We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Skip to main content
Log in

Huanglongbing Control: Perhaps the End of the Beginning

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Huanglongbing (HLB) is one of the most destructive citrus plant diseases worldwide. It is associated with the fastidious phloem-limited α-proteobacteria ‘Candidatus Liberibacter asiaticus’, ‘Ca. Liberibacter africanus’ and ‘Ca. Liberibacter americanus’. In recent years, HLB-associated Liberibacters have extended to North and South America. The causal agents of HLB have been putatively identified, and their transmission pathways and worldwide population structure have been extensively studied. However, very little is known about the epidemiologic relationships of Ca. L. asiaticus, which has limited the scope of HLB research and especially the development of control strategies. HLB-affected plants produce damaged fruits and die within several years. To control the disease, scientists have developed new compounds and screened existing compounds for their antibiotic and antimicrobial activities against the disease. These compounds, however, have very little or even no effect on the disease. The aim of the present review was to compile and compare different methods of HLB disease control with newly developed integrative strategies. In light of recent studies, we also describe how to control the vectors of this disease and the biological control of other citrus plant pathogens. This work could steer the attention of scientists towards integrative control strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Bové JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol:7–37

  2. Gottwald TR (2010) Current epidemiological understanding of citrus Huanglongbing. Annu Rev Phytopathol 48:119–139. https://doi.org/10.1146/annurev-phyto-073009-114418

    Article  PubMed  CAS  Google Scholar 

  3. Reinking OA (1919) Diseases of economic plants in Southern China. Philipp Agric 8:109–135

    Google Scholar 

  4. Husain MA, Nath D (1927) The Citrus Psylla:(Diaphorina Citri, Kuw.) Psyllidae: Homoptera. Government of India Central Pubilication Branch

  5. Chen Q (1943) A report of a study on yellow shoot of citrus in Chaoshan. New Agric Q Bull 3:75

    Google Scholar 

  6. Coletta-Filho H, Targon M, Takita M, De Negri J, Pompeu Jr J, Machado M, Do Amaral A, Muller G (2004) First report of the causal agent of Huanglongbing (“Candidatus Liberibacter asiaticus”) in Brazil. Plant Dis 88:1382–1382

    Article  Google Scholar 

  7. Halbert S (2005) The discovery of huanglongbing in Florida. Proceedings of the 2nd international citrus canker and huanglongbing research workshop. Florida Citrus Mutual, p 50

  8. Alvarez S, Solis D, Thomas M (2015) Can Florida’s citrus industry be saved while preserving the environment? An economic analysis for the bio-control of the Asian Citrus Psyllid. 2015 Annual meeting, January 31–February 3, 2015, Atlanta, Georgia. Southern Agricultural Economics Association

  9. Yang C, Powell CA, Duan Y, Shatters R, Fang J, Zhang M (2016) Deciphering the bacterial microbiome in huanglongbing-affected citrus treated with thermotherapy and sulfonamide antibiotics. PLoS One 11:e0155472

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Hodges A, Spreen T (2012) Economic impacts of citrus greening (HLB) in Florida, 2006/07–2010/11. Electronic data information source (EDIS) FE903: 32611

  11. Bove JM, Ayres AJ (2007) Etiology of three recent diseases of citrus in Sao Paulo State: sudden death, variegated chlorosis and huanglongbing. IUBMB Life 59:346–354

    Article  PubMed  CAS  Google Scholar 

  12. Jagoueix S, Bove J-M, Garnier M (1994) The phloem-limited bacterium of greening disease of citrus is a member of the α subdivision of the Proteobacteria. Int J Syst Evol Microbiol 44:379–386

    CAS  Google Scholar 

  13. Halbert SE, Manjunath KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Fla Entomol 87:330–353

    Article  Google Scholar 

  14. Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski KS, Alborn HT, Stelinski LL (2012) Induced release of a plant-defense volatile ‘deceptively’ attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathog 8:e1002610

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Stelinski LL, Ali JG, Alborn HT, Mann R, Pelz-Stelinski K (2013) Methyl salicylate-based attractants for vectors of citrus greening disease. Google Patents

  16. Tsai JH, Liu YH (2000) Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. J Econ Entomol 93:1721–1725

    Article  PubMed  CAS  Google Scholar 

  17. Farmanullah HB, Gul R (2005) Evaluation of six different groups of insecticides for the control of citrus psylla Diaphorina citri (Hemiptera: Psyllidae). Evaluation 27:18

    Google Scholar 

  18. Etxeberria E, Gonzalez P, Achor D, Albrigo G (2009) Anatomical distribution of abnormally high levels of starch in HLB-affected Valencia orange trees. Physiol Mol Plant Pathol 74:76–83

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  20. Da Graça J, Korsten L (2004) Citrus huanglongbing: review, present status and future strategies. Diseases of fruits and vegetables, vol I. Springer, pp 229–245

  21. Xia X-J, Wang Y-J, Zhou Y-H, Tao Y, Mao W-H, Shi K, Asami T, Chen Z, J-Q Y (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Jo Y-K, Kim BH, Jung G (2009) Antifungal activity of silver ions and nanoparticles on phytopathogenic fungi. Plant Dis 93:1037–1043

    Article  CAS  Google Scholar 

  23. Aritua V, Achor D, Gmitter FG, Albrigo G, Wang N (2013) Transcriptional and microscopic analyses of citrus stem and root responses to Candidatus Liberibacter asiaticus infection. PLoS One 8:e73742

