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Friend or foe? Relationship between ‘Candidatus Liberibacter asiaticus’ and Diaphorina citri

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Abstract

Interactions between insects and plant pathogens have been more enthusiastically studied in the recent decade, especially those relationships which takes the insects as vectors. The spectrum of these interactions ranges from mutualistic to pathogenic. The length of the co-evolutionary process will determine whether a microorganism shares a friend or a foe relationship with its host, and a friendship connection is frequently observed if the coexistence is longer. This review updates knowledge about the morphological, physiological and genetic mechanisms that drive the interaction between ‘Candidatus Liberibacter asiaticus’ (Las) and its vector, the Asian citrus psyllid, Diaphorina citri. Las is the predominant causal agent of citrus huanglongbing (HLB) disease, the major constrain to citrus production worldwide. This bacterium is transmitted by D. citri, in a propagative-circulative manner during its feeding from plant host. Understanding of the interactions among vector, plant pathogen and host plant are important for the management of this vector-borne disease complex.

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References

  • Adams AS, Currie CR, Cardoza Y et al (2009) Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Canadian Journal of Forest Research 39:1133–1147

    CAS  Google Scholar 

  • 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 Science 175:291–306

    CAS  Google Scholar 

  • Alves AGR, Diniz AJF, Parra JRP (2014) Biology of the huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants. Journal of Economic Entomology 107:691–696

    CAS  PubMed  Google Scholar 

  • Alves GR, Vieira JM, Diniz AJF, Parra JRP (2016) Can the choice behavior and fitness of Tamarixia radiata (Hymenoptera: Eulophidae) be affected by the citrus (Sapindales: Rutaceae) variety used to rear the Asian citrus psyllid (Hemiptera: Liviidae)? Florida Entomologist 99:281–285

  • Alves GR, Beloti VH, Faggioni-Floriano KM et al (2018) Does the scion or rootstock of Citrus sp. affect the feeding and biology of Diaphorina citri Kuwayama (Hemiptera: Liviidae)? Arthropod Plant Interact 12:77–84

    Google Scholar 

  • Ammar E-D, Shatters RG, Hall DG (2011) Localization of Candidatus Liberibacter asiaticus, Associated with Citrus Huanglongbing Disease, in its Psyllid Vector using Fluorescence in situ Hybridization. Journal of Phytopathology 159:726–734

    CAS  Google Scholar 

  • Ammar ED, Ramos JE, Hall DG et al (2016) Acquisition, replication and inoculation of Candidatus Liberibacter asiaticus following various acquisition periods on huanglongbing-infected citrus by nymphs and adults of the asian citrus psyllid. PLoS One 11:e0159594

    PubMed Central  Google Scholar 

  • Ammar E-D, Hall DG, Hosseinzadeh S, Heck M (2018) The quest for a non-vector psyllid: Natural variation in acquisition and transmission of the huanglongbing pathogen ‘Candidatus Liberibacter asiaticus’ by Asian citrus psyllid isofemale lines. PLoS One 13:e0195804

    PubMed  PubMed Central  Google Scholar 

  • Ammar E, Achor D, Levy A (2019) Immuno-Ultrastructural Localization and Putative Multiplication Sites of Huanglongbing Bacterium in Asian Citrus Psyllid Diaphorina citri. Insects 10:422

    PubMed Central  Google Scholar 

  • Andrade EC, Hunter WB (2017) RNAi feeding bioassay: development of a non-transgenic approach to control Asian citrus psyllid and other hemipterans. Entomologia Experimentalis et Applicata 162:389–396

    CAS  Google Scholar 

  • Arp AP, Hunter WB, Pelz-Stelinski KS (2016) Annotation of the Asian Citrus Psyllid Genome Reveals a Reduced Innate Immune System. Frontiers in Physiology 7:570

    PubMed  PubMed Central  Google Scholar 

  • Arp AP, Martini X, Pelz-Stelinski KS (2017) Innate immune system capabilities of the Asian citrus psyllid, Diaphorina citri. Journal of Invertebrate Pathology 148:94–101

