerable regulatory effort is directed at preventing the spread of CC because it is not present in all citrus-growing regions
of the world where the climate is conducive to CC development.
HISTORY: The Asian, or A-strain, of CC is thought to have originated in southeastern Asia or India (Civerolo 1984) and spread
through much of Asia, to Japan, southern and central Africa, the Middle East, Australia, New Zealand, Pacific Islands, South
America and the southeastern United States (CABI/CMI 1996; Schubert et al. 2001; Gottwald et al. 2002b). CC has been
eradicated from South Africa, Australia, the Fiji Islands, Mozambique, New Zealand and the United States (Koizumi 1985).
Active eradication/containment programs are continuing in Uruguay and Brazil.
The history of CC in Florida began presumably around 1910 (Dopson 1964; Loucks 1934) when the disease was introduced into
North Florida and other Gulf States on trifoliate citrus rootstock material from Japan. The disease was previously undescribed,
and it was not until 1915 that the pathogen was identified as bacterial. By 1913, South Florida citrus growers had reached a
consensus that eradication efforts were warranted since all control efforts against the rapidly spreading disease proved
ineffective. The pathogen had spread throughout the Gulf States and up the Atlantic coast to South Carolina by the time
eradication efforts were well underway. A quarantine prohibiting the importation of all citrus plants was enacted in 1915. The
newly formed State Plant Board took over the eradication program for Florida that same year. Federal assistance from the USDA
- Bureau of Plant Industry commenced soon after. The last infected tree in Florida was removed in 1927. An intensive inspection
program continued until 1933, when the disease was declared officially eradicated. The disease was declared eradicated from
the United States in 1947. Citrus canker has been a target of regulatory detection surveys in Florida ever since.
In June 1986, CC was detected in residential citrus in Hillsborough, Pinellas, Sarasota and Manatee counties, and was also
found soon after in two Manatee County commercial citrus groves and one commercial grove in Highlands County. All infected
citrus were removed and all exposed trees within 125 ft (38.1 m) were either removed or cut back to brown wood (Schubert 1991).
This second eradication program concluded with the last detection in January 1992. The official declaration of eradication was
made two years later.
In late September 1995, CC was discovered for a third time in Florida in a residential area near the Miami International Airport.
Initial surveys delimited an area of about 50 square miles containing thousands of diseased trees. An eradication effort was
begun immediately. Genetic fingerprinting of the isolate of Xac causing CC in the Miami area revealed that the pathogen was
recognizably different from the archived isolates from the 1986-92 outbreak in west-central Florida (Schubert et al. 1996). As of
March 2001, even with an extensive eradication effort, the disease had managed to spread predominantly northward from Dade
into Broward and Palm Beach counties. The logistics of regular inspections and eradication activities in the urban residential
setting of Southeast Florida have proven very challenging.
In May 1997, CC was rediscovered in eastern Manatee County in both commercial groves and residential citrus. Genetic
fingerprinting of the isolate of Xac present there closely matches that of the 1986-92 outbreak, and suggests that some holdover
infections went undetected in the final two years of intensive inspection in the area.
A third concurrent outbreak of CC was discovered in June 1998 in a commercial grapefruit grove in the Immokalee area of
Southwest Florida, and in a remote residential area nearby a year later. Two outbreaks of CC were detected in commercial groves
in southeast Hendry County in February 1999. In June 1999, the disease was detected in a commercial grove in western
Manatee County. All pathogen isolates from new locations are routinely genetically characterized to help identify the source(s)
of inoculum. With the exception of the isolates in eastern Manatee County and some isolates in Hillsborough County, all other
pathogen isolates in Florida are identical to the pathogen which was initially discovered in Miami in 1995. For an update on
the status of the Citrus Canker Eradication Program in Florida, visit the DPI citrus canker website at
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1 Contribution No. 703, Bureau of Entomology, Nematology & Plant Pathology - Plant Pathology Section.
2 Administrator and 3 Plant Pathologist, FDACS, Division of Plant Industry, P. O. Box 147100, Gainesville, FL 32614-7100.
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SYMPTOMS AND INFECTION PROCESS: All young above-ground tissues of citrus are susceptible to Xac (Fig. 1). The
bacterial pathogen enters plant tissues through natural openings (stomates) and wounds. The earliest symptoms on leaves
appear as slightly raised tiny blister-like lesions about 4-7 days after inoculation under optimum conditions, i.e., a water film
present and temperature between 20-30oC (Koizumi 1985). Under less than optimum conditions, symptoms may take 60+ days
to appear (Loucks 1934; Goto 1992). As the lesions age, they turn tan to brown, and a water-soaked margin appears surrounded
by a chlorotic halo. The center of the lesion becomes raised and corky (Figs. 2, 3). Lesions are usually visible on both sides of
a leaf. Eventually, the centers of leaf lesions become crater-like and may fall out, creating a shot-hole effect. Defoliation and
twig dieback become a problem as the disease intensifies on a plant.
