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PP323

Dooryard Production: Asiatic Disease1 Megan M. Dewdney, Jamie D. Burrow, James H. Graham, Timothy M. Spann, and Ryan A. Atwood2

Asiatic citrus canker is a bacterial disease of citrus caused States. In 1915, a quarantine banned the import of all citrus by the pathogen Xanthomonas citri subsp. citri. The bacte- plant material. The last known infected tree was removed rium causes necrotic lesions on leaves, stems, and of from in 1933, and the disease was declared eradi- infected trees. Severe cases can cause defoliation, premature cated from the in 1947. Since that time, citrus fruit drop, twig dieback, and general tree decline. Consider- canker has been the focus of regulatory rules to prevent its able efforts have been made to prevent its introduction re-introduction into the United States. or limit its spread in citrus-growing areas throughout the world. Despite regulatory efforts, citrus canker was found on residential trees in Hillsborough, Pinellas, Sarasota, and History of Citrus Canker in Florida Manatee Counties in 1986. Shortly after these detections, the disease was found in nearby commercial groves. Not surprisingly, citrus canker is believed to have originated Infected trees were removed immediately. The last tree in the native home of citrus, Southeast and . with citrus canker from this outbreak was detected in 1992. From there, the disease has spread to most of the subtropi- Citrus canker was once again declared eradicated in 1994. cal citrus-producing areas of the world, including Japan, parts of , the Middle East, , South America, Citrus canker was detected for the third time in a residen- and Florida. Eradication efforts were successful in South tial area near the Miami International Airport in September Africa, Australia, the Fiji Islands, and New Zealand. 1995. An initial survey found thousands of infected trees within a 14-square mile area. Eradication efforts began im- The first known outbreak of citrus canker in Florida mediately. New molecular genetic tools enabled researchers occurred around 1910. It is believed that the disease was to determine that the specific strain ofX. citri subsp. citri brought into the United States on infected rootstock responsible for this new outbreak was different from the material from Japan. The causal organism was unknown 1986–1992 outbreak. State and federal eradication efforts at the time, and it was not until 1915 that the pathogen proved inadequate and by 2001, the disease had moved was determined to be a bacterium. After the failure of all northward from Dade County and was detected in Broward control measures, an eradication effort was begun in 1913, and Palm Beach Counties. by which time the disease had spread throughout the Gulf

1. This document is PP323, one of a series of the Plant Pathology Department, UF/IFAS Extension. Original publication date March 2016. Visit the EDIS website at http://edis.ifas.ufl.edu. Previously published in February 2008 as HS113 (HS382) Dooryard Citrus Production: Citrus Canker Disease by the Horticultural Sciences Department and Timothy M. Spann, Ryan A. Atwood, Jamie D. Yates, and James H. Graham, Jr.

2. Megan M. Dewdney, associate professor, Plant Pathology, Citrus Research and Center; Jamie D. Burrow, program coordinator, Citrus Canker and Greening Extension Education Program, Citrus REC; James H. Graham, professor, Soil Microbiology; Timothy M. Spann, former associate professor, Horticultural Science; and Ryan A. Atwood, former Extension Agent II; UF/IFAS Extension, Gainesville, FL 32611.

The Institute of Food and Agricultural Sciences (IFAS) is an Equal Opportunity Institution authorized to provide research, educational information and other services only to individuals and institutions that function with non-discrimination with respect to race, creed, color, religion, age, disability, sex, sexual orientation, marital status, national origin, political opinions or affiliations. For more information on obtaining other UF/IFAS Extension publications, contact your county’s UF/IFAS Extension office.

U.S. Department of Agriculture, UF/IFAS Extension Service, University of Florida, IFAS, Florida A & M University Cooperative Extension Program, and Boards of County Commissioners Cooperating. Nick T. Place, dean for UF/IFAS Extension. In 1997, a separate outbreak of citrus canker occurred in As of January 11, 2008, Florida was placed under a state- Manatee County in commercial and residential citrus. wide citrus quarantine by the United States Department of Again, molecular genetic tools were used to determine the Agriculture (USDA) and no citrus (trees, fruit, rootstocks, strain of X. citri subsp. citri responsible for this outbreak. leaves, potted citrus plants, etc.), whether commercial or It was the same strain as the 1986–1992 outbreak in the dooryard, may leave the state unless the USDA has issued same area. These data suggested some infections had gone a limited permit. Quarantine regulations change frequently undetected during the earlier eradication efforts. but can be accessed through the Citrus Health Response Program website (see Resources), including information on Another simultaneous outbreak was detected in the Immo- which packinghouses will grade homeowner fruit. These kalee area of southwest Florida in 1998. As new outbreaks regulatory efforts are in place to limit the spread of citrus occurred, the bacterial isolates were genetically character- canker beyond those areas already infected and to control ized by researchers. With the exception of the 1986 and the severity of infections within affected areas. Much of 1997 Manatee County outbreaks, all of these new outbreaks Florida now has citrus canker, but the northern third of the were caused by the strain of the pathogen detected in 1995 peninsula and the eastern panhandle remain canker free for near the Miami airport. now.

