Candidatus Liberibacter Species and Associated Plant Diseases

Abstract

Currently, seven species of Liberibacter have been described. Most Liberibacters have not been cultured in artificial medium except Liberibacter crescens. Liberibacters are causal agents of multiple devastating plant diseases including citrus Huanglongbing and potato zebra chip. Importantly, pathogens, and psyllid vectors, are expanding worldwide, leading to spread of corresponding diseases and potential new diseases with host jump of psyllids, threatening the production of many important crops. It is critical to understand the interactions among the pathogens, psyllid vectors, and the hosts, as well as epidemiology of the diseases to design efficient, environment friendly and sustainable disease management strategies.

Key Concepts

  • Candidatus Liberibacters are gram‐negative, uncultured, plant‐associated bacteria.
  • Liberibacters cause serious diseases on many plants, including devastating diseases such as citrus Huanglongbing and potato zebra chip.
  • Liberibacter pathogens are transmitted by psyllids in nature, and the pathogens and psyllid vectors are expanding worldwide.
  • Diseases caused by Liberibacters can be confirmatively diagnosed by quantitative polymerase chain reaction (qPCR) with pathogen‐specific primers.
  • Molecular mechanisms of pathogenesis of Liberibacter remain largely unknown due to the difficulty in culturing these bacteria.
  • The diseases may be controlled via reducing the inoculum sources and limiting the spread of psyllid vectors.

Keywords: Liberibacter; psyllid; phloem; Huanglongbing; HLB; greening; zebra chip

Figure 1. Valencia sweet orange trees showing the symptoms characteristic of Huanglongbing (HLB) disease including yellow shoot; blotchy mottling leaves; upright, harden and small leaves; twig dieback; premature and smaller fruit; and preharvest fruit drop. (a) A young HLB‐diseased tree, (b) a mature HLB‐diseased tree, (c) typical HLB leaf symptoms showing blotchy mottle symptom, small and upright leaf, corky vein and secondary zinc deficiency, (d) branches showing dieback and leaf fall off, (e) top showing branch dieback, leaf fall off. Pictures a–e are by Nian Wang and Jinyun Li. (f) Asian citrus psyllid (D. citri) feeding on citrus plants. Photograph taken by Dr. Yuanchun Wang, Citrus Research and Education Center, University of Florida.
Figure 2. Zebra chip disease symptoms. (a) A potato field showing zebra chip‐diseased potato plants. (b) Beginning symptoms of ZC showing leaf curling and smaller leaves in the terminal. (c) ZC symptoms at a later stage. (d) An adult potato psyllid Bactericera cockerelli feeding on potato leaf. (e) A nymph of potato psyllid feeding on potato leaf. (f) Zebra chip‐diseased potato tuber with internal necrosis (right two) and healthy tuber (left). (g) Fried potato chips from healthy (upper) and zebra chip‐diseased plant tubers (bottom). Courtesy of Kay Ledbetter and Charlie Rush.
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References

Aguilar E, Sengoda VG, Bextine B, McCue KF and Munyaneza JE (2013) First report of “Candidatus Liberibacter solanacearum” on tobacco in Honduras. Plant Disease 97 (10): 1376–1377.

Alfaro‐Fernández A, Hernández‐Llopis D and Font MI (2017) Haplotypes of ‘Candidatus Liberibacter solanacearum’ identified in Umbeliferous crops in Spain. European Journal of Plant Pathology 149: 127–131. DOI: 10.1007/s10658-017-1172-2.

Alvarez S, Rohrig E, Solís D and Thomas MH (2016) Citrus greening disease (Huanglongbing) in Florida: economic impact, management and the potential for biological control. Agricultural Research 5: 109–118.

Bertolini E, Teresani GR, Loiseau M, et al. (2015) Transmission of ‘Candidatus Liberibacter solanacearum’ in carrot seeds. Plant Pathology 64 (2): 276–285.

Borges KM, Cooper WR, Garczynski SF, et al. (2017) “Candidatus Liberibacter solanacearum” associated with the psyllid, Bactericera maculipennis (Hemiptera: Triozidae). Environmental Entomology 46 (2): 210–216. DOI: 10.1093/ee/nvw174.

Camerota C, Raddadi N, Pizzinat A, et al. (2012) Incidence of ‘Candidatus Liberibacter europaeus’ and phytoplasmas in Cacopsylla species (Hemiptera: Psyllidae) and their host/shelter plants. Phytoparasitica 40: 213–221.

Canale MC, Tomaseto AF, de Lara Haddad M, Coletta‐Filho HD and Lopes JRS (2017) Latency and persistence of ‘Candidatus Liberibacter asiaticus’ in its psyllid vector, Diaphorina citri (Hemiptera: Liviidae). Phytopathology 107 (3): 264–272.