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Koh E-J, Zhou L, Williams DS, Park J, Ding N, Duan Y-P, Kang B-H (2012) Callose deposition in the phloem plasmodesmata and inhibition of phloem transport in citrus leaves infected with “Candidatus Liberibacter asiaticus”. Protoplasma 249:687–697

    Article  PubMed  Google Scholar 

  25. Fan J, Chen C, Brlansky R, Gmitter Jr F, Li ZG (2010) Changes in carbohydrate metabolism in Citrus sinensis infected with ‘Candidatus Liberibacter asiaticus’. Plant Pathol 59:1037–1043

    Article  CAS  Google Scholar 

  26. Ammar ED, Shatters RG, Hall DG (2011) Localization of Candidatus Liberibacter asiaticus, associated with citrus huanglongbing disease, in its psyllid vector using fluorescence in situ hybridization. J Phytopathol 159:726–734

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. McManus PS, Stockwell VO, Sundin GW, Jones AL (2002) Antibiotic use in plant agriculture. Annu Rev Phytopathol 40:443–465

    Article  PubMed  CAS  Google Scholar 

  29. McManus P, Jones A (1994) Epidemiology and genetic analysis of streptomycin-resistant Erwinia amylovora from Michigan and evaluation of oxytetracycline for control. Phytopathology 84:627–632

    Article  Google Scholar 

  30. McManus PS, Stockwell VO (2001) Antibiotic use for plant disease management in the United States. Peach 2:2,900

    Google Scholar 

  31. Zhang M, Duan Y, Zhou L, Turechek WW, Stover E, Powell CA (2010) Screening molecules for control of citrus huanglongbing using an optimized regeneration system for'Candidatus Liberibacter asiaticus'-infected periwinkle (Catharanthus roseus) cuttings. Phytopathology 100:239–245

    Article  PubMed  CAS  Google Scholar 

  32. Zhang M, Powell CA, Zhou L, He Z, Stover E, Duan Y (2011) Chemical compounds effective against the citrus Huanglongbing bacterium ‘Candidatus Liberibacter asiaticus’ in planta. Phytopathology 101:1097–1103

    Article  PubMed  CAS  Google Scholar 

  33. Zhang M, Powell CA, Guo Y, Doud MS, Duan Y (2012) A graft-based chemotherapy method for screening effective molecules and rescuing huanglongbing-affected citrus plants. Phytopathology 102:567–574

    Article  PubMed  Google Scholar 

  34. Zhang M, Guo Y, Powell CA, Doud MS, Yang C, Duan Y (2014) Effective antibiotics against ‘Candidatus Liberibacter asiaticus’ in HLB-affected citrus plants identified via the graft-based evaluation. PLoS One 9:e111032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Le Roux H, Van Vuuren S, Pretorius M, Buitendag C (2006) Management of huanglongbing in South Africa. Proc Huanglongbing-Greening Intl Workshop 2006. Ribeirão, pp. 43–47

  36. Su H, Chang S (1974) Electron microscopical study on the heat and tetracycline response, and ultra-structure of the pathogen complex causing citrus likubin disease. Proc 8th Int Congr Electron Microscopy 2:628–629

  37. Chiu R-J, Tsai M-Y, Huang C-H, 邱人璋, 蔡謀祐, 黃秋雄 (1979) Distribution and retention of tetracyclines in healthy and likubin-affected citrus trees following trunk transfusion. Plant Prot Bull 143–152

  38. Supriyanto A, Whittle A (1991) Citrus rehabilitation in Indonesia. Proc 11th Conference of the International Organization of Citrus Virologists Riverside, CA, pp 409–413

  39. Abdullah T, Shokrollah H, Sijam K, Abdullah S (2009) Control of Huanglongbing (HLB) disease with reference to its occurrence in Malaysia. Afr J Biotechnol 8

  40. Cheema S, Kapur S, Sharma O (1986) Chemo-therapeutic controls of greening disease of citrus through bud dip treatment. Indian J Virol 2:104–107

    Google Scholar 

  41. Buitendag C, Von Broembsen L (1993) Living with citrus greening in South Africa. Proc 12th Conference of the International Organization of Citrus Virologists University of California, riverside, pp 269–273

  42. Zhang M, Powell CA, Guo Y, Benyon L, Duan Y (2013) Characterization of the microbial community structure in Candidatus Liberibacter asiaticus-infected citrus plants treated with antibiotics in the field. BMC Microbiol 13:1

    Article  CAS  Google Scholar 

  43. Schwarz R, Van Vuuren S (1971) Decrease in fruit greening of sweet orange by trunk injection of tetracyclines. Plant Disease Reporter

  44. Michelini L, La Rocca N, Rascio N, Ghisi R (2013) Structural and functional alterations induced by two sulfonamide antibiotics on barley plants. Plant Physiol Biochem 67:55–62

    Article  PubMed  CAS  Google Scholar 

  45. Sagaram M, Burns JK (2009) Leaf chlorophyll fluorescence parameters and huanglongbing. J Am Soc Hortic Sci 134:194–201

    Google Scholar 

  46. Tyler HL, Roesch LF, Gowda S, Dawson WO, Triplett EW (2009) Confirmation of the sequence of ‘Candidatus Liberibacter asiaticus’ and assessment of microbial diversity in Huanglongbing-infected citrus phloem using a metagenomic approach. Mol Plant-Microbe Interact 22:1624–1634

