Citrus greening disease ( abbr. HLB) is a disease of

citrus ''Citrus'' is a genus of flowering trees and shrubs in the family Rutaceae. Plants in the genus produce citrus fruits, including important crops such as oranges, mandarins, lemons, grapefruits, pomelos, and limes. ''Citrus'' is nativ ...

caused by a

vector Vector most often refers to: * Euclidean vector, a quantity with a magnitude and a direction * Disease vector, an agent that carries and transmits an infectious pathogen into another living organism Vector may also refer to: Mathematics a ...

-transmitted

pathogen In biology, a pathogen (, "suffering", "passion" and , "producer of"), in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a Germ theory of d ...

. The causative agents are motile bacteria, '' Liberibacter'' spp. The disease is transmitted by the Asian citrus psyllid, '' Diaphorina citri'', and the African citrus psyllid, '' Trioza erytreae''. It has no known cure. It is graft-transmissible. There are three different types of the disease: a heat-tolerant Asian form, and the heat-sensitive African and American forms. It was first described in 1929, and first reported in

South China South China ( zh, s=, p=Huá'nán, j=jyut6 naam4) is a geographical and cultural region that covers the southernmost part of China. Its precise meaning varies with context. A notable feature of South China in comparison to the rest of China is ...

in 1943. The African variation was first reported in 1947 in

South Africa South Africa, officially the Republic of South Africa (RSA), is the Southern Africa, southernmost country in Africa. Its Provinces of South Africa, nine provinces are bounded to the south by of coastline that stretches along the Atlantic O ...

, where it is still widespread. It reached

Florida Florida ( ; ) is a U.S. state, state in the Southeastern United States, Southeastern region of the United States. It borders the Gulf of Mexico to the west, Alabama to the northwest, Georgia (U.S. state), Georgia to the north, the Atlantic ...

in 2005, and within three years had spread to the majority of citrus farms. The rapid increase in this disease has threatened the citrus industry in the entire US. As of 2009, 33 countries had reported the infection in their citrus crop.

Symptoms

Citrus greening is distinguished by the common symptoms of yellowing of the

vein Veins () are blood vessels in the circulatory system of humans and most other animals that carry blood towards the heart. Most veins carry deoxygenated blood from the tissues back to the heart; exceptions are those of the pulmonary and feta ...

s and adjacent tissues (hence the "yellow dragon" name given by observing Chaozhou farmers as early as the 1870s); 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 be mistaken for nutrient deficiencies; the distinguishing factor 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.

Transmission

Citrus greening was originally thought to be a viral disease, but is caused by a bacterium, carried by insect vectors. 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 erytreae'', an insect that favors cool and moist conditions for optimal activity. 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 relationship between the bacteria and the insect vector, affecting how it is acquired and transmitted by the insects. The causative agents are fastidious

phloem Phloem (, ) is the living tissue in vascular plants that transports the soluble organic compounds made during photosynthesis and known as ''photosynthates'', in particular the sugar sucrose, to the rest of the plant. This transport process is ...

-restricted,

Gram-negative bacteria Gram-negative bacteria are bacteria that, unlike gram-positive bacteria, do not retain the Crystal violet, crystal violet stain used in the Gram staining method of bacterial differentiation. Their defining characteristic is that their cell envelo ...

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

Distribution of the Asian citrus psyllid is primarily in

tropical The tropics are the regions of Earth surrounding the equator, where the sun may shine directly overhead. This contrasts with the temperate or polar regions of Earth, where the Sun can never be directly overhead. This is because of Earth's ax ...

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 The , also known as the or the , are a chain of Japanese islands that stretch southwest from Kyushu to Geography of Taiwan, Taiwan: the Ryukyu Islands are divided into the Satsunan Islands (Ōsumi Islands, Ōsumi, Tokara Islands, Tokara and A ...

, Nepal, Saudi Arabia, and Afghanistan. Areas outside Asia have also reported the disease:

Réunion Réunion (; ; ; known as before 1848) is an island in the Indian Ocean that is an overseas departments and regions of France, overseas department and region of France. Part of the Mascarene Islands, it is located approximately east of the isl ...

, Mauritius, Brazil, Paraguay, and

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

California California () is a U.S. state, state in the Western United States that lies on the West Coast of the United States, Pacific Coast. It borders Oregon to the north, Nevada and Arizona to the east, and shares Mexico–United States border, an ...

. The first report of HLB in Texas occurred on January 13, 2012, from a Valencia sweet orange tree in a commercial orchard in 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 a vector of the African strain of ''huanglongbing'' (''Candidatus'' Liberibacter africanus), which is sensitive to heat. This strain 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 as of 2004.