Cen Y, Zhang L, Xia Y, et al. (2012) Detection of ‘Candidatus Liberibacter asiaticus’ in Cacopsylla (Psylla) citrisuga (Hemiptera: Psyllidae). Florida Entomologist 95: 304–311.

Chiyaka C, Singer BH, Halbert SE, Morris JG Jr and van Bruggen AHC (2012) Modeling huanglongbing transmission within a citrus tree. Proceedings of the National Academy of Sciences of the United States of America 109 (30): 12213–12218; published ahead of print July 10, 2012. DOI: 10.1073/pnas.1208326109.

Cocuzza G, Massimino E, Urbaneja A, et al. (2017) A review on Trioza erytreae (African citrus psyllid), now in mainland Europe, and its potential risk as vector of huanglongbing (HLB) in citrus. Journal of Pest Science 90 (1): 1–17.

Duan Y, Zhou L, Hall DG, et al. (2009) Complete genome sequence of citrus huanglongbing bacterium, ‘Candidatus Liberibacter asiaticus’ obtained through metagenomics. Molecular Plant‐Microbe Interactions 22: 1011–1020.

EPPO (2016) EPPO Global Database. Paris: EPPO. https://gd.eppo.int/.

Fagen JR, Leonard MT, Coyle JF, et al. (2014) Liberibacter crescens gen. nov., sp. nov., the first cultured member of the genus Liberibacter. Int. J. Syst. Evol. Microbiol. 64: 2461–2466. DOI: 10.1099/ijs.0.063255-0

Garnier M, Jagoueix‐Eveillard S, Cronje P, Le Roux H and Bové JM (2000) Genomic characterization of a liberibacter present in an ornamental Rutaceous tree, Calodendrum capense, in the Western Cape Province of South Africa. Proposal for a “Candidatus Liberibacter africanus subsp. capensis”. International Journal of Systematic and Evolutionary Microbiology 50: 2119–2125.

Ghanim M, Fattah‐Hosseini S, Levy A and Cilia M (2016) Morphological abnormalities and cell death in the Asian citrus psyllid (Diaphorina citri) midgut associated with Candidatus Liberibacter asiaticus. Scientific Reports 6: 33418. DOI: 10.1038/srep33418.

Haapalainen M, Kivimäki P, Latvala S, et al. (2016) Frequency and occurrence of the carrot pathogen ‘Candidatus Liberibacter solanacearum’ haplotype C in Finland. Plant Pathology 66 (4): 559–570. DOI: 10.1111/ppa.12613.

Hall DG, Albrecht U and Bowman KD (2016) Transmission rates of 'Ca. Liberibacter asiaticus by Asian citrus psyllid are enhanced by the presence and developmental stage of citrus flush. Journal of Economic Entomology 109 (2): 558–563.

Hu J and Wang N (2016) Evaluation of the spatiotemporal dynamics of oxytetracycline and its control effect against citrus Huanglongbing via trunk injection. Phytopathology 106: 1495–1503.

Jain M, Fleites LA and Gabriel DW (2015) Prophage‐encoded peroxidase in ‘Candidatus Liberibacter asiaticus’ is a secreted effector that suppresses plant defenses. Molecular Plant‐Microbe Interactions 28: 1330–1337.

Lee JA, Halbert SE, Dawson WO, et al. (2015) Asymptomatic spread of huanglongbing and implications for disease control. Proceedings of the National Academy of Sciences of the United States of America 112: 7605–7610.

Leonard MT, Fagen JR, Davis‐Richardson AG, Davis MJ and Triplett EW (2012) Complete genome sequence of Liberibacter crescens BT‐1. Standards in Genomic Sciences 7: 271–283.

Li W, Hartung JS and Levy L (2006) Quantitative real‐time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. Journal of Microbiological Methods 66: 104–115.

Li J, Trivedi P and Wang N (2016) Field evaluation of plant defense inducers for the control of citrus Huanglongbing. Phytopathology 106: 37–46.

Liefting LW, Sutherland PW, Ward LI, et al. (2009) A new ‘Candidatus Liberibacter’ species associated with diseases of solanaceous crops. Plant Disease 93: 208–214.

Lin H and Gudmestad NC (2013) Aspects of pathogen genomics, diversity, epidemiology, vector dynamics, and disease management for a newly emerged disease of potato: zebra chip. Phytopathology 103: 524–537.

Lin H, Pietersen G, Han C, et al. (2015) Complete genome sequence of “Candidatus Liberibacter africanus,” a bacterium associated with citrus Huanglongbing. Genome Announcements 3: e00733‐15. DOI: 10.1128/genomeA.00733-15.

