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Citrus greening disease
Citrus greening disease on mandarin oranges
Common namesHLB, 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 agentsLiberibacter spp. (L. asiaticus, L. africanus, L. americanus)[1]
Hostscitrus trees
VectorsDiaphorina citri, Trioza erytreae
EPPO Code1LIBEG
DistributionAsia, 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

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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

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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

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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 as of 2004[28]

Culturing

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History

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The effort to culture Candidatus Liberibacter asiaticus (CLas), a vasculature-restricted citrus pathogen associated with citrus greening disease, has been a significant challenge in plant pathology. Despite several attempts, CLas has not been successfully established in pure culture, remaining elusive compared to other fastidious bacteria associated with citrus diseases. Over the past decade, transient cultures of CLas have been reported, marking incremental progress toward its sustained cultivation. Notably, cocultivation with Propionibacterium acnes facilitated CLas growth in vitro, highlighting the potential for mutualistic bacterial relationships in supporting CLas's nutritional and chemical needs. Further experiments achieved viable CLas cultures for weeks using commercial grapefruit juice and biofilms, though these did not constitute independent cultivation. Attempts to culture CLas on Liber A medium suggested pathogenicity in citrus, yet this claim was met with skepticism and has not been reproducible. Recent efforts involving coculture with phloem-associated microbiota indicated possible growth through DNA quantification, but direct viability measures were lacking. The research underscores the complexity of CLas's nutritional and environmental requirements, suggesting that association with specific microflora is essential for its growth. Despite these advances, the cultivation of CLas remains a challenging frontier, necessitating further studies for reproducible and sustainable culture methods.

Limitations

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Unlike many bacteria, CLas demonstrates a specialized metabolic reliance on a diverse range of nutrients directly sourced from its host environments. Remarkably, CLas bypasses traditional glycolytic pathways for energy production, likely due to the absence of key glycolytic enzymes, and instead leans on alternative metabolic routes, including a dependence on the tricarboxylic acid (TCA) cycle for processing organic acids—a crucial carbon source found abundantly within the phloem sap of its plant hosts The bacterium's nutrient acquisition strategies extend to the assimilation of both proteinogenic and nonproteinogenic amino acids, as well as choline, through specialized transport systems, despite its inability to synthesize all amino acids de novo. This nuanced interaction with its environment highlights an evolved adaptation to extract and utilize host-derived nutrients, even in the face of its reduced genomic capacity. Furthermore, CLas’s exploitation of host nucleotides and cofactors through specific transport proteins underlines its sophisticated survival strategies within the host's microenvironments.

Environmental conditions also significantly impact CLas's culturability. The bacterium favors slightly acidic conditions, thriving in the naturally low pH found within citrus phloem sap and in vitro media such as commercial grapefruit juice. Additionally, CLas exhibits limited aerobic respiration capabilities, a result of lacking a terminal oxidase complex, and shows a preference for microaerophilic conditions that reflect the oxygen levels of its natural phloem habitat. These specific requirements complicate efforts to culture CLas outside its host, as the replication of these conditions in vitro is challenging. Genetic factors further constrain the cultivation of CLas. The bacterium’s genome has undergone significant reduction, losing pathways and enzymes crucial for independent growth. For example, the absence of the glyoxalase pathway, necessary for mitigating methylglyoxal toxicity, and the lack of biosynthetic pathways for essential lipids, necessitate the supplementation of culture media with specific nutrients or cofactors. Moreover, the presence of bacteriophage genes within CLas adds complexity, potentially affecting its pathogenicity and culturability. The combination of these unique growth requirements and genetic limitations underscores the inherent challenges in cultivating CLas, necessitating innovative culturing approaches to overcome these hurdles and advance our understanding of citrus greening disease. A report by Zheng et al, (2024) entitle: Towards the completion of Koch's postulates for the citrus Huanglongbing bacterium, Candidatus Liberibacter asiaticus. in Horticulture Research 11(3):1-7, describes establishing CLas cultures. This opens the door to a wide range of research experiments on effective CLas microbicides that were previously not possible.

Model system

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Liberibacter crescens has emerged as a valuable model system for studying CLas. Unlike CLas, L. crescens can be cultured axenically and does not require a plant or insect host, offering insights into the genus's early evolutionary stages. This system has been instrumental in functional genomic studies of CLas genes, allowing researchers to explore CLas physiology and pathogenicity mechanisms in a controlled environment. Moreover, the ability of L. crescens to form biofilms under modified culture conditions provides a unique platform for studying biofilm formation, a critical aspect of CLas's lifecycle in insect vectors.