    CAS  PubMed  Google Scholar 

  • Augustinos AA, Tsiamis G, Cáceres C et al (2019) Taxonomy, Diet, and Developmental Stage Contribute to the Structuring of Gut-Associated Bacterial Communities in Tephritid Pest Species. Frontiers in Microbiology 10:2004

    PubMed  PubMed Central  Google Scholar 

  • Ausique JJS, D’Alessandro CP, Conceschi MR et al (2017) Efficacy of entomopathogenic fungi against adult Diaphorina citri from laboratory to field applications. Journal of Pest Science (2004) 90:947–960

  • Baldwin IT (2010) Plant volatiles. Current Biology 20:392–397

    Google Scholar 

  • Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). Journal of Ecology 96:971–980

    CAS  Google Scholar 

  • Belliure B, Janssen A, Maris PC et al (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters 8:70–79

    Google Scholar 

  • Beloti VH, Alves GR, Feliciano D, Araújo D (2015) Lethal and Sublethal Effects of Insecticides Used on Citrus, on the Ectoparasitoid Tamarixia radiata. PLoS One 10:e0132128

    PubMed  PubMed Central  Google Scholar 

  • Beloti VH, Alves, GR, Coletta-Filho HD, Yamamoto PT (2018) The Asian citrus psyllid host Murraya koenigii is immune to citrus Huanglongbing pathogen ‘Candidatus Liberibacter asiaticus’. Phytopathology 108:1089–1094

  • Ben-Yosef M, Pasternak Z, Jurkevitch E, Yuval B (2014) Symbiotic bacteria enable olive flies (Bactrocera oleae) to exploit intractable sources of nitrogen. Journal of Evolutionary Biology 27:2695–2705

    CAS  PubMed  Google Scholar 

  • Blanc S, Michalakis Y (2016) Manipulation of hosts and vectors by plant viruses and impact of the environment. Current Opinion in Insect Science 16:36–43

    PubMed  Google Scholar 

  • Boava L, Cristofani-Yaly M, Machado M (2017) Physiologic, anatomic, and gene expression changes in Citrus sunki, Poncirus trifoliata and their hybrids after Liberibacter asiaticus infection. Phytopathology 107:590–599

    CAS  PubMed  Google Scholar 

  • Bonani JP, Fereres A, Garzo E et al (2009) Characterization of electrical penetration graphs of the Asian citrus psyllid, Diaphorina citri, in sweet orange seedlings. Entomologia Experimentalis et Applicata 134:35–49

    Google Scholar 

  • Bourtzis K, Miller TA (2008) Insect Symbiosis, 1st Edition. CRC Press Book. 368p

  • Bove JM, Genomique DR, Pathogene P et al (2006) Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal Plant Pathology 88:7–37

    Google Scholar 

  • Canale MC, Tomaseto AF, Haddad ML et al (2017) Latency and Persistence of ‘Candidatus Liberibacter asiaticus’ in Its Psyllid Vector, Diaphorina citri (Hemiptera: Liviidae). Phytopathology 107:264–272

    PubMed  Google Scholar 

  • Cardoza YJ, Klepzig KD, Raffa KF (2006) Bacteria in oral secretions of an endophytic. Ecological Entomology 31:636–645

    Google Scholar 

  • Celli J (2015) The changing nature of the Brucella-Containing Vacuole. Cellular Microbiology 17:951–958

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cen Y, Yang C, Holford P et al (2012) Feeding behaviour of the Asiatic citrus psyllid, Diaphorina citri, on healthy and huanglongbing-infected citrus. Entomologia Experimentalis et Applicata 143:13–22

    Google Scholar 

  • Chen X, Stansly PA (2014) Biology of Tamarixia radiata (Hymenoptera: Eulophidae), Parasitoid of the Citrus Greening Disease Vector Diaphorina citri (Hemiptera: Psylloidea): A Mini Review. Florida Entomologist 97:1404–1413