Although eradication efforts continued, legal battles over the forced removal of infected trees hampered the effort. Citrus Canker Symptoms The paths of hurricanes during the very active hurricane All above-ground tissues of citrus trees are susceptible to season of 2004 (Figure 1), followed by more hurricanes in infection by citrus canker when young. Canker symptoms 2005, spread the disease from the original affected areas in appear on fruit, leaves, and stems and vary in appearance southeast Florida throughout most of the citrus-growing depending on the age and severity of the infection (Figure areas of the state. In January 2006, it was determined that 2). Severe infections can cause defoliation, stem dieback, eradication of citrus canker from Florida was no longer fruit drop, general tree decline, and result in very unap- feasible, and eradication efforts ceased. Containment within pealing fruit. Trees with persistent, severe infections can Florida to minimize further spread became paramount. become weak and unproductive.

Figure 2. Canker symptoms on a citrus leaf (upper left), stem (right), and fruit (lower left). Credits: Leaf and stem: UF/IFAS; Fruit: Jim Graham, UF/IFAS Figure 1. Map showing the paths of Hurricanes Charlie, Frances, and Jeanne in 2004. The red, outlined areas indicate the Citrus Canker Leaf Symptoms Eradication Program (CCEP) quarantine areas prior to the hurricanes. The hurricanes followed paths that spread the canker causing- The bacteria enter plant tissues through natural openings bacterium from infected areas to non-infected areas. (e.g. stomates—pores in leaf surfaces) and wounds. Early Credits: Compiled by the Florida Department of Agriculture leaf symptoms appear as tiny, slightly raised, blister-like

Dooryard Citrus Production: Asiatic Citrus Canker Disease 2 lesions (Figure 3). These lesions can develop water-soaked margins. The time from infection to symptom appearance will depend on environmental conditions. Under ideal conditions, that is, the presence of moisture and tempera- tures between 68–86°F (20–30°C), lesion development will occur 10–14 days after inoculation. Under very unfavorable conditions, symptoms may take as long as 60 days to appear. As young, blister-like lesions age, they change color, Figure 5. Older canker lesions on leaves develop a raised, corky appearance. Note the water-soaking around the perimeter of each turning tan to brown, and the area immediately surround- lesion. ing the lesion can have a water-soaked appearance with a Credits: Mongi Zekri, UF/IFAS yellow halo (Figure 4). The centers of the lesions become raised and corky (Figure 5) and lesions are visible on both sides of the leaf. The centers of large, old lesions may fall out, leaving holes in the leaf, a symptom known as shot- hole (Figure 6).

Figure 6. An older canker lesion where the center has fallen out (see arrows) as the tissue at the center of the lesion dies. Credits: Jamie Burrow, UF/IFAS The disease severity of citrus canker can be greatly increased by the citrus leafminer (Phyllocnistis citrella), a tiny moth that provides entry points for the bacterium. Figure 3. Young canker lesions on leaves have a blister-like appearance Leaves damaged by citrus leafminer become more sensi- with water-soaked margins. Photo is magnified to show detail of tive to canker infection because leafminer wounds allow lesions. easy penetration of the bacterium into the leaf tissue and Credits: USDA because they heal more slowly than other types of wounds (Figure 7). Citrus canker lesions caused by the infection of leafminer feeding galleries are larger and more numerous than when infections occur through natural openings. These large lesions result in the production of very high inoculum levels for more infections as the bacteria repro- duce. Additional information can be found in the EDIS publication on Citrus Leafminer available online at http:// edis.ifas.ufl.edu/IN165.

Stem and Twig Symptoms Because stems and twigs are less susceptible to infection than leaves, the presence of citrus canker lesions on stems and twigs generally indicates an infection has been present for some time. Stem lesions can serve as a reservoir of inoculum that can continue to re-infect new tissues as they Figure 4. Young canker lesions on leaves with prominent yellow haloes are produced. Symptoms on stems and twigs are generally and water-soaked margins. dark brown, raised, corky lesions which when young, may Credits: Mongi Zekri, UF/IFAS

Dooryard Citrus Production: Asiatic Citrus Canker Disease 3 have an oily or water-soaked appearance around the edges (Figure 8, top). Stem lesions do not usually have the yellow halo typical of leaf lesions. As the lesions on stems age they begin to appear more dried out and take on a scabby appearance (Figure 8 bottom).

