Citrus greening disease

Bacterial disease of citrus, bug-borne

Citrus greening disease

Citrus greening disease on mandarin oranges

Common names| HLB, citrus vein phloem degeneration (CVPD), citrus greening disease, yellow shoot disease, yellow dragon disease, leaf mottle yellows in the Philippines, citrus dieback in India
Causal agents| Liberibacter spp. (L. asiaticus, L. africanus, L. americanus)[1]
Hosts| citrus trees
Vectors| Diaphorina citri, Trioza erytreae
EPPO Code| 1LIBEG
Distribution| Asia, Africa, United States
Orange juice prices 1973 - 2022
Citrus greening was first found in 2005 in the US and has cut the Orange tree production in half[2][3]

Citrus greening disease or yellow dragon disease[4] (calque of Chinese: 黃龍病; pinyin: huánglóngbìng abbr. HLB)[5] is a disease of citrus caused by a vector-transmitted pathogen. 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, also known as the two-spotted citrus psyllid. It has no known cure.[6] It has also been shown to be graft-transmissible.[7]

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 South China[1] 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.[8]

## Symptoms[edit]

HLB is distinguished by the common symptoms of yellowing of the veins and adjacent tissues (hence the "yellow dragon" name given by observing Chaozhou 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.[10] 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.[11]

## Transmission[edit]

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.[12] For example, citrus crops in Africa become infected under cool conditions as the bacteria are transmitted by the African citrus psyllid Trioza erytreae,[13] an invasive 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.[14][15]

The young larval stage is the most suitable for acquisition of ca. L. asiaticus by the Asian citrus psyllid Diaphorina citri,[15] and some cultivars show greater efficiency in transmitting the disease to the vector than others.[16] 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.[16]

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.[17] 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.[18]

## Distribution[edit]

Diaphorina citri

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[19][20][21][22][23] On March 30, 2012, citrus greening disease was confirmed in a single citrus tree in Hacienda Heights, Los Angeles County, California.[24] 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.[25] 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.[26]

The distribution of the African citrus psyllid includes Africa, Madeira, Saudi Arabia, Portugal, and Yemen.[27] 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.[28]

## Control[edit]

Some cultural practices can be effective in managing this disease. Cultural methods include antibacterial management, sanitation, removal of infected plants, frequent scouting, and most importantly, crisis declaration.[29] 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 that may attract psyllids to citrus plants in the vicinity such as Murraya paniculata, Severinia buxifolia, and other plants in the family Rutaceae.[30]

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.[31]

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.[32] 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.[33] Field tests by Southern Gardens Citrus of oranges with the spinach genes in Florida are ongoing.[32]

A resistant variety of mandarin orange called 'Bingo' has been bred at the University of Florida.[34] Other varieties can have a partial tolerance to the disease.[35]

### Antibiotics[edit]

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.[36] In June 2014, the USDA allocated an additional US$31.5 million to expand research combating citrus greening disease.[37]

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.[38] 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.[38][39] 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 affect human health.[38][39]

### Peptide[edit]

University of California scientists have discovered a peptide that prevented and treated citrus greening disease in greenhouse trials; as of 2021[update], it is being tested in field trials.[40][41] The university entered into an exclusive license with Invaio to develop an enhanced injectable version of the product.[42]

### Cover crops[edit]

Some success has been reported using a cover crop strategy.[43] The citrus trees were not free of the disease bacteria, yet a healthy soil environment allowed them to produce fruit and remain profitable.[citation needed]