    Google Scholar 

  • Chu C-C, Gill TA, Hoffmann M, Pelz-Stelinski KS (2016) Inter-Population Variability of Endosymbiont Densities in the Asian Citrus Psyllid (Diaphorina citri Kuwayama). Microbial Ecology 71:999–1007

    PubMed  PubMed Central  Google Scholar 

  • Coletta-Filho HD, Tagon MLPN, Takita MA et al (2004) First report of the causal agent of huanglongbing (“Candidatus Liberibacter asiaticus”) in Brazil. Plant Disease 88:1382

    CAS  PubMed  Google Scholar 

  • Coyle JF, Lorca GL, Gonzalez CF (2018) Understanding the Physiology of Liberibacter asiaticus: An Overview of the Demonstrated Molecular Mechanisms. Journal of Molecular Microbiology and Biotechnology 28:116–127

    CAS  PubMed  Google Scholar 

  • Dan H, Ikeda N, Fujikami M, Nakabachi A (2017) Behavior of bacteriome symbionts during transovarial transmission and development of the Asian citrus psyllid. PLoS One 12:e0189779

    PubMed  PubMed Central  Google Scholar 

  • Davis TS, Horton DR, Munyaneza JE, Landolt PJ (2012) Experimental Infection of Plants with an Herbivore- Associated Bacterial Endosymbiont Influences Herbivore Host Selection Behavior. PLoS One 7:e49330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dheilly NM, Poulin R, Thomas F (2015) Biological warfare: Microorganisms as drivers of host-prasite interactions. Infection Genetics Evolution 34:251–259

    Google Scholar 

  • Dillon RJ, Dillon VM (2004) The Gut Bacteria of Insects: Nonpathogenic Interactions. Annual Review of Entomology 49:71–92

    CAS  PubMed  Google Scholar 

  • Diacovich L, Lorenzi L, Tomassetti M et al (2017) The infectious intracellular lifestyle of Salmonella enterica relies on the adaptation to nutritional conditions within the Salmonella-containing vacuole. Virulence 8:975–992

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Eigenbrode SD, Bosque-Pérez NA, Davis TS (2018) Insect-Borne Plant Pathogens and Their Vectors: Ecology, Evolution, and Complex Interactions. Annual Review of Entomology 63:169–191

    CAS  PubMed  Google Scholar 

  • El-Shesheny I, Hajeri S, El-hawary I et al (2013) Silencing Abnormal Wing Disc Gene of the Asian Citrus Psyllid, Diaphorina citri Disrupts Adult Wing Development and Increases Nymph Mortality. PLoS One 8:e65392

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engel P, Moran NA (2013) The gut microbiota of insects - diversity in structure and function. FEMS Microbiology Reviews 37:699–735

    CAS  PubMed  Google Scholar 

  • Fagen JR, Giongo A, Brown CT et al (2012) Characterization of the Relative Abundance of the Citrus Pathogen Ca. Liberibacter asiaticus in the Microbiome of Its Insect Vector, Diaphorina citri, using High Throughput 16S rRNA Sequencing. The Open Microbiology Journal 6:29–33

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher TW, Vyas M, He R et al (2014) Comparison of potato and asian citrus psyllid adult and nymph transcriptomes identified vector transcripts with potential involvement in circulative, propagative liberibacter transmission. Pathog (Basel Switzerland) 3:875–907

    CAS  Google Scholar 

  • Galdeano DM, Lopes S, Falk W, Machado MA (2017) Oral delivery of double-stranded RNAs induces mortality in nymphs and adults of the Asian citrus psyllid, Diaphorina citri. PLoS One 12:e0171847

    PubMed  PubMed Central  Google Scholar 

  • Garnier M, Bové J, Cronje CPR (2000) Presence of “Candidatus Liberibacter africanus” in the Western Cape Province of South Africa. Fourteenth IOCV Conference, Short Communications, 369–372

  • Gauthier J-P, Outreman Y, Mieuzet L, Simon J-C (2015) Bacterial Communities Associated with Host- Adapted Populations of Pea Aphids Revealed by Deep Sequencing of 16S Ribosomal DNA. PLoS One 10:e0120664