Loiseau M, Garnier S, Boirin V, et al. (2014) First report of ‘Candidatus Liberibacter solanacearum’ in carrots in France. Plant Disease 98: 839.

Lopes SA, Frare GF, Bertolini E, et al. (2009) Liberibacters associated with citrus huanglongbing in Brazil: ‘Candidatus Liberibacter asiaticus’ is heat tolerant, ‘Ca. L. americanus’ is heat sensitive. Plant Disease 93: 257–262.

Morris J, Shiller J, Mann R, et al. (2017) Novel 'Candidatus Liberibacter' species identified in the Australian eggplant psyllid, Acizzia solanicola. Microbiol Biotechnology 10 (4): 833–844. DOI: 10.1111/1751-7915.12707.

Munyaneza JE, Sengoda VG, Buchman JL and Fisher TW (2012) Effects of temperature on ‘Candidatus Liberibacter solanacearum’ and zebra chip potato disease symptom development. Plant Disease 96: 18–23.

Munyaneza JE, Swisher KD, Hommes M, et al. (2015) First report of ‘Candidatus Liberibacter solanacearum’ associated with psyllid‐infested carrots in Germany. Plant Disease 99: 1269.

Munyaneza JE, Mustafa T, Fisher TW, Sengoda VG and Horton DR (2016) Assessing the likelihood of transmission of Candidatus Liberibacter solanacearum to carrot by potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae). PLoS One 11 (8): e0161016. DOI: 10.1371/journal.pone.0161016.

Nelson WR, Eveillard S, Dubrana MP and Bové JM (2015) Cryptic haplotypes of “Candidatus Liberibacter africanus”. Journal of Plant Pathology 97 (2): 291–295.

Pagliai FA, Gardner CL, Bojilova L, et al. (2014) The transcriptional activator LdtR from ‘Candidatus Liberibacter asiaticus’ mediates osmotic stress tolerance. PLoS Pathogens 10 (4): e1004101. DOI: 10.1371/journal.ppat.1004101.

Pelz‐Stelinski KS, Brlansky RH and Rogers ME (2010) Transmission of Candidatus Liberibacter asiaticus by the Asian citrus psyllid, Diaphorina citri. Journal of Economic Entomology 103: 1531–1541.

Pelz‐Stelinski KS and Killiny N (2016) Better together: association with ‘Candidatus Liberibacter Asiaticus’ increases the reproductive fitness of its insect vector, Diaphorina citri (Hemiptera: Liviidae). Annals of the Entomological Society of America 109 (3): 371–376.

Raddadi N, Gonella E, Camerota C, et al. (2011) ‘Candidatus Liberibacter europaeus’ sp. nov. that is associated with and transmitted by the psyllid Cacopsylla pyri apparently behaves as an endophyte rather than a pathogen. Environmental Microbiology 13: 414–426.

Ramadugu C, Manjunath L, Keremane L, et al. (2016) Long‐term field evaluation reveals Huanglongbing resistance in citrus relatives. Plant Disease 100 (9): 1858–1869.

Ravindran A, Levy J, Pierson E and Gross DC (2012) Development of a loop‐mediated isothermal amplification procedure as a sensitive and rapid method for detection of 'Candidatus Liberibacter solanacearum' in potatoes and Psyllids. Phytopathology 102: 899–907.

Roberts R and Pietersen G (2017) A novel subspecies of ‘Candidatus Liberibacter africanus’ found on native Teclea gerrardii (Family: Rutaceae) from South Africa. Antonie van Leeuwenhoek 110 (3): 437–444. DOI: 10.1007/s10482-016-0799-x.

Sengoda VG, Munyaneza JE, Crosslin JM, Buchman JL, and Pappu HR (2010) Phenotypic and etiological differences between psyllid yellows and zebra chip diseases of potato. Am J Potato Res 87: 41–49.

Sengoda VG, Cooper WR, Swisher KD, Henne DC and Munyaneza JE (2014) Latent period and transmission of “Candidatus Liberibacter solanacearum” by the potato psyllid Bactericera cockerelli (Hemiptera: Triozidae). Plos One 9: e93475.

Shimwela MM, Narouei‐Khandan HA, Halbert SE, et al. (2016) First occurrence of Diaphorina citri in East Africa, characterization of the Ca. Liberibacter species causing huanglongbing (HLB) in Tanzania, and potential further spread of D. citri and HLB in Africa and Europe. European Journal of Plant Pathology 146 (2): 349–368.

Tahzima RS, Massart EH, Achbani J, Munyaneza E and Ouvrard D (2017) First report of ‘Candidatus Liberibacter solanacearum’ associated with the psyllid Bactericera trigonica Hodkinson on carrots in northern Africa. Plant Disease 101 (1): 242. 10.1094/PDIS-07-16-0964-PDN.