Figure 7. Canker lesions develop along the tunnels of citrus leafminer damage. Figure 9. Canker lesions on fruit with a yellow halo, similar to leaf Credits: Mongi Zekri, UF/IFAS lesions. Credits: Jamie Burrow, UF/IFAS

Figure 10. Comparison of the appearance of citrus canker lesions on (left) and sweet (right). Credits: Jamie Burrow, UF/IFAS Other Diseases Figure 8. Canker lesions on stems are generally dark brown and raised. Other diseases of citrus, such as citrus scab, melanose, Young lesions may have a water-soaked or oily appearance around greasy spot, , and alternaria brown spot, the edges. Older lesions appear dry and have a scab-like appearance. have symptoms that may at first be mistaken for citrus Credits: UF/IFAS canker (Figure 11). However, upon closer inspection these Fruit Symptoms diseases can be distinguished quite easily from citrus canker. Lesions on fruit, similar to those on stems, tend to be dark brown and raised, and are frequently surrounded by a Scab infections begin as small, pale pink, somewhat yellow halo (Figure 9). The appearance of fruit symptoms circular, elevated spots on leaves and fruit. As the infection differs slightly depending on the citrus variety (Figure 10). develops, the spots become wart-like and, depending on Canker lesions on fruit may cause premature fruit drop, variety, can become highly raised. The crests of the wart- thus reducing fruit yield and giving the fruit an unappeal- like growths usually become covered with a corky pale ing appearance. However, canker lesions on fruit are only tissue and can flatten as the fruit matures, especially on “skin deep”, and the fruit is still edible. grapefruit. Scab is very rarely seen on sweet oranges and is most common on or mandarin varieties.

Dooryard Citrus Production: Asiatic Citrus Canker Disease 4 point of entry for the bacterium and lead to an infection. Wounds can be caused by physical means, such as pruning, thorn punctures, or by plant pests, such as citrus leafminer.

Figure 12. Canker lesions developing on young fruit (left) and leaves (right) showing the susceptibility of these immature tissues. Figure 11. Citrus fruit with symptoms of citrus scab (top left), melanose Credits: UF/IFAS (left) and Mongi Zekri, UF/IFAS (right) (top middle), and alternaria brown spot (top right). Citrus black spot hard spot symptoms (bottom). The disease cycle of citrus canker, showing infection and Credits: Jamie Burrow, UF/IFAS scab and alternaria brown spot, UF/ IFAS melanose, Megan Dewdney, UF/IFAS citrus black spot spread, is illustrated in Figure 13. Wind-driven rain is the primary mechanism for movement over short to medium Melanose lesions are small (~1/32”; > 1 mm), raised, and distances. A rain drop can carry millions of bacteria. These irregularly shaped spots on the fruit or leaf surface, ranging rain drops can then flow into leaf pores called stomates, from brick red to black, that feel like sandpaper when introducing the bacteria to the internal leaf tissues where it touched. They commonly will cover a quarter to one half causes infection. of the surface of the fruit. Melanose occurs on any citrus variety that has dead wood in the canopy but is particularly common on grapefruit varieties.

Alternaria brown spot infections on fruit appear as small, slightly depressed black spots that can cause the young fruit to fall from the tree. Alternaria lesions may also be surrounded by a yellow halo, similar to canker; however, the depressed lesions distinguish it from canker. Alternaria brown spot is mainly found on tangerine varieties, espe- cially Minneola (Honeybell), and much less frequently on grapefruit. It is never seen on sweet orange.

Citrus black spot has four symptom types, but the most common and most likely to be confused with citrus canker is the hard spot symptom. The hard spot lesions on fruit are sunken with pycnidia (small, pencil-sized dots) in the center of the lesions. Sometimes green halos surround the Figure 13. Flow diagram illustrating the citrus canker disease cycle hard spot lesions. The hard spot lesions most commonly and the contribution of wind-blown rain to spreading the infection (Gottwald et al 2002). occur on mature fruit and are most common on sweet oranges and but all varieties can get the disease. Long-distance spread of citrus canker occurs primarily through human activity, via the movement of infected plant Citrus Canker Infection and Spread material, equipment, clothing, or even cell phones and cell phone cases. Other natural events, such as hurricanes, can For X. citri subsp. citri to cause an infection, it must be able transport bacteria long distances. to enter plant tissues. For this reason, young leaves, stems, and fruit (Figure 12) are highly susceptible to natural infec- tions because they have not yet fully developed their natural Citrus Canker Management protective layer, called the cuticle. Once these tissues have As of January 2006, citrus canker eradication efforts have matured and “hardened-off,” infection is unlikely. However, been suspended. This means the removal of infected citrus wounding any of these tissues, young or old, can provide a trees and all other citrus trees within a 1,900 foot radius