    Article  PubMed  CAS  Google Scholar 

  47. Trivedi P, Duan Y, Wang N (2010) Huanglongbing, a systemic disease, restructures the bacterial community associated with citrus roots. Appl Environ Microbiol 76:3427–3436

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Trivedi P, He Z, Van Nostrand JD, Albrigo G, Zhou J, Wang N (2012) Huanglongbing alters the structure and functional diversity of microbial communities associated with citrus rhizosphere. ISME J 6:363–383

    Article  PubMed  CAS  Google Scholar 

  49. Zhang M, Powell CA, Benyon LS, Zhou H, Duan Y (2013) Deciphering the bacterial microbiome of citrus plants in response to ‘Candidatus Liberibacter asiaticus’-infection and antibiotic treatments. PLoS One 8:e76331

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Gatineau F, Bonnot F, Yen TTH, Tuyen ND, Truc NTN (2010) Effects of imidacloprid and fenobucarb on the dynamics of the psyllid Diaphorina citri Kuwayama and on the incidence of Candidatus Liberibacter asiaticus. Fruits 65:209–220

    Article  CAS  Google Scholar 

  51. Hammesfahr U, Heuer H, Manzke B, Smalla K, Thiele-Bruhn S (2008) Impact of the antibiotic sulfadiazine and pig manure on the microbial community structure in agricultural soils. Soil Biol Biochem 40:1583–1591

    Article  CAS  Google Scholar 

  52. Thiele-Bruhn S, Beck I-C (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465

    Article  PubMed  CAS  Google Scholar 

  53. Kunkel L (1936) Heat treatments for the cure of yellows and other virus diseases of peach. Phytopathology 26:809–830

    Google Scholar 

  54. Grant T (1957) Heat treatments for obtaining sources of virus-free citrus budwood. Fla State Hortic Soc 70:51–53

    Google Scholar 

  55. Grant T, Jones J, Norman G (1960) Present status of heat treatment of citrus viruses. Proc Florida State Hortic Soc 72:45–48

    Google Scholar 

  56. Nyland G, Goheen A (1969) Heat therapy of virus diseases of perennial plants. Annu Rev Phytopathol 7:331–354

    Article  Google Scholar 

  57. Hoffman MT, Doud MS, Williams L, Zhang M-Q, Ding F, Stover E, Hall D, Zhang S, Jones L, Gooch M (2013) Heat treatment eliminates ‘Candidatus Liberibacter asiaticus’ from infected citrus trees under controlled conditions. Phytopathology 103:15–22

    Article  PubMed  Google Scholar 

  58. Lopes S, Frare G, Bertolini E, Cambra M, Fernandes N, Ayres A, Marin D, Bové J (2009) Liberibacters associated with citrus huanglongbing in Brazil:‘Candidatus Liberibacter asiaticus’ is heat tolerant,‘Ca. L. americanus’ is heat sensitive. Plant Dis 93:257–262

    Article  Google Scholar 

  59. Lo X (1983) Studies on the sterilization effect of the intermittent hot water treatment on citrus budwood and nursling infected with citrus yellow shoot. JS China Agric Univ 1:97–102

    Google Scholar 

  60. Lo X, Lo D, Tang W (1981) Studies on the thermotherapy of citrus yellow shoot disease. Chih wu pao hu hsueh pao= Acta phytophylacica sinica

  61. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Panswad T, Doungchai A, Anotai J (2003) Temperature effect on microbial community of enhanced biological phosphorus removal system. Water Res 37:409–415

    Article  PubMed  CAS  Google Scholar 

  63. Ahlgren IF, Ahlgren CE (1965) Effects of prescribed burning on soil microorganisms in a Minnesota jack pine forest. Ecology 46:304–310

    Article  Google Scholar 

  64. Grasso G, Ripabelli G, Sammarco M, Mazzoleni S (1996) Effects of heating on the microbial populations of a grassland soil. Int J Wildland Fire 6:67–70

    Article  Google Scholar 

  65. Zeng Y, Feng F, Medová H, Dean J, Koblížek M (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci 111:7795–7800

    Article  PubMed  CAS  Google Scholar 

  66. Guo F, Zhang T (2014) Detecting the nonviable and heat-tolerant bacteria in activated sludge by minimizing DNA from dead cells. Microb Ecol 67:829–836. https://doi.org/10.1007/s00248-014-0389-2

    Article  PubMed  CAS  Google Scholar 

  67. Castenholz RW (1981) Isolation and cultivation of thermophilic cyanobacteria. The prokaryotes. Springer, pp 236–246

  68. Lyu C, Chen C, Ge F, Liu D, Zhao S, Chen D (2013) A preliminary metagenomic study of puer tea during pile fermentation. J Sci Food Agric 93:3165–3174

    Article  PubMed  CAS  Google Scholar 

  69. Yokota T (1997) The structure, biosynthesis and function of brassinosteroids. Trends Plant Sci 2:137–143

    Article  Google Scholar 

  70. Bishop GJ, Yokota T (2001) Plants steroid hormones, brassinosteroids: current highlights of molecular aspects on their synthesis/metabolism, transport, perception and response. Plant Cell Physiol 42:114–120

    Article  PubMed  CAS  Google Scholar 

  71. Khripach V, Zhabinskii V, de Groot A (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century. Ann Bot 86:441–447