Teresani GR, Bertolini E, Alfaro‐Fernandez A, et al. (2014) Association of ‘Candidatus Liberibacter solanacearum’ with a vegetative disorder of celery in Spain and development of a real‐time PCR method for its detection. Phytopathology 104: 804–811.

Teresani G, Hernández E, Bertolini E, et al. (2015) Search for potential vectors of ‘Candidatus Liberibacter solanacearum’: population dynamics in host crops. Spanish Journal of Agricultural Research 13: e10–e002.

Thompson S, Fletcher JD, Ziebell H, et al. (2013) First report of ‘Candidatus Liberibacter europaeus’ associated with psyllid infested Scotch broom. New Disease Reports 27: 6. DOI: 10.5197/j.2044-0588.2013.027.006.

Ukuda‐Hosokawa R, Sadoyama Y, Kishaba M, et al. (2015) Infection density dynamics of the citrus greening bacterium “Candidatus Liberibacter asiaticus” in field populations of the psyllid Diaphorina citri and its relevance to the efficiency of pathogen transmission to citrus plants. Applied and Environmental Microbiology 81: 3728–3736.

Wang N and Trivedi P (2013) Citrus huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology 103: 652–665.

Wang N, Pierson EA, Setubal JC, et al. (2017) The Candidatus Liberibacter‐host interface: insights into pathogenesis mechanisms and disease control. Annual Review of Phytopathology 55: 451–482.

West Jonathan S (2014) Plant Pathogen Dispersal. In: eLS. Chichester: John Wiley & Sons Ltd. http://www.els.net [DOI: 10.1002/9780470015902.a0021272].

Wulff NA, Zhang S, Setubal JC, et al. (2014) The complete genome sequence of ‘Candidatus Liberibacter americanus’, associated with citrus huanglongbing. Molecular Plant‐Microbe Interactions 27: 163–176.

Zambon FT, Plant K and Etxeberria E (2017) Leaf‐disc grafting for the transmission of Candidatus Liberibacter asiaticus in citrus (Citrus sinensis; Rutaceae) seedlings. Applications in Plant Sciences 5 (1): 1600085. DOI: 10.3732/apps.1600085.

Zou X, Jiang X, Xu L, et al. (2017) Transgenic citrus expressing synthesized cecropin B genes in the phloem exhibits decreased susceptibility to Huanglongbing. Plant Molecular Biology 93 (4): 341–353.

Further Reading

Bové JM (2006) Huanglongbing: a destructive, newly‐emerging, century‐old disease of citrus. Journal of Plant Pathology 88: 7–37.

Gottwald TR, da Graça JV and Bassanezi RB (2007) Citrus Huanglongbing: the pathogen and its impact. Plant Health Progress (online). DOI: 10.1094/PHP-2007-0906-01-RV.

Gottwald TR (2010) Current epidemiological understanding of citrus huanglongbing. Annual Review of Phytopathology 48: 119–139.

Haapalainen M (2014) Biology and epidemics of Candidatus Liberibacter species, psyllid‐transmitted plant‐pathogenic bacteria. Annals of Applied Biology 165: 172–198.

Li J, Pang Z, Trivedi P, et al. (2017) ‘Candidatus Liberibacter asiaticus’ encodes a functional salicylic acid (SA) hydroxylase that degrades SA to suppress plant defenses. Molecular Plant‐Microbe Interactions 30 (8): 620–630.

Lin H and Civerolo EL (2014) Comparative genomics of the Liberibacteral plant pathogens. In: Gross DC, Lichens‐Park A and Kole C (eds) Genomics of Plant‐Associated Bacteria, pp. 203–233. Berlin: Springer‐Verlag.

Nelson WR, Munyaneza JE, McCue KF and Bové JM (2013) The Pangaean origin of “Candidatus Liberibacter” species. Journal of Plant Pathology 95: 455–461.

Rigano LA, Malamud F, Orce IG, et al. (2014) Rapid and sensitive detection of Candidatus Liberibacter asiaticus by loop mediated isothermal amplification combined with a lateral flow dipstick. BMC Microbiology 14: 86.

Wang N, Stelinski LL, Pelz‐Stelinski KS, Graham JH and Zhang Y (2017) Tale of the Huanglongbing disease pyramid in the context of the citrus microbiome. Phytopathology 107 (4): 380–387. PHYTO‐12‐16‐0426‐RVW.

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Li, Jinyun, and Wang, Nian(Oct 2017) Candidatus Liberibacter Species and Associated Plant Diseases. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0027201]