Dooryard Citrus Production: Asiatic Citrus Canker Disease 5 of infected trees is no longer required. However, under time because another, more serious disease, Huanglongbing the USDA statewide quarantine, no citrus may leave the (HLB; citrus greening) causes the young trees to rapidly state of Florida without a USDA-issued limited permit. decline. It is very difficult for a homeowner to protect their These restrictions apply to commercially grown as well as citrus trees from HLB and these trees, which will almost residential citrus, and apply to all plant material, not just assuredly become infected, contribute to the further spread fruit. These rules may change in the future and the Florida of HLB that is imperiling the Florida citrus industry. Department of Agriculture and Consumer Services, Divi- sion of Plant Industry (FDACS, DPI) Citrus Quarantine Controlling Existing Infections Information website (http://www.freshfromflorida.com/ Once a canker lesion occurs, the lesion cannot be cured. Divisions-Offices/Plant-Industry/Agriculture-Industry/ However, because the bacterium is not systemic within the Citrus-Health-Response-Program/Citrus-Quarantine- plant, the bacteria can be prevented from spreading beyond Information) should be consulted for the most current that lesion and creating a more severe infection on the rest quarantine information. of the tree. That is, the bacteria do not move within the plant; they are restricted to the lesion itself unless moved by Preventing Infection water or some other physical means. When working in your yard, you should take precautions to avoid infecting your trees or spreading the disease from one If you find citrus canker on your trees, the best thing you tree to another. Your hands and gardening tools should be can do is try to suppress the disease if it is limited to a disinfested while working in your yard to help prevent the relatively small area (e.g. a single branch or a few fruit). This spread of the disease if one of your trees is infected. If you can be easily done by pruning away the infected portion borrow gardening tools from a friend, disinfest prior to us- of the tree. The remaining portion of the tree should be ing them on your citrus trees and before you return them. It monitored carefully for any new infections and they should is best to practice personal and equipment decontamination be removed as soon as they are detected. Citrus canker between trees. bacteria can easily survive from one season to the next in old lesions on fruit, leaves, and stems, especially in Florida’s To remove the bacterium from the skin, wash hands and climate. Thus, removing infected plant material reduces arms with soap and water, hot or cold, for a minimum of 20 inoculum sources and the potential for new infections. Any seconds. The use of an alcohol-based hand-sanitizer after material removed from a plant that has citrus canker should hand-washing will make personal decontamination more be sealed inside a double plastic bag before being disposed effective. Tools should be decontaminated with a solution of in the trash. Do not place canker-infected plant material of 1 ounce household bleach to 1 gallon of water. To reduce in compost piles or horticultural waste because this will the risk of rusting, tools should be rinsed afterwards. not kill the bacteria and may allow for easy spread of the The bleach solution will not be effective if used on dirty disease. equipment and should be made fresh daily because it loses effectiveness quickly. Disease spread can also occur The only chemical products that are effective for canker via clothing, so it is best to wash or change clothing after control are copper-based fungicides/bactericides. However, handling citrus trees and when switching between yards. these products act only as a chemical barrier against canker infection, not systemically. Therefore, if one of these At this time, homeowners may replant citrus trees products is applied to a young leaf or fruit, that leaf or fruit anywhere in Florida, regardless of past citrus canker will only be protected as long as the copper coating remains quarantine areas. However, in an effort to control citrus intact. The copper only coats the surface, and when the canker and other diseases, the FDACS has implemented plant surface expands, the coating is no longer intact and strict regulations for propagating and selling citrus trees in the new exposed tissue is again susceptible to infection. Florida. New citrus trees must be purchased from certified Because of the rapid expansion of the citrus tissue, it is dif- nurseries registered with the state. Every citrus tree sold in ficult to protect the fruit with copper, especially grapefruit. Florida must have a tag on it that identifies the nursery that It is nearly impossible to protect leaves to which copper is produced the tree by name and state registration number. applied less often than once every three weeks during the Do not buy a citrus tree without this certification tag. early summer growing period (Table 1). Often, homeown- ers find they are not able to apply copper as frequently as Florida residents should be aware that UF/IFAS is not en- needed and do not bother. However, if you choose to use couraging the planting of new residential citrus trees at this