    Article  CAS  Google Scholar 

  72. Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 33:887–898

    Article  PubMed  CAS  Google Scholar 

  73. Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297

    Article  PubMed  CAS  Google Scholar 

  74. Ding J, Shi K, Zhou Y-H, J-Q Y (2009) Effects of root and foliar applications of 24-epibrassinolide on fusarium wilt and antioxidant metabolism in cucumber roots. Hortscience 44:1340–1345

    Google Scholar 

  75. Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:1

    Article  CAS  Google Scholar 

  76. Xia XJ, Zhou YH, Ding J, Shi K, Asami T, Chen Z, JQ Y (2011) Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. New Phytol 191:706–720

    Article  PubMed  CAS  Google Scholar 

  77. Ali SS, Kumar GS, Khan M, Doohan FM (2013) Brassinosteroid enhances resistance to fusarium diseases of barley. Phytopathology 103:1260–1267

    Article  PubMed  CAS  Google Scholar 

  78. Canales E, Coll Y, Hernández I, Portieles R, García MR, López Y, Aranguren M, Alonso E, Delgado R, Luis M (2016) ‘Candidatus Liberibacter asiaticus’, causal agent of citrus huanglongbing, is reduced by treatment with brassinosteroids. PLoS One 11:e0146223

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Nürnberger T, Kemmerling B (2006) Receptor protein kinases–pattern recognition receptors in plant immunity. Trends Plant Sci 11:519–522

    Article  PubMed  CAS  Google Scholar 

  80. Belkhadir Y, Jaillais Y, Epple P, Balsemão-Pires E, Dangl JL, Chory J (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci 109:297–302

    Article  PubMed  Google Scholar 

  81. Wang Z-Y (2012) Brassinosteroids modulate plant immunity at multiple levels. Proc Natl Acad Sci 109:7–8

    Article  PubMed  Google Scholar 

  82. Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S, Chinchilla D, Rathjen JP, de Vries SC, Zipfel C (2012) Brassinosteroids inhibit pathogen-associated molecular pattern–triggered immune signaling independent of the receptor kinase BAK1. Proc Natl Acad Sci 109:303–308

    Article  PubMed  Google Scholar 

  83. Folimonova SY, Robertson CJ, Garnsey SM, Gowda S, Dawson WO (2009) Examination of the responses of different genotypes of citrus to huanglongbing (citrus greening) under different conditions. Phytopathology 99:1346–1354

    Article  PubMed  Google Scholar 

  84. Dutt M, Barthe G, Irey M, Grosser J (2015) Transgenic citrus expressing an Arabidopsis NPR1 gene exhibit enhanced resistance against Huanglongbing (HLB; Citrus Greening). PLoS One 10:e0137134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Westbrook CJ, Hall DG, Stover E, Duan YP, Lee RF (2011) Colonization of citrus and citrus-related germplasm by Diaphorina citri (Hemiptera: Psyllidae). Hortscience 46:997–1005

    Google Scholar 

  86. Furr J, Cooper W, Reece P (1947) An investigation of flower formation in adult and juvenile citrus trees. Am J Bot:1–8

  87. Gmitter Jr F, Grosser J, Castle W, Moore G (2007) A comprehensive citrus genetic improvement program. Citrus genetics, breeding and biotechnology. CAB International, Oxfordshire, pp 9–18

    Google Scholar 

  88. Zhang X, Francis MI, Dawson WO, Graham JH, Orbović V, Triplett EW, Mou Z (2010) Over-expression of the Arabidopsis NPR1 gene in citrus increases resistance to citrus canker. Eur J Plant Pathol 128:91–100

    Article  CAS  Google Scholar 

  89. Kuć J (1982) Induced immunity to plant disease. Bioscience 32:854–860

    Article  Google Scholar 

  90. Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annu Rev Phytopathol 35:235–270

    Article  PubMed  CAS  Google Scholar 

  91. Pieterse CM, van Pelt JA, Verhagen BW, Ton J, van Wees A, Léon-Kloosterziel KM, Van Loon L (2003) Induced systemic resistance by plant growth-promoting rhizobacteria. Symbiosis 35:39–54

    CAS  Google Scholar 

  92. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Pieterse CM, van Loon LC (1999) Salicylic acid-independent plant defence pathways. Trends Plant Sci 4:52–58

    Article  PubMed  CAS  Google Scholar 

  94. Smith-Becker J, Marois E, Huguet EJ, Midland SL, Sims JJ, Keen NT (1998) Accumulation of salicylic acid and 4-hydroxybenzoic acid in phloem fluids of cucumber during systemic acquired resistance is preceded by a transient increase in phenylalanine ammonia-lyase activity in petioles and stems. Plant Physiol 116:231–238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  95. Conrath U (2006) Systemic acquired resistance. Plant Signal Behav 1:179–184

    Article  PubMed  PubMed Central  Google Scholar 

  96. Albrecht U, Bowman KD (2008) Gene expression in Citrus sinensis (L.) Osbeck following infection with the bacterial pathogen Candidatus Liberibacter asiaticus causing Huanglongbing in Florida. Plant Sci 175:291–306

    Article  CAS  Google Scholar 

  97. Albrecht U, Bowman KD (2012) Transcriptional response of susceptible and tolerant citrus to infection with Candidatus Liberibacter asiaticus. Plant Sci 185:118–130