On twigs and fruit, CC symptoms are similar: raised corky lesions surrounded by an oily or water-soaked margin. No chlorosis
typically surrounds twig lesions (Fig. 4), but may be present on fruit lesions (Fig. 5). Chlorosis symptoms can fade over time.
It is the twig lesions on angular young shoots that provide much of the perpetuating Xac inoculum in areas where CC is
endemic. Fruit blemishes and early fruit drop are major economic impacts of the disease.
As a general rule, Xac is capable of naturally infecting green citrus tissues while they are in the expansion phase of growth.
Once leaves, twigs and fruit reach mature size and begin to harden off, they become more resistant to infection. Since the young
growth provides the susceptible tissues, vigorously growing trees are most threatened by Xac. Any wound sites on young or
older tissues, however, can provide the infection court for Xac establishment and disease development. The serpentine mines
caused by the citrus leafminer (Phyllocnistis citrella Stainton), also Asian, first detected in 1993 in Florida (Heppner 1993),
provide ample wounding on new growth to greatly amplify CC infection (Sohi and Sandhu 1968; Sinha et al. 1972) (Fig. 6).
Wounds become naturally infected at much lower inoculum concentrations than via the stomatal route (minimum dose of
approx. 102 cells / ml for wounds vs. approx. 105 cells / ml for stomates) (Goto, 1992).
Wind-driven rain is the primary short- to medium-distance dispersal mechanism for CC, similar to other bacterial diseases. A drop
of rainwater can carry a maximum load of bacteria of about 107 to 108 cells. Inoculum-contaminated equipment and hands can
transmit Xac. Long-distance spread normally occurs by movement of infected or exposed citrus plant material, but circumstantial
evidence points to occasional long-distance transport by unusual storm events such as tornadoes and tropical storms.
Xac easily persists season to season in old lesions, especially in warmer climates and in lesions formed late in the growing
season (Pruvost et al. 2002). The pathogen is not systemic in the host plant. Xac can remain viable as long as host cells in the
vicinity of the lesion remain viable, though the bacterial titer will drop considerably. Reports on inoculum longevity outside
host tissue are inconsistent. On exposed, symptomless citrus, circumstantial evidence suggests some inoculum persistence for
at least several months, since root sprouts from infected trees that have been removed months prior frequently become infected
themselves. Xac may persist for several weeks on non-host plant material, with some exceptional reports of longer persistence
(about 8 months) in the root zone of certain grasses under infected trees in Japan (Goto et al. 1975). Once infected/exposed
leaves or fruit drop to the ground, the bacterial population declines to a non-detectable level in 1-2 months because of
antagonism and competition with saprophytic microorganisms (Goto 1992). Reports of survival on inanimate surfaces vary
from a few hours to several months. In general, when inoculum dries on nonporous surfaces, it dies. Concentrated inoculum,
such as from natural lesions or from culture, survives longer than cells diluted in a water suspension. The intact polysaccharide
slime coating on the bacterial cells is thought to be essential for longer survival.
HOST RANGE: Civerolo (1984) lists a number of plants in the Rutaceae other than Citrus and Poncirus that can serve as
hosts of Xac under experimental conditions or heavy disease pressure in nature. A comprehensive host list is presented on the
DPI website (address above). Among commercial citrus varieties and rootstocks, CC is most severe on grapefruit (C. x
paradisi), Key limes (C. aurantiifolia), and trifoliate orange (Poncirus trifoliata) and their hybrids because of their high
susceptibility (Table 1). All natural hosts of CC must be considered potential risks when eradication is the goal.
Table 1. Susceptibility of several commercial citrus varieties and rootstocks to Xac.
Highly Susceptible Moderately Susceptible
Citrus x paradisi Macf., grapefruit C. sinensis (L.) Osbeck, sweet orange
C. aurantiifolia (Christ.) Swingle, Key lime C. aurantium L., sour orange
C. limettioides Tan., Palestine sweet lime C. limon (L.) Burm. lemon
Poncirus trifoliata (L.) Raf., trifoliate citrus & hybrids C. x tangelo J. Ingram & H.E. Moore, tangelo
Susceptible Resistant
C. reticulata Blanco, mandarin, tangerine C. medica L., citron
C. maxima (Burm.) Merr., pummelo X Citrofortunella microcarpa (Bunge) Wijnands, calamondin
C. aurantiifolia (Christ.) Swingle, Persian or Tahiti lime Fortunella spp., kumquat
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Recently, it was reported that goat weed (Ageratum conyzoides L.) could serve as a host of Xac. This plant is common in citrus
orchards in India (Kalita et al. 1997). This represents one of only a few unsubstantiated reports of a non-Rutaceous host of Xac.