Control

Some cultural practices are effective in managing this disease. Cultural methods include antibacterial management, sanitation, removal of infected plants, frequent scouting, and most importantly, crisis declaration. Tracking the disease can 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 that may attract psyllids to citrus plants in the vicinity such as ''Murraya paniculata'', ''Severinia buxifolia'', and other plants in the family

Rutaceae The Rutaceae () is a family (biology), family, commonly known as the rueRUTACEAE
in Bo ...

. 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 ('' 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. The effort to culture ''Candidatus Liberibacter asiaticus'' (CLas) has been a significant challenge in plant pathology. Progress has included culturing a different species of ''Liberibacter''. 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. A resistant variety of

mandarin orange A mandarin orange (''Citrus reticulata''), often simply called mandarin, is a small, rounded citrus tree fruit. Treated as a distinct species of orange, it is usually eaten plain or in fruit salads. The mandarin is small and oblate, unlike the ...

called 'Bingo' has been bred at the University of Florida. Some other varieties have a partial tolerance to the disease.

Antibiotics

Researchers at the Agricultural Research Service of the

United States Department of Agriculture The United States Department of Agriculture (USDA) is an executive department of the United States federal government that aims to meet the needs of commercial farming and livestock food production, promotes agricultural trade and producti ...

have used lemon trees infected with citrus greening disease to infect periwinkle plants to study the disease. Periwinkle plants are easily infected and respond well when experimentally treated with

antibiotics An antibiotic is a type of antimicrobial substance active against bacteria. It is the most important type of antibacterial agent for fighting pathogenic bacteria, bacterial infections, and antibiotic medications are widely used in the therapy ...

. 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 the disease. Certain antibiotics, specifically

streptomycin Streptomycin is an antibiotic medication used to treat a number of bacterial infections, including tuberculosis, Mycobacterium avium complex, ''Mycobacterium avium'' complex, endocarditis, brucellosis, Burkholderia infection, ''Burkholderia'' i ...

and oxytetracycline, may be effective and have been used in the United States, but are banned in Brazil and the European Union. In 2016, the EPA allowed use of streptomycin and oxytetracycline 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 The Centers for Disease Control and Prevention (CDC) is the national public health agency of the United States. It is a United States federal agency under the Department of Health and Human Services (HHS), and is headquartered in Atlanta, ...

, primarily as antibiotic resistance can be expected to develop and affect human health.

Possible future treatments

peptide Peptides are short chains of amino acids linked by peptide bonds. A polypeptide is a longer, continuous, unbranched peptide chain. Polypeptides that have a molecular mass of 10,000 Da or more are called proteins. Chains of fewer than twenty am ...

that prevents and treats citrus greening disease in greenhouse trials was being tested in field trials in 2021; an enhanced injectable version of the product was being developed in 2020. Two types of antisense oligonucleotide (FANA and Morpholinos) can be delivered efficiently into citrus trees, suppressing their RNA targets. FANA can suppress 'Candidatus Liberibacter asiaticus' in citrus trees. Morpholinos can suppress CLas in infected citrus trees and the psyllid vectors. Furthermore, the PPMOs designed to endosymbiotic bacteria of the psyllid vectors, can reduce psyllid populations by targeting and suppressing the insects endosymbionts, the bacteria which are essential for psyllid survival. Morpholinos must be covalently linked with a charged molecule or peptide, to enter bacteria. The target RNA is made susceptible to cleavage by ribonuclease P (RNase-P).

Cover crops

Some success has been reported using a cover crop strategy. The citrus trees were not free of the disease bacteria, yet a healthy soil environment allowed them to produce fruit and remain profitable.

References

External links

Asian citrus psyllid
on the UF / IFAS Featured Creatures Web site
Species Profile – Citrus Greening
an
Species Profile – Asian Citrus Psyllid
National Invasive Species Information Center,

National Agricultural Library The United States National Agricultural Library (NAL) is one of the world's largest agricultural research libraries, and serves as a national library of the United States and as the library of the United States Department of Agriculture. Locate ...

. Lists general information and resources for citrus greening and the Asian citrus psyllid.
CISR: Huanglongbing/Citrus Greening
Center for Invasive Species Research page on Huanglongbing and Citrus Greening * https://www.aumbiotech.com/ AUM BioTech, LLC, Philadelphia, PA, USA. AUMsilence RNA silencing platform. {{Citrus Bacterial citrus diseases Bacterial tree pathogens and diseases Candidatus taxa