    Article  PubMed  CAS  Google Scholar 

  98. Nwugo CC, Duan Y, Lin H (2013) Study on citrus response to Huanglongbing highlights a down-regulation of defense-related proteins in lemon plants upon ‘Ca. Liberibacter asiaticus’ infection. PLoS One 8:e67442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Martinelli F, Reagan RL, Uratsu SL, Phu ML, Albrecht U, Zhao W, Davis CE, Bowman KD, Dandekar AM (2013) Gene regulatory networks elucidating Huanglongbing disease mechanisms. PLoS One 8:e74256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Mafra V, Martins PK, Francisco CS, Ribeiro-Alves M, Freitas-Astúa J, Machado MA (2013) Candidatus Liberibacter americanus induces significant reprogramming of the transcriptome of the susceptible citrus genotype. BMC Genomics 14:1

    Article  CAS  Google Scholar 

  101. Bouchemal K, Briançon S, Perrier E, Fessi H (2004) Nano-emulsion formulation using spontaneous emulsification: solvent, oil and surfactant optimisation. Int J Pharm 280:241–251

    Article  PubMed  CAS  Google Scholar 

  102. Lopes S, Frare G (2008) Graft transmission and cultivar reaction of citrus to ‘Candidatus Liberibacter americanus’. Plant Dis 92:21–24

    Article  Google Scholar 

  103. Nariani TK, Raychaudhuri SP, Viswanath SM (1973) Tolerance to greening disease in certain citrus species. Curr Sci 42:513–514

  104. Schonberr J, Schmidt W (1979) Water permeability of plant cuticles. Dependence of permeability coefficients of cuticular transpiration on vapour pressure saturation deficit. Planta 144:391–300

    Article  Google Scholar 

  105. Hull HM (1970) Leaf structure as related to absorption of pesticides and other compounds. Residue Reviews/Rückstands-Berichte. Springer, pp 1–150

  106. Kolattukudy P (1985) Enzymatic penetration of the plant cuticle by fungal pathogens. Annu Rev Phytopathol 23:223–250

    Article  CAS  Google Scholar 

  107. Baker EA, Procopiou J, Hunt GM (1975) The cuticles of citrus species. Composition of leaf and fruit waxes. J Sci Food Agric 26:1093–1101

    Article  CAS  Google Scholar 

  108. Skoss JD (1955) Structure and composition of plant cuticle in relation to environmental factors and permeability. Bot Gaz:55–72

  109. Stock D, Holloway PJ (1993) Possible mechanisms for surfactant-induced foliar uptake of agrochemicals. Pestic Sci 38:165–177

    Article  CAS  Google Scholar 

  110. Castro MJ, Ojeda C, Cirelli AF (2014) Advances in surfactants for agrochemicals. Environ Chem Lett 12:85–95

    Article  CAS  Google Scholar 

  111. Bondada B, Syvertsen J, Albrigo L (2001) Urea nitrogen uptake by citrus leaves. Hortscience 36:1061–1065

    CAS  Google Scholar 

  112. Orbović V, Achor D, Syvertsen JP (2007) Adjuvants affect penetration of copper through isolated cuticles of citrus leaves and fruit. Hortscience 42:1405–1408

    Google Scholar 

  113. Ocsoy I, Paret ML, Ocsoy MA, Kunwar S, Chen T, You M, Tan W (2013) Nanotechnology in plant disease management: DNA-directed silver nanoparticles on graphene oxide as an antibacterial against Xanthomonas perforans. ACS Nano 7:8972–8980

    Article  PubMed  CAS  Google Scholar 

  114. Yang C, Powell CA, Duan Y, Shatters R, Zhang M (2015) Antimicrobial nanoemulsion formulation with improved penetration of foliar spray through citrus leaf cuticles to control citrus huanglongbing. PLoS One 10:e0133826

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Yang C, Powell C, Duan Y, Zhang M (2016) Characterization and antibacterial activity of oil-in-water Nano-emulsion formulation against Candidatus Liberibacter asiaticus. Plant Dis 100:2448–2454

    Article  CAS  Google Scholar 

  116. Hijaz F, Nehela Y, Killiny N (2016) Possible role of plant volatiles in tolerance against huanglongbing in citrus. Plant Signal Behav 11:e1138193

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Maffei M (2010) Sites of synthesis, biochemistry and functional role of plant volatiles. S Afr J Bot 76:612–631

    Article  CAS  Google Scholar 

  118. Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923. https://doi.org/10.1093/pcp/pcp030

    Article  PubMed  CAS  Google Scholar 

  119. Gao Y, YJ JIN, HD LI, HJ CHEN (2005) Volatile organic compounds and their roles in bacteriostasis in five conifer species. J Integr Plant Biol 47:499–507

    Article  CAS  Google Scholar 

  120. Richardson ML, Hall DG (2013) Resistance of poncirus and citrus × Poncirus germplasm to the Asian citrus psyllid. Crop Sci 53:183–188

    Article  Google Scholar 

  121. Scora RW, Ahmed M (1994) The leaf oils of Severinia buxifolia (Poir.) Tenore. J Essent Oil Res 6:363–367

    Article  CAS  Google Scholar 

  122. Yamasaki Y, Kunoh H, Yamamoto H, Akimitsu K (2007) Biological roles of monoterpene volatiles derived from rough lemon (Citrus jambhiri Lush) in citrus defense. J Gen Plant Pathol 73:168–179