CONTROL: In Florida, the predicted negative economic impact of allowing CC to become endemic clearly favors eradication.
The Florida approach to CC eradication has evolved over time. In the first program from 1915 to 1933, infected trees were usually
doused with an incendiary fuel and burned in place. In later programs, infected trees have been burned in place or removed
mechanically. The necessity of removing exposed in addition to obviously infected trees was recognized in the 1986 program,
and a guideline calling for removal of all citrus within 125 ft of infected citrus was adopted based on studies of inoculum
dispersal in Argentina (Stall et al. 1980). In the latest eradication program with citrus leafminer involvement (Gottwald et al.
1997; Gottwald et al. 2001, 2002a), even the 125 ft radius was deemed inadequate for eradication in most situations, and a general
policy of removing infected trees plus exposed trees within a 1900 ft radius is now in place. Through risk assessment, exposure
zones are determined commensurate with the amount of disease, age of infection, inoculum dispersal opportunities,
environment, susceptibility of hosts, physical access to potential hosts for regular inspection, plus other factors. In these
exposure zones, all citrus is removed.
Guidelines call for quarantine areas to extend one to two miles in all directions from infected citrus. No citrus material is allowed
to move into or out of the quarantine zone unless risk-assessed. Survey and inspection crews should practice rigorous
sanitation of hands, shoes, clothing or any equipment that comes in contact with citrus before moving from property to
property. Quaternary ammonium disinfectants are available for use on both inanimate surfaces and for application to bare skin
and clothing.
In areas of the world where CC is endemic, disease management involves use of resistant varieties, windbreaks to hinder
inoculum dispersal and timely applications of copper-containing bactericides. Selective pruning of infected tissues is also
utilized in citrus growing areas where labor-intensive practices prevail.
SURVEY AND DETECTION: Look for raised, corky, tan lesions with water-soaked margins and yellow halos on the citrus
leaves. Similar citrus leaf pathogensCsour orange scab caused by Elsinoe fawcettii Bitancourt & Jenkins, melanose caused by
Diaporthe citri F.A. Wolf, and citrus bacterial spot caused by Xanthomonas axonopodis Starr & Garces emend. Vauterin et al.
pv. citrumelo Gabriel et al.Care illustrated in Figs. 7-9, respectively. The field inspector unfamiliar with CC should not rely on
these photographs for a definitive distinction of these three diseases. Any suspicious plant symptoms should be brought to
the attention of the DPI Pathology Section. Samples of suspect citrus should be double-bagged with the inner bag and hands
disinfected with quaternary ammonium before placing in the outer bag. Attach paperwork to the outer bag indicating >suspect
citrus canker= so the sample can be immediately processed in the DPI Plant Disease Quarantine Facility in Gainesville.
LITERATURE CITED
Civerolo, E. L. 1984. Bacterial canker disease of citrus. Journal of the Rio Grande Valley Horticultural Society 37: 127-146.
Commonwealth Agricultural Bureaux International - International Mycological Institute. 1996. Distribution maps of plant
diseases, Xanthomonas campestris pv. citri. Map No. 11. Edition 6. 2 p.
Dopson, R. N. 1964. The eradication of citrus canker. Plant Disease Reporter 48: 30-31.
Goto, M. 1992. Citrus canker. In: Plant Diseases of International Importance: Diseases of Fruit Crops (Vol. III) Ed. by J. Kumar,
et al. Englewood Cliffs, NJ, Prentice Hall, pp. 170-208.
Goto, M., K. Ohta and N. Okabe. 1975. Studies on saprophytic survival of Xanthomonas citri (Hasse) Dowson. 1. Detection
of the bacterium from a grass (Zoysia japonica). Annals of the Phytopathological Society of Japan 41: 9-14.
Gottwald, T. R., J.H. Graham and T.S. Schubert. 1997. An epidemiological analysis of the spread of citrus canker in urban
Miami, Florida, and synergistic interaction with the Asian citrus leafminer. Fruits 52: 371-378.
Gottwald, T.R., G. Hughes, J.H. Graham, X. Sun and T. Riley. 2001. The citrus canker epidemic in Florida: The scientific basis
of regulatory eradication policy for an invasive species. Phytopathology 91: 30-34
Gottwald, T.R., X. Sun, T. Riley, J.H. Graham, F. Ferrandino and E.L. Taylor. 2002a. Geo-referenced spatiotemporal analysis
of the urban citrus canker epidemic in Florida. Phytopathology 92: 362-377.
