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 inSouth China[1] in 1943. The African variation was first reported in 1947 inSouth Africa, where it is still widespread. It reachedFlorida 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.[8]
Citrus greening is distinguished by the common symptoms of yellowing of theveins and adjacent tissues (hence the "yellow dragon" name given by observingChaozhou farmers as early as the 1870s[1]); 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.[9] 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.[10]
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 ofpsyllid insects.[11] For example, citrus crops in Africa become infected under cool conditions as the bacteria are transmitted by the African citrus psyllidTrioza erytreae,[12] 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 psyllidDiaphorina citri.[13][14]
The young larval stage is the most suitable for acquisition ofca. L. asiaticus by the Asian citrus psyllidDiaphorina citri,[14] and some cultivars show greater efficiency in transmitting the disease to the vector than others.[15] 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.[15]
The causative agents are fastidiousphloem-restricted,Gram-negative bacteria in thegracilicutes 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.[16] AlthoughT. erytreae is the natural vector of African citrus greening andD. 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.[17]
Distribution of the Asian citrus psyllid is primarily intropical 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, theRyukyu Islands, Nepal, Saudi Arabia, and Afghanistan. Areas outside Asia have also reported the disease:Réunion, Mauritius, Brazil, Paraguay, andFlorida since 2005, and in several municipalities in Mexico since 2009[18][19][20][21][22] On March 30, 2012, citrus greening disease was confirmed in a single citrus tree inCalifornia.[23] The first report of HLB in Texas occurred on January 13, 2012, from a Valencia sweet orange tree in a commercial orchard in Texas.[24] 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.[25]
The distribution of the African citrus psyllid includes Africa, Madeira, Saudi Arabia, Portugal, and Yemen.[26] 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 ofhuanglongbing (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.[27]
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.[28] 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 asMurraya paniculata,Severinia buxifolia, and other plants in the familyRutaceae.[29]
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 phytopathogenin planta, adverse impacts of broad-spectrum treatments on plant-beneficial microbiota, and potential implications on public and ecosystem health.[30] The effort to cultureCandidatus Liberibacter asiaticus (CLas) has been a significant challenge in plant pathology. Progress has included culturing a different species ofLiberibacter.[31]
No naturally immune citrus cultivars have been identified; however, creatinggenetically modified citrus may be a possible solution, but questions of its acceptability to consumers exist.[32] A researcher atTexas AgriLife Research reported in 2012 that incorporating two genes from spinach into citrus trees improved resistance to citrus greening disease in greenhouse trials.[33] Field tests bySouthern Gardens Citrus of oranges with the spinach genes in Florida are ongoing.[32]
A resistant variety ofmandarin orange called 'Bingo' has been bred at the University of Florida.[34] Some other varieties have a partial tolerance to the disease.[35]
Researchers at theAgricultural Research Service of theUnited States Department of Agriculture have used lemon trees infected with citrus greening disease to infectperiwinkle plants to study the disease. Periwinkle plants are easily infected and respond well when experimentally treated withantibiotics. Researchers are testing the effect ofpenicillin G sodium andbiocide 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.[36] In June 2014, the USDA allocated an additional US$31.5 million to expand research combating the disease.[37]
Certain antibiotics, specificallystreptomycin andoxytetracycline, may be effective and have been used in the United States, but are banned in Brazil and the European Union.[38] In 2016, theEPA 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.[38][39] Further expansion of medically important antibiotics is proposed by the EPA but opposed by theFDA andCDC, primarily as antibiotic resistance can be expected to develop and affect human health.[38][39]
Apeptide that prevents and treats citrus greening disease in greenhouse trials was being tested in field trials in 2021;[40][41] an enhanced injectable version of the product was being developed in 2020.[42]
Two types ofantisense oligonucleotide (FANA and Morpholinos) can be delivered efficiently into citrus trees,[43] suppressing their RNA targets. FANA can suppress 'Candidatus Liberibacter asiaticus' in citrus trees.[44][45]
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.[46][47] 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).[48]
Some success has been reported using a cover crop strategy.[49] The citrus trees were not free of the disease bacteria, yet a healthy soil environment allowed them to produce fruit and remain profitable.[50][51]
^Gutierrez, Andrew Paul; Ponti, Luigi (2013). "Prospective Analysis of the Geographic Distribution and Relative Abundance of Asian Citrus Psyllid (Hemiptera:Liviidae) and Citrus Greening Disease in North America and the Mediterranean Basin".Florida Entomologist.96 (4):1375–1391.
^"CISR: Asian Citrus Psyllid".Center for Invasive Species Research. University of California Riverside. Retrieved17 June 2017.
^abWu, Fengnian; Qureshi, Jawwad A; Huang, Jiaquan; Fox, Eduardo Gonçalves Paterson; Deng, Xiaoling; Wan, Fanghao; Liang, Guangwen; Cen, Yijing (2018-07-12). "Host Plant-Mediated Interactions Between 'candidatus Liberibacter asiaticus' and Its Vector Diaphorina citri Kuwayama (Hemiptera: Liviidae)".Journal of Economic Entomology.111 (5):2038–2045.doi:10.1093/jee/toy182.PMID30010958.S2CID51628267.
^abWu, Fengnian; Huang, Jiaquan; Xu, Meirong; Fox, Eduardo G P; Beattie, G Andrew C; et al. (December 2018). "Host and environmental factors influencing 'candidatus Liberibacter asiaticus' acquisition inDiaphorina citri: Interactions betweenD. citri and 'candidatus Liberibacter asiaticus'".Pest Management Science.74 (12):2738–2746.doi:10.1002/ps.5060.PMID29726075.S2CID19098533.
^Garnier, M.; Jagoueix-Eveillard, S.; Cronje, P. R.; LeRoux, G. F.; Bové, J. M. (2000). "Genomic characterization of a Liberibacter present in an ornamental rutaceous tree, Calodendrum capense, in the Western Cape Province of South Africa. Proposal of 'candidatus Liberibacter africanus subsp. capensis".International Journal of Systematic and Evolutionary Microbiology (50):2119–2125.
^Lallemand, J.; Fos, A.; Bové, J. M. (1986). "Transmission de la bacterie associé à la forme africaine de la maladie du 'greening' par le psylle asiatiqueDiaphorina citri Kuwayama".Fruits (in French) (41):341–343.
^Kunta, M.; Sétamou, M.; Skaria, M.; Rascoe, J.; Li, W.; Nakhla, M.; da Graça, J.V. (2012). "First report of citrus Huanglongbing in Texas".Phytopathology (102): S4.66.
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