    Article  CAS  Google Scholar 

  123. Rodríguez A, San Andrés V, Cervera M, Redondo A, Alquézar B, Shimada T, Gadea J, Rodrigo MJ, Zacarías L, Palou L (2011) Terpene down-regulation in orange reveals the role of fruit aromas in mediating interactions with insect herbivores and pathogens. Plant Physiol 156:793–802

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  124. Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci 103:16672–16676

    Article  PubMed  CAS  Google Scholar 

  125. Hijaz F, El-Shesheny I, Killiny N (2013) Herbivory by the insect diaphorina citri induces greater change in citrus plant volatile profile than does infection by the bacterium, Candidatus Liberibacter asiaticus. Plant Signal Behav 8:e25677

    Article  PubMed Central  CAS  Google Scholar 

  126. Sagaram US, DeAngelis KM, Trivedi P, Andersen GL, S-E L, Wang N (2009) Bacterial diversity analysis of Huanglongbing pathogen-infected citrus, using PhyloChip arrays and 16S rRNA gene clone library sequencing. Appl Environ Microbiol 75:1566–1574

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  127. Albiach-Marti MR, Grosser JW, Gowda S, Mawassi M, Satyanarayana T, Garnsey SM, Dawson WO (2004) Citrus tristeza virus replicates and forms infectious virions in protoplasts of resistant citrus relatives. Mol Breed 14:117–128

    Article  CAS  Google Scholar 

  128. Rahman A, Al-Reza SM, Yoon JI, Kang SC (2009) In vitro inhibition of foodborne pathogens by volatile oil and organic extracts of Poncirus trifoliata Rafin. seeds. J Sci Food Agric 89:876–881

    Article  CAS  Google Scholar 

  129. Albrecht U, Bowman KD (2011) Tolerance of the trifoliate citrus hybrid US-897 (Citrus reticulata Blanco× Poncirus trifoliata L. Raf.) to Huanglongbing. Hortscience 46:16–22

    CAS  Google Scholar 

  130. Kim D-H, Bae E-A, Han MJ (1999) Anti-Helicobacter pylori activity of the metabolites of poncirin from Poncirus trifoliata by human intestinal bacteria. Biol Pharm Bull 22:422–424

    Article  PubMed  CAS  Google Scholar 

  131. Dorman H, Deans S (2000) Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol 88:308–316

    Article  PubMed  CAS  Google Scholar 

  132. Griffin SG, Wyllie SG, Markham JL, Leach DN (1999) The role of structure and molecular properties of terpenoids in determining their antimicrobial activity. Flavour Fragr J 14:322–332

    Article  CAS  Google Scholar 

  133. Park S-N, Lim YK, Freire MO, Cho E, Jin D, Kook J-K (2012) Antimicrobial effect of linalool and α-terpineol against periodontopathic and cariogenic bacteria. Anaerobe 18:369–372

    Article  PubMed  CAS  Google Scholar 

  134. Oztürk M, Duru ME, Aydoğmuş-Oztürk F, Harmandar M, Mahlicli M, Kolak U, Ulubelen A (2009) GC-MS analysis and antimicrobial activity of essential oil of Stachys cretica subsp. smyrnaea. Nat Prod Commun 4:109–114

    PubMed  Google Scholar 

  135. Şahin F, Güllüce M, Daferera D, Sökmen A, Sökmen M, Polissiou M, Agar G, Özer H (2004) Biological activities of the essential oils and methanol extract of Origanum vulgare ssp. vulgare in the Eastern Anatolia region of Turkey. Food Control 15:549–557

    Article  CAS  Google Scholar 

  136. Inoue H, Ohnishi J, Ito T, Tomimura K, Miyata S, Iwanami T, Ashihara W (2009) Enhanced proliferation and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition feeding in the nymphal stage. Ann Appl Biol 155:29–36

    Article  Google Scholar 

  137. Pelz-Stelinski K, Brlansky R, Ebert T, Rogers M (2010) Transmission parameters for Candidatus Liberibacter asiaticus by Asian citrus psyllid (Hemiptera: Psyllidae). J Econ Entomol 103:1531–1541

    Article  PubMed  CAS  Google Scholar 

  138. Ghanim M, Fattah-Hosseini S, Levy A, Cilia M (2016) Morphological abnormalities and cell death in the Asian citrus psyllid (Diaphorina citri) midgut associated with Candidatus Liberibacter asiaticus. Sci Rep 6

  139. Leong SCT, Abang F, Beattie A, Kueh RJH, Wong SK (2012) Impacts of horticultural mineral oils and two insecticide practices on population fluctuation of Diaphorina citri and spread of huanglongbing in a citrus orchard in Sarawak. Sci World J 2012

  140. Khan I, Zahid M, Khan GZ (2012) Toxicity of botanic and synthetic pesticide residues to citrus psyllid Diaphorina citri Kuwayama and Chrysoperla carnea (Stephens). Pak J Zool 44:197–201

    Google Scholar 

  141. Belasque Jr J, Bassanezi R, Yamamoto P, Ayres A, Tachibana A, Violante A, Tank Jr A, Di Giorgi F, Tersi F, Menezes G (2010) Lessons from huanglongbing management in São Paulo state, Brazil. J Plant Pathol:285–302

  142. Roistacher C (1996) The economics of living with citrus diseases: huanglongbing (greening) in Thailand. Proc 13th Conference of the International Organization of Citrus Virologists (IOCV) University of California, Riverside, pp 279–285

  143. Yasuda K, Ooishi T, Kawamura F (2006) Effect of insecticides on adults and larvae of Asian citrus psyllid, Diaphorina citri (Homoptera: Psyllidae). Kyushu Plant Protection Research (Japan)