Gottwald, T.R., J.H. Graham and T.S. Schubert. 2002b. Citrus canker: The pathogen and its impact. Online. Plant Health
Progress doi:10.1094/PHP-2002-0812-01-RV. http://www.plantmanagementnework.org/pub/php/review/citruscanker/
Heppner, J. P. 1993. Citrus leafminer, Phyllocnistis citrella, in Florida. Tropical Lepidoptera 4: 49-64.
Kalita, P., L.C. Bora and K.N. Bhagabati. 1997. Goat weed - a host of citrus canker - (Xanthomonas campestris pv. citri).
Journal of Mycology and Plant Pathology 27: 96-97.
Koizumi, M. 1985. Citrus canker: the world situation. Pp. 2-7. In Timmer, L.W. (ed.). Citrus canker: An international
perspective. University of Florida, Lake Alfred.
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Loucks, K. W. 1934. Citrus canker and its eradication from Florida. (Unpublished manuscript, Library) Florida Department of
Agriculture and Consumer Services, Division of Plant Industry, Gainesville, FL. 111 p.
Pruvost, O., B. Boher, C. Brocherieus, M. Nicole and F. Chiroleu. 2002. Survival of Xanthomonas axonopodis pv. citri in leaf
lesions under tropical environmental conditions and simulated splash dispersal of inoculum. Phytopathology 92: 336-346.
Schubert, T.S. 1991. Recent history of citrus canker eradication programs in Florida. Newsletter of the Florida
Phytopathological Society 2: 1-6.
Schubert, T.S., J.W. Miller and D.W. Gabriel. 1996. Another outbreak of bacterial canker on citrus in Florida. Plant Disease
80: 1208.
Schubert, T.S., S.A. Rizvi, X. Sun, T.R. Gottwald, J.H. Graham and W.N. Dixon. 2001. Meeting the challenge of eradicating
citrus canker in Florida - Again. Plant Disease 85: 340-356.
Sinha, M.K., R.C. Batra and D.K. Uppal. 1972. Role of citrus leaf-miner (Phyllocnistis citrella Staintan (sic)) on the prevalence
and severity of citrus canker (Xanthomonas citri (Hasse) Dowson). Madras Agricultural Journal (Madras) 59: 240-245.
Sohi, G. S. and M. S. Sandhu. 1968. Relationship between citrus leafminer (Phyllocnistis citrella Stainton) injury and citrus
canker (Xanthomonas citri (Hasse) Dowson) incidence on citrus leaves. Journal of Research Punjab Agriculture
University (Ludhiana) 5: 66-69.
Stall, R. E., J. W. Miller, C. M. Marco and B. I. C. DeEchenique. 1980. Population dynamics of Xanthomonas citri causing
cancrosis of citrus in Argentina. Proceedings of the Florida Horticultural Society 93: 10-14.
USDA-APHIS-PPQ Biological Assessment Support Staff. 1982. Citrus canker. Pests not known to occur in the United States
or of limited distribution. No. 27. 12 p.
Plant Path
Revised Jan 2003
Fig. 1. Typical CC symptoms on leaves, stems and
fruit of grapefruit.
Fig. 2. Whole leaf symptoms of CC on top and bottom of grapefruit leaves (left) and key lime leaves (right).
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Fig. 3. Close-up views of CC lesions on top (left) and bottom (right) of grapefruit leaf. Photo credit: Jeffrey Lotz, DPI.
Fig. 4. Twig symptoms of Xac. young lesions on grapefruit (left); older lesions on Key lime (right).
Photo credit: Jeffrey Lotz, DPI.
Fig. 5. Fruit symptoms of CC on sweet orange (left) and grapefruit (right). Photo credit (left): Jeffrey Lotz, DPI.
Fig. 6. Leaf symptoms of CC on lemon exacerbated by citrus leafminer wounding, top (left) and bottom (right) of leaves.
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Fig. 7. Sour orange scab on sour orange leaf (left), close-up view of scab lesion (center), and scab lesions on tangelo
(right), caused by Elsinoe fawcettii Bitancourt & Jenk., for comparison to CC. Photo credit (right): V. Jane Windsor, DPI.
Fig. 8. Melanose (Diaporthe citri) and CC lesions on the same grapefruit leaf, bottom side. CC lesions are the
larger, brown raised corky lesions on the lower left; melanose lesions are the other smaller, black raised lesions.
Fig. 9. Citrus bacterial spot (Cbs) top (left) and bottom (right) of leaf on grapefruit, caused by Xanthomonas axonopodis
Starr & Garces emend. Vauterin, et al. pv. citrumelo Gabriel, et al., for comparison to CC. Cbs lesions are less pustular and
corky than CC, and aggressive strains exhibit a much more pronounced watersoaked margin than CC. Cbs can perpetuate
in young trees in crowded nursery environments, but disappears spontaneously when trees are outplanted.
All photos by T. S. Schubert, DPI, unless otherwise credited.
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