## See also[edit]

* Citrus black spot
* Plant pathology

## References[edit]

1. ^ a b c Bové, J. M. (2006). "Huanglongbing: A destructive, newly emerging, century-old disease of citrus". J. Plant Pathol. 88 (1): 7–37.
2. ^ "FE983/FE983: Impact of Citrus Greening on Citrus Operations in Florida".
3. ^ "Researchers Find Possible Answer to Citrus Greening". 14 February 2021.
4. ^ "Citrus greening". Animal and Plant Health Inspection Service. Retrieved 21 September 2023.
5. ^ "The Disease: Huanglongbing (HLB)". Citrus Research Board. Archived from the original on 17 January 2011. Retrieved 29 November 2010.
6. ^ Killiny, Nabil; Nehela, Yasser; George, Justin; Rashidi, Mahnaz; Stelinski, Lukasz L.; Lapointe, Stephen L. (2021-07-01). "Phytoene desaturase-silenced citrus as a trap crop with multiple cues to attract Diaphorina citri, the vector of Huanglongbing". Plant Science. 308: 110930. doi:10.1016/j.plantsci.2021.110930. ISSN 0168-9452. PMID 34034878. S2CID 235203508.
7. ^ Lin, K. H. 1956. Observation on yellow shoot on citrus. Etiological studies of yellow shoot on Citrus. Acta Phytopathological Sinica 2:1–42.
8. ^ "Can Genetic Engineering Save the Florida Orange?". 13 September 2014. Archived from the original on September 15, 2014. Retrieved 17 June 2017.
9. ^ Li, Xue; Ruan, Huaqin; Zhou, Chengqian; Meng, Xiangchun; Chen, Wenli (2021). "Controlling Citrus Huanglongbing: Green Sustainable Development Route Is the Future". Frontiers in Plant Science. 12. doi:10.3389/fpls.2021.760481. ISSN 1664-462X. PMC 8636133. PMID 34868155.
10. ^ Hong-Ji Su (2001-02-01). "Citrus Greening Disease". Food & Fertilizer Technology Center. Retrieved 2014-05-18.
11. ^ "UF/IFAS Citrus Extension: Plant Pathology". Crec.ifas.ufl.edu. Archived from the original on 14 April 2021. Retrieved 17 June 2017.
12. ^ Andrew Paul Gutierrez and Luigi Ponti 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
13. ^ "Trioza erytreae (African citrus psyllid)". Cabi.org. Retrieved 17 June 2017.
14. ^ "CISR: Asian Citrus Psyllid". Cisr.ucr.edu. Retrieved 17 June 2017.
15. ^ a b Wu, 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. ISSN 0022-0493. PMID 30010958. S2CID 51628267.
16. ^ a b Wu, Fengnian; Huang, Jiaquan; Xu, Meirong; Fox, Eduardo G P; Beattie, G Andrew C; Holford, Paul; Cen, Yijing; Deng, Xiaoling (December 2018). "Host and environmental factors influencing ' candidatus Liberibacter asiaticus' acquisition in Diaphorina citri: Interactions between D. citri and ' candidatus Liberibacter asiaticus'". Pest Management Science. 74 (12): 2738–2746. doi:10.1002/ps.5060. PMID 29726075. S2CID 19098533.
17. ^ Garnier, M., S. Jagoueix-Eveillard, P. R. Cronje, G. F. LeRoux, and J. M. Bové. 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.
18. ^ Lallemand, J., A. Fos, and J. M. Bové. 1986. Transmission de la bacterie associé à la forme africaine de la maladie du "greening" par le psylle asiatique Diaphorina citri Kuwayama. Fruits 41: 341–343.
19. ^ "Detection of Huanglongbing (Candidatus Liberibacter asiaticus) in the municipality of Tizimin, Yucatan, Mexico". North American Plant Protection Organization's Phytosanitary Alert System. Retrieved 2010-10-02.
20. ^ "Update on the detection of Huanglongbing (Candidatus Liberibacter asiaticus) in backyard trees in the States of Yucatan and Quintana Roo, Mexico". North American Plant Protection Organization's Phytosanitary Alert System. Retrieved 2010-10-02.
21. ^ "Update on the detection of Huanglongbing (Candidatus Liberibacter asiaticus) in backyard trees in Mexico". North American Plant Protection Organization's Phytosanitary Alert System. Retrieved 2010-10-02.
22. ^ "Detection of Huanglongbing (Candidatus Liberibacter asiaticus) in the Municipality of Calakmul, Campeche, Mexico". North American Plant Protection Organization's Phytosanitary Alert System. Retrieved 2010-10-02.
23. ^ "Detection of Huanglongbing (Candidatus Liberibacter asiaticus) in the Municipalities of Mazatlan and Escuinapa, Sinaloa, Mexico". North American Plant Protection Organization's Phytosanitary Alert System. Retrieved 2010-10-02.