  144. Qureshi JA, Stansly PA (2007) Integrated approaches for managing the Asian citrus psyllid Diaphorina citri (Homoptera: Psyllidae) in Florida. Proc Florida State Hortic Soc 120:110–115

    Google Scholar 

  145. Bergamin-Filho A, Gasparoto M, Amorim L, Bassanezi R (2008) Number of insecticide sprays has no effect on the incidence of citrus huanglongbing in a commercial orchard in Sao Paulo, Brazil. Phytopathology, vol. 98. AMER PHYTOPATHOLOGICAL SOC 3340 PILOT KNOB ROAD, ST PAUL, MN 55121 USA, pp. S21-S21

  146. Srinivasan R, Hoy MA, Singh R, Rogers ME (2008) Laboratory and field evaluations of Silwet L-77 and kinetic alone and in combination with imidacloprid and abamectin for the management of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 91:87–100

    Article  CAS  Google Scholar 

  147. Rogers M, Stansly P, Stelinski L (2012) Florida Citrus pest management guide: Asian citrus psyllid and citrus leafminer. Entomol Nematol Dept, Fla Coop Ext Serv, Inst FoodAgri Sci, Univer Fla. http://edis.ifas.ufl.edu/in686/ENY734

  148. Hoffmann C, Fritz B, Martin D, Atwood R, Hurner T, Ledebuhr M, Tandy M, Jackson JL, Wisler G (2010) Evaluation of low-volume sprayers used in Asian citrus psyllid control applications. HortTechnology 20:632–638

    Google Scholar 

  149. Abd-Elgawad M, El-Mougy N, El-Gamal N, Abdel-Kader M, Mohamed M (2010) Protective treatments against soilborne pathogens in citrus orchards. J Plant Prot Res 50:477–484

    Article  Google Scholar 

  150. Ichinose K, Bang DV, Tuan DH, Dien LQ (2010) Effective use of neonicotinoids for protection of citrus seedlings from invasion by Diaphorina citri (Hemiptera: Psyllidae). J Econ Entomol 103:127–135

    Article  PubMed  CAS  Google Scholar 

  151. Pena J, Duncan R, Klema E, Hunsberger A (1999) Evaluation of direct and indirect action of insecticides and acaricides for control of lime and avocado pests. Proc Fla State Hortic Soc 112:213–217

    Google Scholar 

  152. Ahmed S, Ahmad N, Khan RR (2004) Studies on population dynamics and chemical control of citrus psylla, Diaphorina citri. Int J Agric Biol 6:970–973

    Google Scholar 

  153. Childers CC, Rogers ME (2005) Chemical control and management approaches of the Asian citrus psyllid, Diaphorina citri Kuwayama (Homoptera: Psyllidae) in Florida citrus. Proc Fla State Hortic Soc 110:49–53

    Google Scholar 

  154. Shivankar V, Rao C, Singh S (2000) Studies on citrus psylla, Diaphorina citri Kuwayama: a review. Agricultural Reviews (Karnal, India) 21

  155. Stansly PA, Qureshi JA, Kostyk BC (2012) Foliar applications of sulfoxaflor, byi02960, and some commonly used insecticides for control of Asian citrus psyllid and citrus leafminer in oranges: summer, 2011. Arthrop Manag Tests:37

  156. Stansly PA, Rogers ME (2006) Managing Asian citrus psyllid populations. Citrus Ind 87:17–19

    Google Scholar 

  157. Qureshi J, Kostyk B, Stansly PA (2012) Registered and experimental insecticides for control of Asian citrus psyllid and citrus leafminer on mature orange trees. Proc Fla State Hortic Soc 125:92–97

    Google Scholar 

  158. Tiwari S, Stelinski LL (2013) Effects of cyantraniliprole, a novel anthranilic diamide insecticide, against Asian citrus psyllid under laboratory and field conditions. Pest Manag Sci 69:1066–1072

    Article  PubMed  CAS  Google Scholar 

  159. Ichinose K, Miyazi K, Matsuhira K, Yasuda K, Sadoyama Y, Tuan DH, Van Bang D (2010) Unreliable pesticide control of the vector psyllid Diaphorina citri (Hemiptera: Psyllidae) for the reduction of microorganism disease transmission. J Environ Sci Health B 45:466–472

    Article  PubMed  CAS  Google Scholar 

  160. Hayashikawa S, Suenaga H, Torigoe H (2006) Insecticidal activity of some insecticides on Asian citrus psyllid, Diaphorina citri Kuwayama. Kyushu Plant Protection Research (Japan)

  161. Qureshi JA, Stansly PA (2010) Dormant season foliar sprays of broad-spectrum insecticides: an effective component of integrated management for Diaphorina citri (Hemiptera: Psyllidae) in citrus orchards. Crop Prot 29:860–866

    Article  CAS  Google Scholar 

  162. Chiyaka C, Singer BH, Halbert SE, Morris JG, van Bruggen AH (2012) Modeling huanglongbing transmission within a citrus tree. Proc Natl Acad Sci 109:12213–12218

    Article  PubMed  Google Scholar 

  163. Powell CA, Burton MS, Pelpsi M, Bullock R (2007) Effects of insecticide on Asian citrus psyllid (Hemiptera: Psyllidae) populations in a Florida citrus grove. Plant Health Progress http://www.plantmanagementnetwork.org/php/. Accessed 24 May 2010

