Background

Citrus greening, also called Huanglongbing or yellow dragon disease, is one of the more serious diseases of citrus. This bacterial disease is thought to have originated in China in the early 1900s. The disease is primarily spread by two species of psyllid insects. One species, the Asian citrus pysllid, Diaphorina citri, has been present in Florida since 1998. The bacteria itself is not harmful to humans but the disease has harmed trees in Asia, Africa, the Arabian Peninsula, and Brazil. There are three strains of the bacteria, an Asian, an African version, and a recently described American strain discovered in Brazil.

The Asian strain, Candidatus Liberibacter asiaticus was found in Florida in early September, 2005. To respond to the problem, USDA, APHIS, PPQ and the Florida Department of Agriculture and Consumer Services deployed a Unified Command under the Incident Command Structure, and delimiting survey crews are working in southern Florida to define the extent of the problem.

Citrus greening disease is a threat to the U.S. citrus industry. Other than tree removal, there is no effective control once a tree is infected and there is no known cure for the disease. Infected trees may produce misshapen, unmarketable, bitter fruit. Citrus greening reduces the quantity and quality of citrus fruits, eventually rendering infected trees useless. In areas of world affected by citrus greening the average productive lifespan of citrus trees has dropped from 50 or more years to 15 or less. The trees in the orchards usually die 3-5 years after becoming infected and require removal and replanting. An infected tree produces fruit that is unsuitable for sale as fresh fruit or for juice.

Symptoms

Citrus plants infected by the citrus greening bacteria may not show symptoms for years following infection. Initial symptoms frequently include the appearance of yellow shoots on a tree. As the bacteria move within the tree, the entire canopy progressively develops a yellow color.

The most characteristic symptoms of citrus greening are a blotchy leaf mottle and vein yellowing that develop on leaves attached to shoots showing the overall yellow appearance. These foliar symptoms may superficially resemble a zinc deficiency although the green and yellow contrast is not as vivid with greening as it is with zinc deficiency or another disease, citrus variegated chlorosis. Leaves with citrus greening have a mottled appearance that differs from nutrition-related mottling in that greening-induced mottling usually crosses leaf veins. Nutrition related mottles usually are found between or along leaf veins and leaves may be small and upright.

Fruit from diseased trees are small, often misshapen, and typically some green color remains on ripened fruit. On Mandarin orange, fruit may develop an uneven ripening such that they appear half orange and half yellow. This symptom is the origin of the common name “greening.” Yields are almost non-existent, and remaining fruit is rendered worthless due to small size, poor color, and bad taste.

The only definitive method of diagnosis of trees suspected of infection by citrus greening pathogens is by analysis of DNA in an authorized plant diagnostic laboratory.

Disease Spread

Citrus greening pathogens can also be spread through the activities of humans by grafting with diseased budwood and by insect vectors.While citrus greening had not previously been found in the U.S., the insect that transmits citrus greening, the Asian citrus psyllid, Diaphorina citri Kuwayama, was discovered in the Florida in 1998. Surveys and testing for citrus greening in Florida has been in place since the discovery of this insect. The concern is that this insect, in the presence of the citrus greening bacteria, will spread the disease to new areas. In September 2001, the Asian citrus psyllid was found in Texas. Another vector of citrus greening is the African citrus psyllid, Trioza erytreae (Del Gercio), but this species has not been detected in the US.

Distribution

Citrus greening has been reported from the following countries in Africa, Asia and South America:

Bangladesh, Bhutan, Brazil, Burundi, Cambodia, Cameroon, Central African Republic, China, Comoros, Ethiopia, Hong Kong, India, Indonesia, Japan, Kenya, Laos, Madagascar, Malawi, Malaysia, Mauritius, Myanmar, Nepal, Pakistan, Papua New Guinea, Philippines, Reunion, Rwanda, Saudi Arabia, Somalia, South Africa, Sri Lanka, Swaziland, Taiwan, Tanzania, Thailand, Vietnam, Yemen, and Zimbabwe.

Citrus greening has not been reported from citrus-producing regions of Australia or the Mediterranean countries.

Hosts

The following is a partial list of know citrus hosts of Candidatus Liberibacter (See Halbert and Manjuath 2004 for a complete list).

Common name Scientific Name
Sweet orange** Citrus sinensis

Mandarin orange** C. reticulata
Tangelo C. paradisi X C. reticulata
Key Lime C. aurantifolia
Sour Orange* C. aurantium
Pommelo* C. maxima
Khafir lime C. hystix
Lemon* C. limon
Calamondin C. madensis
Rough lemon C. jambhiri
King Orange C. X nobilis
Grapefruit* C. X paradisi
Kumquat Fortunella spp.
Chinese box orange Severinia buxifolia
Wood apple Limonia acidissima


Uganda powder-flask Balsamocitrus dawei
Finger lime Microcitrus australisica
Trifoliate orange Poncirus trifoliata
Tabog Swinglea glutinosa
Limeberry Triphasia trifolia
Wampi Clausena lansium
Curry leaf plant M. koenegii
Clausena C. indica
* moderately susceptible
**highly susceptible

The host list above are all potentially hosts for the psyllid vector as well as the citrus greening disease, however a number of citrus relatives are also hosts for the psyllid, but have not conclusively been shown to be hosts for the disease. They are important as reservoirs or pathways for infected insect vectors to non-infested areas.

Common Name Scientific Name
Orange jasmine, (Jessamine) Murraya paniculata (preferred)
Jackfruit Artocarpus heterophyllus

Detection and Reporting

After the collection of suspect plant samples by surveyors, they are looked at by specialists within each state department of agriculture, cooperating university, or by the National Plant Diagnostic Network (NPDN) labs. The ultimate authority for confirming a diagnosis of citrus greening, since it is a select agent and exotic pest, rests with the Plant Protection and Quarantine (PPQ) division of USDA/APHIS.

More information can be found on the APHIS website:

Select Agent Program
FAQs on Select Agent Program
USDA/APHIS/PPQ permit and registration requirements for plant diseases and laboratories fall under two authorities, the Plant Protection Act (7 CFR Part 330) and the Agricultural Bioterrorism Protection Act of 2002 (7 CFR Part 331). Laboratories receiving suspect infected plant material or cultures are required to have PPQ authorizations and permits. Laboratories possessing, using, or transferring select agents such as "Candidatus" Liberibacter spp., the causal agents of citrus greening, are required to be registered, however diagnostic laboratories that identify select agents are exempt from this requirement as long as they notify PPQ complete an APHIS/CDC Form 4 and destroy the culture within 7 days.