Despite the advances with L. crescens and the theoretical potential of cell culture infection models and bacterial cocultures, the axenic culturing of CLas remains a significant challenge. The development of CLas transformation protocols, which has been successful with L. crescens but not yet with CLas, is considered a critical step forward. This approach, whether through direct transformation or leveraging L. crescens as a surrogate, holds promise for unlocking the complexities of CLas biology and ultimately devising effective strategies to combat citrus greening disease.

Control

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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] 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.[33] Other varieties can have a partial tolerance to the disease.[34]

Antibiotics

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

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.[37] 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.[37][38] 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.[37][38]

Peptides

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University of California scientists have discovered a peptide that prevented and treated citrus greening disease in greenhouse trials; as of 2021, it is being tested in field trials.[39][40] The university entered into an exclusive license with Invaio to develop an enhanced injectable version of the product.[41]

Antisense oligonucleotides

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Researchers from the Agricultural Research Service, USDA at the U.S. Horticultural Research Laboratory in Fort Pierce, FL along with University of Florida Collaborators have developed two types of antisense oilgos (FANA and Morpholino's), and demonstrated efficient delivery into citrus trees, potato and tomato plants.[42] The oligonucleotide FANA (2′-deoxy-2′-fluoro-arabinonucleotide) RNA-targeting technology into citrus trees and potato plants for management of bacterial pathogens and arthropod pests. The FANA ASO technology is a single nucleotide strand of 20–24 nt in length that incorporates 2′F- chemically modifications of nucleotides, along with a phosphorothioate backbone and modified flanking nucleotides, in their structure called “gapmers,” produced by AUM LifeTech., Inc. These unique modified structures of FANA “triggers” enables gymnotic activity that self-delivers into cells, moving systemically in treated plants and insects, with significant suppression of their RNA targets. Reported is the FANA suppression of two plant-infecting bacterium Candidatus Liberibacter asiaticus, CLas (in citrus trees), and C. Liberibacter solanacearum, CLso (in potato and tomato) [43] [44]]

Morpholino's: These researchers demonstrated that PPMOs moved systemically in plants, fruit trees, and grapevines, such that they could 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.[45][46] Morpholino's must be covalently linked with a charged molecule or peptide, such as a cell-penetrating peptide, CPP, to enter bacteria (both Gram-positive or Gram-negative). After the MOs are conjugated to a carrier, they are referred to as PPMO, CPPMO, PMO, or similar. For more protocols, references at GeneTools, LLC, website (http://www.gene-ools.com/morpholino_antisense_oligos). Short PPMOs of 14–18nt are used to target bacteria, using a sequence, referred to as the external guide sequence, EGS, that when complexed with the target RNA modifies the shape to resemble a tRNA precursor which renders the target RNA susceptible to cleavage by ribonuclease P (RNase-P).[47]

Cover crops

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Some success has been reported using a cover crop strategy.[48] The citrus trees were not free of the disease bacteria, yet a healthy soil environment allowed them to produce fruit and remain profitable.[49] [50]