  164. Atwood R, Stelinski L (2008) Is there a future for low-volume application for psyllid control. Citrus Ind 89:16–18

    Google Scholar 

  165. Anonymous (2009a) Low volume sprays improve psyllid management-the story of 24(c) label, particle size distribution, area wide applications and a pesticide application tool

  166. Anonymous (2009b) Psyllid management in Florida-position statement

  167. Stelinski LL RM, Yates Y, Dewdney M and Spann T, (2009) Low volume applications: an emerging technology in the citrus industry. 2009. Accessed 15-02-2017

  168. Qureshi JA, Stansly PA (2008) Rate, placement and timing of aldicarb applications to control Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), in oranges. Pest Manag Sci 64:1159–1169

    Article  PubMed  CAS  Google Scholar 

  169. Sétamou M, Rodriguez D, Saldana R, Schwarzlose G, Palrang D, Nelson S (2010) Efficacy and uptake of soil-applied imidacloprid in the control of Asian citrus psyllid and a citrus leafminer, two foliar-feeding citrus pests. J Econ Entomol 103:1711–1719

    Article  PubMed  Google Scholar 

  170. Gutiérrez IR, Watanabe N, Harter T, Glaser B, Radke M (2010) Effect of sulfonamide antibiotics on microbial diversity and activity in a Californian Mollic Haploxeralf. J Soils Sediments 10:537–544

    Article  CAS  Google Scholar 

  171. Yasuda K, Yoshitake H, Ooishi T, Toudou A, Uechi N (2007) Effect of high-density scatter of the infiltration shift insecticide on invasion by adult and egg-laying individuals of the Asian citrus psyllid, Diaphorina citri (Homoptera: Psyllidae). Kyushu Plant Protection Research (Japan)

  172. Ichinose K, Tuan DH, Van Bang D, Miyaji K, Yasuda K, Matsuhira K, Van Hoa N, Sadoyama Y (2011) Differential efficacy of insecticides according to crop growth: the citrus psyllid on citrus plants. INTECH Open Access Publisher

  173. Staal G (1975) Insect growth regulators with juvenile hormone activity. Annu Rev Entomol 20:417–460

    Article  PubMed  CAS  Google Scholar 

  174. Mondal K, Parween S (2000) Insect growth regulators and their potential in the management of stored-product insect pests. Integr Pest Manag Rev 5:255–295

    Article  Google Scholar 

  175. Boina DR, Rogers ME, Wang N, Stelinski LL (2010) Effect of pyriproxyfen, a juvenile hormone mimic, on egg hatch, nymph development, adult emergence and reproduction of the Asian citrus psyllid, Diaphorina citri Kuwayama. Pest Manag Sci 66:349–357

    Article  PubMed  CAS  Google Scholar 

  176. Tiwari S, Clayson PJ, Kuhns EH, Stelinski LL (2012) Effects of buprofezin and diflubenzuron on various developmental stages of Asian citrus psyllid, Diaphorina citri. Pest Manag Sci 68:1405–1412

    Article  PubMed  CAS  Google Scholar 

  177. Hall DG, Nguyen R (2010) Toxicity of pesticides to Tamarixia radiata, a parasitoid of the Asian citrus psyllid. BioControl 55:601–611

    Article  CAS  Google Scholar 

  178. Cocco A, Hoy MA (2008) Toxicity of organosilicone adjuvants and selected pesticides to the Asian citrus psyllid (Hemiptera: Psyllidae) and its parasitoid Tamarixia radiata (Hymenoptera: Eulophidae). Fla Entomol 91:610–620

    CAS  Google Scholar 

  179. Michaud J, McKenzie C (2004) Safety of a novel insecticide, sucrose octanoate, to beneficial insects in Florida citrus. Fla Entomol 87:6–9

    Article  CAS  Google Scholar 

  180. Nemec S, Datnoff L, Strandberg J (1996) Efficacy of biocontrol agents in planting mixes to colonize plant roots and control root diseases of vegetables and citrus. Crop Prot 15:735–742

    Article  Google Scholar 

  181. Yang C-H, Menge JA, Cooksey DA (1994) Mutations affecting hyphal colonization and pyoverdine production in pseudomonads antagonistic toward Phytophthora parasitica. Appl Environ Microbiol 60:473–481

    PubMed  PubMed Central  CAS  Google Scholar 

  182. Kean S, Soytong K, To-anun C (2010) Application of biological fungicides to control citrus root rot under field condition in Cambodia. J Agric Technol 6:219–230

    Google Scholar 

  183. d HeidiLdfor (2017) Engineered virus in line to battle citrus disease. Nature 545:277–278

    Article  CAS  Google Scholar 

Download references

Funding

This review paper is part of our project ‘Microbial agents to control huanglongbing’. This research was supported by the Ministry of Agriculture of China, for special fund for the Agro-Scientific Research in the public interest (Grant no: 201003029), The Natural Science Foundation of Yunnan Province (Grant no: 2008CC024), The National Natural Science Foundation of China (Grant no: 31560503), and The R&D Foundation of Yunnan Province (Grant no: 2009 EB060).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yueqiu He.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Munir, S., He, P., Wu, Y. et al. Huanglongbing Control: Perhaps the End of the Beginning. Microb Ecol 76, 192–204 (2018). https://doi.org/10.1007/s00248-017-1123-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1123-7

Keywords

Navigation