Dooryard Citrus Production: Asiatic Citrus Canker Disease 6 chemical control, you must follow and comply with all label Although it is no longer governed by the strict rules that directions for the products you are using. were in place during eradication, citrus canker is still a Table 1. Copper management program indicating citrus fruit serious disease of citrus. The disease has become endemic types and periods in which to implement or schedule copper in many parts of the state, but it is still possible to restrict sprays. its spread beyond these areas. North Florida and parts of Early Oranges April–Mid-July the Panhandle are still canker free. Citrus canker is highly Grapefruit April–Mid-October contagious and can easily be spread by human activity, ‘Valencia’ April–June further threatening what is a hallmark of the Florida and hybrids April–June landscape—citrus. Homeowners should be familiar with disease symptoms and regularly inspect their dooryard trees for citrus canker infections. No citrus, including fruit, Diagnosing Citrus Canker potted trees, or cuttings, should be moved into or out of If you are unsure whether a disorder on your citrus tree is Florida without first checking the most current quarantine citrus canker, please contact your local UF/IFAS Extension regulations on the FDACS, DPI website. Through vigilance office (visit http://solutionsforyourlife.ufl.edu to find your on the part of homeowners and commercial citrus growers local office) or the FDACS, DPI Helpline (1-800-282-5153). alike, citrus canker can be controlled and Florida’s citrus They may ask you to e-mail them a digital photo of the trees can be protected. symptomatic tissue for positive identification. If a positive identification cannot be made in this way or you are unable Additional Information to provide them a photo, you may be asked to bring a Dewdney, M.D., P.D. Roberts, J.H. Graham, K.R. Chung sample to the office. If you bring a sample to the county and M. Zekri. 2009. Homeowner Fact Sheet: Citrus Canker. extension office it should be sealed inside two clear plastic PP194. Gainesville: University of Florida Institute of Food zip-top bags to prevent the possibility of spreading the and Agricultural Sciences. http://edis.ifas.ufl.edu/pp116 disease. Do not transport suspect material without being specifically asked to do so and without first double-bagging Gottwald, T.R., J.H. Graham, and T.S. Schubert. 2002. the sample. “Citrus Canker: The pathogen and its impact.” Online.Plant Health Progress. http://www.plantmanagementnetwork.org/ Susceptible Varieties pub/php/review/citruscanker/ Citrus canker affects all types of citrus, but there is some variability in the disease severity depending on the variety Gottwald, T.R., and M. Irey. 2007. “Post-hurricane analysis of citrus grown. A general ranking of varietal susceptibility, of citrus canker II: Predictive model estimation of disease from most susceptible to least susceptible is shown in Table spread and area potentially impacted by various eradication 2. protocols following catastrophic weather events.” Online. Plant Health Progress. http://www.plantmanagementnet- Table 2. General ranking of susceptibility to citrus work.org/sub/php/research/2007/hurricane/ canker from most susceptible to least susceptible (resistant). Highly Susceptible Heppner, J.B. and T.R. Fasula. Citrus Leafminer. 2013. Grapefruit Key Phyllocnistis citrella Stainton (Insecta: Lepidoptera: Phyl- locnistinae). EENY038. Gainesville: University of Florida Susceptible Institute of Food and Agricultural Sciences. http://edis.ifas. Hamlin Orange Persian/Tahiti Lime ufl.edu/IN165. Navel Orange Hoy, M.A., L. Zappala, and R. Nguyen. 2014. Parasitoid Less Susceptible of the Citrus Leafminer, Semielacher petiolatus (Girault) (Insecta: Hymenoptera: Eulophidae). EENY-313. Gainesville: Mandarin/Tangerine hybrids University of Florida Institute of Food and Agricultural Resistant Sciences. http://edis.ifas.ufl.edu/IN589. Calamondin Mandarins

Dooryard Citrus Production: Asiatic Citrus Canker Disease 7 Irey, M., T.R. Gottwald, J.H. Graham, T.D. Riley, and G. Carlton. 2006. “Post-hurricane analysis of citrus canker spread and progress towards the development of a predic- tive model to estimate disease spread due to catastrophic weather events.” Online. Plant Health Progress. http://www. plantmanagementnetwork.org/pub/php/research/2006/ canker/ Resources Citrus Health Response Program http://www.fresh- fromflorida.com/Divisions-Offices/Plant-Industry/ Agriculture-Industry/Citrus-Health-Response-Program

Shipping Home Grown Citrus Fruit from Florida http://www.freshfromflorida.com/content/down- load/24077/487192/Homeowner_Fruit_Packinghouses.pdf

Dooryard Citrus Production: Asiatic Citrus Canker Disease 8