|Citrus greening disease|
Citrus greening disease on mandarin oranges
|Common names||HLB, citrus vein phloem degeneration (CVPD), citrus greening disease, yellow shoot disease, leaf mottle yellows in the Philippines, citrus dieback in India|
|Causal agents||Candidatus Liberibacter spp. (Liberibacter asiaticus, Liberibacter africanus,Liberibacter americanus)|
|Vectors||Diaphorina citri, Trioza erytreae|
|Distribution||Asia, Africa, United States|
Citrus greening disease (Chinese: ; pinyin: ; literally: 'yellow dragon disease'; or HLB) is a disease of citrus caused by a vector-transmitted pathogen. The causative agents are motile bacteria, Candidatus Liberibacter spp. The disease is vectored and transmitted by the Asian citrus psyllid, Diaphorina citri, and the African citrus psyllid, Trioza erytreae, also known as the two-spotted citrus psyllid. It has also been shown to be graft-transmissible. Three different types of HLB are currently known: The heat-tolerant Asian form, and the heat-sensitive African and American forms. The disease was first described in 1929 and first reported in China in 1943. The African variation was first reported in 1947 in South Africa, where it is still widespread. Eventually, it affected the United States, reaching Florida in 2005. Within three years, it had spread to the majority of citrus farms. The rapid increase in this disease has threatened the citrus industry not only in Florida, but the entire US. As of 2009, 33 countries have reported HLB infection in their citrus crop.
HLB is distinguished by the common symptoms of yellowing of the veins and adjacent tissues; followed by splotchy mottling of the entire leaf, premature defoliation, dieback of twigs, decay of feeder rootlets and lateral roots, and decline in vigor, ultimately followed by the death of the entire plant. Affected trees have stunted growth, bear multiple off-season flowers (most of which fall off), and produce small, irregularly shaped fruit with a thick, pale peel that remains green at the bottom and tastes very bitter. Common symptoms can often be mistaken for nutrient deficiencies; however, the distinguishing factor between nutrient deficiencies is the pattern of symmetry. Nutrient deficiencies tend to be symmetrical along the leaf vein margin, while HLB has an asymmetrical yellowing around the vein. The most noticeable symptom of HLB is greening and stunting of the fruit, especially after ripening.
HLB was originally thought to be a viral disease, but was later discovered to be caused by bacteria, carried by insect vectors. HLB infection can arise in various climates and is often associated with different species of psyllid insects. For example, citrus crops in Africa become infected under cool conditions as the bacteria are transmitted by the African citrus psyllid Trioza ertreae, an invasive insect that favors cool and moist conditions for optimal growth. Citrus crops in Asia, however, are often infected under warm conditions as the bacteria are transmitted by the Asian citrus psyllid Diaphorina citri.
The young larval stage is the most suitable for acquisition of Ca. L. asiaticus by the Asian citrus psyllid Diaphorina citri, and some cultivars show greater efficiency in transmitting the disease to the vector than others. Temperature also shows a great influence in the parasite-host relatioship between the bacteria and the insect vector, affecting how it is acquired and transmitted by the insects.
The causative agents are fastidious phloem-restricted, Gram-negative bacteria in the gracilicutes clade. The Asian form, Ca. L. asiaticus is heat tolerant. This means the greening symptoms can develop at temperatures up to 35 °C. The African form, Ca. L. africanus, and American form, Ca. L. americanus, are heat sensitive, thus symptoms only develop when the temperature is in the range 20-25 °C. Although T. erytreae is the natural vector of African citrus greening and D. citri is the natural vector of American and Asian citrus greening, either psyllid can in fact transmit either of the greening agents under experimental conditions.
Distribution of the Asian citrus psyllid that is a vector of the citrus greening disease, is primarily in tropical and subtropical Asia. It has been reported in all citrus-growing regions in Asia except mainland Japan. The disease has affected crops in China, India, Sri Lanka, Malaysia, Indonesia, Myanmar, the Philippines, Pakistan, Thailand, the Ryukyu Islands, Nepal, Saudi Arabia, and Afghanistan. Areas outside Asia have also reported the disease: Réunion, Mauritius, Brazil, Paraguay, and Florida in the U.S. since 2005, and in several municipalities in Mexico since 2009 On March 30, 2012, citrus greening disease was confirmed in a single citrus tree in Hacienda Heights, Los Angeles County, California. The first report of HLB in Texas occurred on January 13, 2012 from a Valencia sweet orange tree in a commercial orchard in San Juan, Texas. Prospects are bleak for the ubiquitous backyard citrus orchards of California as residential growers are unlikely to consistently use the pesticides which provide effective control in commercial orchards.