    PubMed  PubMed Central  Google Scholar 

  • George J, Ammar ED, Hall DG et al (2018) Prolonged phloem ingestion by Diaphorina citri nymphs compared to adults is correlated with increased acquisition of citrus greening pathogen. Scientific Reports 8:1–11

    Google Scholar 

  • 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. Scientific Reports 6:33418

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghanim M, Achor D, Ghosh S et al (2017) ‘Candidatus Liberibacter asiaticus’ Accumulates inside Endoplasmic Reticulum Associated Vacuoles in the Gut Cells of Diaphorina citri. Scientific Reports 7:16945

    PubMed  PubMed Central  Google Scholar 

  • Gharaei AM, Ziaaddini M, Jalali MA, Michaud JP (2014) Sex-specific responses of Asian citrus psyllid to volatiles of conspecific and host-plant origin. Journal of Applied Entomology 138:500–509

    Google Scholar 

  • Ghosh S, Jassar O, Kontsedalov S et al (2019) A Transcriptomics Approach Reveals Putative Interaction of Candidatus Liberibacter solanacearum with the Endoplasmic Reticulum of Its Psyllid Vector. Insects 10:279

    PubMed Central  Google Scholar 

  • Gill TA, Chu C, Pelz-Stelinski KS (2017) Comparative proteomic analysis of hemolymph from uninfected and Candidatus Liberibacter asiaticus-infected Diaphorina citri. Amino Acids 49:389–406

    CAS  PubMed  Google Scholar 

  • Goenaga S, Kenney JL, Duggal NK et al (2015) Potential for Co-Infection of a Mosquito-Specific Flavivirus, Nhumirim Virus, to Block West Nile Virus Transmission in Mosquitoes. Viruses 7:5801–5812

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gonella E, Tedeschi R, Crotti E, Alma A (2019) Multiple guests in a single host: interactions across symbiotic and phytopathogenic bacteria in phloem-feeding vectors – a review. Entomologia Experimentalis et Applicata 167:171–185

    Google Scholar 

  • Goulin EH, Galdeano DM, Granato LM et al (2019) RNA interference and CRISPR: Promising approaches to better understand and control citrus pathogens. Microbiological Research 226:1–9

    CAS  PubMed  Google Scholar 

  • Granato LM, Galdeano DM, D’Alessandre NDR et al (2019) Callose synthase family genes plays an important role in the Citrus defense response to Candidatus Liberibacter asiaticus. European Journal of Plant Pathology 155:25–38

    CAS  Google Scholar 

  • Gross J (2016) Chemical Communication between Phytopathogens, Their Host Plants and Vector Insects and Eavesdropping by Natural Enemies. Frontiers in Ecology Evolution 2:1–5

    Google Scholar 

  • Guédot C, Horton DR, Landolt PJ (2009) Attraction of male winterform pear psylla to female-produced volatiles and to female extracts and evidence of male–male repellency. Entomologia Experimentalis et Applicata 130:191–197

    Google Scholar 

  • Guidolin AS, Cônsoli FL (2013) Molecular Characterization of Wolbachia Strains Associated with the Invasive Asian Citrus Psyllid Diaphorina citri in Brazil. Microbial Ecology 65:475–486

    CAS  PubMed  Google Scholar 

  • Guo J, Ye G, Dong S, Liu S (2010) An Invasive Whitefly Feeding on a Virus-Infected Plant Increased Its Egg Production and Realized Fecundity. PLoS One 5:e11713

    PubMed  PubMed Central  Google Scholar 

  • Hajeri S, Killiny N, El-mohtar C et al (2014) Citrus tristeza virus-based RNAi in citrus plants induces gene silencing in Diaphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing). Journal of Biotechnology 176:42–49

    CAS  PubMed  Google Scholar 

  • Halbert ASE, Manjunath KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Florida Entomologist 87:330–353

    Google Scholar 

  • Hall DG, Richardson ML, Ammar E, Halbert SE (2012) Asian citrus psyllid, Diaphorina citri, vector of citrus huanglongbing disease. Entomologia Experimentalis et Applicata 146:207–223