24. ^ "CITRUS DISEASE HUANGLONGBING DETECTED IN HACIENDA HEIGHTS AREA OF LOS ANGELES COUNTY" (Press release). California Department of Food and Agriculture. March 30, 2012. Retrieved April 18, 2012.
25. ^ 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.
26. ^ Ian Lovett (April 17, 2012). "Threat to California Citrus May Finish Backyard Trees". The New York Times. Retrieved April 18, 2012.
27. ^ "(EPPO/ CABI) European and Mediterranean Plant Protection Organization/Centre for Agricultural Bioscience International. 1979. EPPO data sheet on quarantine organisms, No. 46, Trioza erytreae" (PDF). Archived from the original (PDF) on 13 July 2010. Retrieved 17 June 2017.
28. ^ Citrus greening bacterium (PDF). Data Sheets on Quarantine Pests (Report). Archived from the original (PDF) on March 9, 2016. Retrieved March 6, 2022.
29. ^ "UF/IFAS Citrus Extension: Plant Pathology". Crec.ifas.ufl.edu. Archived from the original on 13 April 2021. Retrieved 17 June 2017.
30. ^ "UF/IFAS Citrus Extension: Plant Pathology". Crec.ifas.ufl.edu. Archived from the original on 2 December 2020. Retrieved 17 June 2017.
31. ^ Blaustein, Ryan A.; Lorca, Graciela L.; Teplitski, Max (2018-01-24). "Challenges for Managing Candidatus Liberibacter spp. (Huanglongbing Disease Pathogen): Current Control Measures and Future Directions". Phytopathology. 108 (4): 424–435. doi:10.1094/phyto-07-17-0260-rvw. PMID 28990481.
32. ^ a b Amy Harmon (July 27, 2013). "A Race to Save the Orange by Altering Its DNA". The New York Times. Retrieved July 28, 2013.
33. ^ R-Santaana (26 March 2012) Spinach genes may stop deadly citrus disease Agrilife Today, Texas A&M, Retrieved 1 October 2012
34. ^ Allen, Greg (4 December 2016). "After A Sour Decade, Florida Citrus May Be Near A Comeback". NPR. Retrieved 10 February 2017.
35. ^ "Promising new citrus varieties for greening tolerance". ScienceDaily. Retrieved 5 December 2019.
36. ^ Dennis O'Brien (2010-04-26). "Periwinkle Plants Provide Ammunition in the War on Citrus Greening". USDA Agricultural Research Service. Retrieved 2014-05-18.
37. ^ "$31.5mn allocated by USDA for research to fight citrus fruit disease". canadianbusiness.com. Archived from the original on 4 July 2015. Retrieved 12 June 2014.
38. ^ a b c Andrew Jacobs (May 17, 2019). "Citrus Farmers Facing Deadly Bacteria Turn to Antibiotics, Alarming Health Officials". The New York Times. Retrieved June 5, 2019.
39. ^ a b "Antibiotic Use on Oranges Gets Trump Administration's Approval". Center for Biological Diversity. December 10, 2018. Retrieved June 6, 2019.
40. ^ Huang, Chien-Yu; Araujo, Karla; Sánchez, Jonatan Niño; Kund, Gregory; Trumble, John; Roper, Caroline; Godfrey, Kristine Elvin; Jin, Hailing (2021-02-09). "A stable antimicrobial peptide with dual functions of treating and preventing citrus Huanglongbing". Proceedings of the National Academy of Sciences. 118 (6): e2019628118. Bibcode:2021PNAS..11819628H. doi:10.1073/pnas.2019628118. ISSN 0027-8424. PMC 8017978. PMID 33526689.
41. ^ Wang, Nian (2021-02-09). "A promising plant defense peptide against citrus Huanglongbing disease". Proceedings of the National Academy of Sciences. 118 (6): e2026483118. Bibcode:2021PNAS..11826483W. doi:10.1073/pnas.2026483118. ISSN 0027-8424. PMC 8017718. PMID 33526706.
42. ^ Bernstein, Jules (July 7, 2020). "UC Riverside discovers first effective treatment for citrus-destroying disease". University of California Riverside.
43. ^ Popenoe, Juanita; Diepenbrock, Lauren (2019-04-02). "Citrus Industry Magazine". Citrus Industry Magazine. Retrieved 2022-07-17.

## Further reading[edit]

* Singerman, Ariel; Useche, Pilar (2019-02-26). "FE983/FE983: Impact of Citrus Greening on Citrus Operations in Florida". University of Florida Institute of Food and Agricultural Sciences Electronic Data Information Source. Retrieved 2021-02-16.

## External links[edit]

Look up citrus greening disease in Wiktionary, the free dictionary.

* Asian citrus psyllid on the UF / IFAS Featured Creatures Web site
* Species Profile – Citrus Greening and Species Profile – Asian Citrus Psyllid, National Invasive Species Information Center, National Agricultural Library. 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

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