The distribution of the African citrus psyllid includes Africa, Madeira, Saudi Arabia, Portugal, and Yemen This species is sensitive to high temperatures and will not develop at temperatures greater than 25 °C. It is also a vector of the African strain of huanglongbing (Candidatus Liberibacter africanus), which is also sensitive to heat. This strain of HLB is reported to occur in Africa, (Burundi, Cameroon, Central African Republic, Comoros, Ethiopia, Kenya, Madagascar, Malawi, Mauritius, Reunion, Rwanda, South Africa, St. Helena (unconfirmed), Swaziland, Tanzania, Zimbabwe), Saudi Arabia, and Yemen. The disease was not reported in the EU or USA as of 2004; however see above.
According to UF/IFAS Citrus Extension of University of Florida, some cultural practices can be effective in monitoring this disease. Cultural methods include antibacterial management, sanitation, removal of infected plants, frequent scouting, and most importantly, crisis declaration. Tracking the disease will help prevent further infection in other affected areas and help mitigate more local infections if detected early enough. The Asian citrus psyllid has alternative hosts such as Murraya paniculata, Severinia buxifolia, and other plants in the family Rutaceae. Clearing or controlling these alternative hosts will be an important consideration as they may attract psyllids to citrus plants in the vicinity.
No cure for citrus greening disease is known, and efforts to control it have been slow because infected citrus plants are difficult to maintain, regenerate, and study. Ongoing challenges associated with mitigating disease at the field-scale include seasonality of the phytopathogen (Candidatus Liberibacter spp.) and associated disease symptoms, limitations for therapeutics to contact the phytopathogen in planta, adverse impacts of broad-spectrum treatments on plant-beneficial microbiota, and potential implications on public and ecosystem health.
Researchers from the Citrus Research and Education Center at the Institute of Food and Agricultural Sciences of University of Florida developed a strategy of early diagnosis of HLB using low-cost staining method to identify insect feeding sites and tested those identified sites for the causal agent using quantitative real-time PCR (polymerase chain reaction). Through this method, the researchers were able to detect the HLB causal agent up to two days after transmission. 
No naturally immune citrus cultivars have been identified; however, creating genetically modified citrus may be a possible solution, but questions of its acceptability to consumers exist. A researcher at Texas AgriLife Research reported in 2012 that incorporating two genes from spinach into citrus trees improved resistance to citrus greening disease in greenhouse trials. Field tests by Southern Gardens Citrus of oranges with the spinach genes in Florida are ongoing.
Citrus greening is caused by a phytoplasmas one study found that a treatment of IAA, an auxin plant hormone triggered a full recovery for periwinkle suffering from a phytoplasmas disease. IAA likely triggers plant defenses including the production of hydrogen peroxide. Phytoplasmas lack cell walls making hydrogen peroxide deadly. Some bacteria could also signal to a plant that the plant is infected activating the plant's defenses and the production of hydrogen peroxide.
Researchers at the Agricultural Research Service of the United States Department of Agriculture have used lemon trees infected with citrus greening disease to infect periwinkle plants in an effort to study the disease. Periwinkle plants are easily infected with the disease and respond well when experimentally treated with antibiotics. Researchers are testing the effect of penicillin G sodium and biocide 2,2-dibromo-3-nitrilopropionamide as potential treatments for infected citrus plants based on the positive results that were observed when applied to infected periwinkle. In June 2014, the USDA allocated an additional US$31.5 million to expand research combating citrus greening disease.
Certain antibiotics, specifically streptomycin and oxytetracycline, may be effective in the fight against citrus greening disease and have been used in the United States but have been banned in Brazil and the European Union. In 2016, the EPA allowed use of streptomycin and oxytetracyclin on orchards with citrus fruits like grapefruits, oranges and tangerines in Florida on an emergency basis, this approval was expanded and broadened to other states for oxytetracycline in December 2018. Further expansion of medically important antibiotics is proposed by the EPA but opposed by the FDA and CDC, primarily as antibiotic resistance can be expected to develop and impact human health.