See also

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References

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  1. ^ a b c Bové, J. M. (March 2006). "Huanglongbing: a destructive, newly-emerging, century-old disease of citrus". Journal of Plant Pathology. 88 (1): 7–37. JSTOR 41998278.
  2. ^ "FE983/FE983: Impact of Citrus Greening on Citrus Operations in Florida". Institute of Food and Agricultural Sciences (IFAS). University of Florida.
  3. ^ "Researchers Find Possible Answer to Citrus Greening". Modern Farmer. 14 February 2021.
  4. ^ "Citrus greening". Animal and Plant Health Inspection Service. U.S. Department of Agricultur. Retrieved 21 September 2023.
  5. ^ "The Disease: Huanglongbing (HLB)". Citrus Research Board. 2011. 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. (July 2021). "Phytoene desaturase-silenced citrus as a trap crop with multiple cues to attract Diaphorina citri, the vector of Huanglongbing". Plant Science. 308: 110930. Bibcode:2021PlnSc.30810930K. doi:10.1016/j.plantsci.2021.110930. PMID 34034878. S2CID 235203508.
  7. ^ "Observation on yellow shoot on citrus. Etiological studies of yellow shoot on Citrus". Acta Phytopathological Sinica. 2: 1–42. 1956.
  8. ^ "Can Genetic Engineering Save the Florida Orange?". National Geographic. 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: 760481. doi:10.3389/fpls.2021.760481. PMC 8636133. PMID 34868155.
  10. ^ "Citrus greening disease". Plant Protection. Food & Fertilizer Technology Center: 2001–2. 2001.
  11. ^ "Plant Pathology". UF/IFAS Citrus Extension. University of Florida's Institute of Food and Agricultural Sciences (UF/IFAS). Archived from the original on 14 April 2021. Retrieved 17 June 2017.
  12. ^ Gutierrez, Andrew Paul; Ponti, Luigi (December 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" (PDF). Florida Entomologist. 96 (4): 1375–1391. doi:10.1653/024.096.0417.
  13. ^ "Trioza erytreae (African citrus psyllid)". CABI Digital Library. Centre for Agriculture and Bioscience International (CABI). Retrieved 17 June 2017.
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  15. ^ a b Wu, Fengnian; Qureshi, Jawwad A.; Huang, Jiaquan; Fox, Eduardo Gonçalves Paterson; Deng, Xiaoling; Wan, Fanghao; Liang, Guangwen; Cen, Yijing (September 2018). "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. 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". Pest Management Science. 74 (12): 2738–2746. doi:10.1002/ps.5060. PMID 29726075. S2CID 19098533.
  17. ^ Garnier, M.; Jagoueix-Eveillard, S.; Cronje, P. R.; Le Roux, H. F.; Bové, J. M. (November 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 (Pt 6): 2119–2125. doi:10.1099/00207713-50-6-2119. PMID 11155987.
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  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. ^ "Huanglongbing in Texas: Report on the first detections in commercial citrus". Journal of Citrus Pathology. 2 (1): 1–6. 2015.
  26. ^ "Threat to California Citrus May Finish Backyard Trees". The New York Times. April 17, 2012. Retrieved April 18, 2012.
  27. ^ "Trioza erytreae" (PDF). EPPO Data Sheets on Quarantine Pests. (EPPO/ CABI) European and Mediterranean Plant Protection Organization/Centre for Agricultural Bioscience International. 1979. 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 (April 2018). "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 Santaana R (26 March 2012). "Spinach genes may stop deadly citrus disease". The New York Times. Archived from the original on 16 April 2012. Retrieved 1 October 2012. {{cite news}}: More than one of |work= and |newspaper= specified (help)
  33. ^ "After A Sour Decade, Florida Citrus May Be Near A Comeback". NPR. 4 December 2016. Retrieved 10 February 2017.
  34. ^ "Promising new citrus varieties for greening tolerance". ScienceDaily. Retrieved 5 December 2019.
  35. ^ "Periwinkle Plants Provide Ammunition in the War on Citrus Greening". USDA Agricultural Research Service. 2010-04-26. Retrieved 2014-05-18.
  36. ^ "$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.
  37. ^ a b c "Citrus Farmers Facing Deadly Bacteria Turn to Antibiotics, Alarming Health Officials". The New York Times. May 17, 2019. Retrieved June 5, 2019.
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  40. ^ Wang, Nian (February 2021). "A promising plant defense peptide against citrus Huanglongbing disease". Proceedings of the National Academy of Sciences of the United States of America. 118 (6): e2026483118. Bibcode:2021PNAS..11826483W. doi:10.1073/pnas.2026483118. PMC 8017718. PMID 33526706.
  41. ^ "UC Riverside discovers first effective treatment for citrus-destroying disease". University of California Riverside. July 7, 2020.
  42. ^ "FANA and Morpholino's, Novel Molecules for Gene-Targeting in Plants and Arthropods". Proceedings of the XXV International Plant & Animal Genome Conference. 25 (Paper25794). January 14-18, San Diego,CA. 2017.
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  44. ^ Sandoval-Mojica, Andrés F.; Hunter, Wayne B.; Aishwarya, Veenu; Bonilla, Sylvia; Pelz-Stelinski, Kirsten S. (February 2021). "Antibacterial FANA oligonucleotides as a novel approach for managing the Huanglongbing pathosystem". Scientific Reports. 11 (1): 2760. Bibcode:2021NatSR..11.2760S. doi:10.1038/s41598-021-82425-8. PMC 7854585. PMID 33531619.
  45. ^ Hunter, Wayne B.; Sinisterra-Hunter, Xiomara H. (2018). "Emerging RNA Suppression Technologies to Protect Citrus Trees From Citrus Greening Disease Bacteria". Advances in Insect Physiology. 55. Elsevier: 163–197. doi:10.1016/bs.aiip.2018.08.001. ISBN 978-0-12-815079-5.
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  50. ^ "Citrus Industry Magazine". Citrus Industry Magazine. 2019-11-18. Retrieved 2024-08-17.

Further reading

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