    Google Scholar 

  • Hijaz F, Killiny N (2014) Collection and Chemical Composition of Phloem Sap from Citrus sinensis L. Osbeck (Sweet Orange). PLoS One 9:e101830

    PubMed  PubMed Central  Google Scholar 

  • Hoffmann M, Coy MR, Gibbard HNK (2014) Wolbachia Infection Density in Populations of the Asian Citrus Psyllid (Hemiptera: Liviidae). Environmental Entomology 43:1215–1222

    CAS  PubMed  Google Scholar 

  • Horton DR, Landolt PJ (2007) Attraction of male pear psylla, Cacopsylla pyricola, to female-infested pear shoots. Entomologia Experimentalis et Applicata 123:177–183

    Google Scholar 

  • Hosseinzadeh S, Ramsey J, Mann M et al (2019) Color morphology of Diaphorina citri influences interactions with its bacterial endosymbionts and ‘Candidatus Liberibacter asiaticus’. PLoS Genet 14:e0216599

    CAS  Google Scholar 

  • Huang H-J, Bao Y-Y, Lao S-H et al (2015) Rice ragged stunt virus-induced apoptosis affects virus transmission from its insect vector, the brown planthopper to the rice plant. Scientifc Reports 5:11413

    Google Scholar 

  • Hussain M, Akutse KS, Lin Y et al (2018) Susceptibilities of Candidatus Liberibacter asiaticus-infected and noninfected Diaphorina citri to entomopathogenic fungi and their detoxification enzyme activities under different temperatures. Microbiology Open 7:e00607

    PubMed  Google Scholar 

  • Ibarra-Cortés KH, Gonzáles-Hernández H, Guzmán-Franco AW et al (2018) Interactions between entomopathogenic fungi and Tamarixia radiata (Hymenoptera: Eulophidae) in Diaphorina citri (Hemiptera: Liviidae) populations under laboratory conditions. Journal of Pest Sciences (2004) 91:373–384

  • Inoue H, Ohnishi J, Ito T et al (2009) Enhanced proliferation and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition feeding in the nymphal stage. Annals of Applied Biology 155:29–36

    Google Scholar 

  • Isberg RR, Connor TO, Heidtman M (2009) The Legionella pneumophila replication vacuole: making a cozy niche inside host cells. Nature Reviews Microbiology 7:13–24

    CAS  PubMed  Google Scholar 

  • Jagoueix S, Bove JM, Garnier M (1997) Comparison of the 16S / 23S Ribosomal Intergenic Regions of “Candidatus Liberibacter asiaticum ” and “Candidatus Liberibacter africanum,” the Two Species Associated with Citrus Huanglongbing (Greening) Disease. International Journal of Systematic Evolutionary Bacteriology 47:224–227

    CAS  Google Scholar 

  • Jain M, Munoz-Bodnar A, Gabriel DW (2017) Concomitant Loss of the Glyoxalase System and Glycolysis Makes the Uncultured Pathogen “Candidatus Liberibacter asiaticus” an energy scavenger. Applied and Environmental Microbiology 83:e01670–e01617

    PubMed  PubMed Central  Google Scholar 

  • Killackey SA, Sorbara MT, Girardin SE, Torres AG (2016) Cellular Aspects of Shigella Pathogenesis: Focus on the Manipulation of Host Cell Processes. Frontiers in Cellular Infection Microbiology 6:38

    PubMed  Google Scholar 

  • Killiny N, Kishk A (2017) Delivery of dsRNA through topical feeding for RNA interference in the citrus sap piercing-sucking hemipteran, Diaphorina citri. Archives of Insect Biochemistry and Physiology 95:1–13

    Google Scholar 

  • Killiny N, Hijaz F, Ebert TA, Rogers ME (2017) A Plant Bacterial Pathogen Manipulates Its Insect Vector’s Energy Metabolism. Applied and Environmental Microbiology 83:AEM.03005-A16

    Google Scholar 

  • Killiny N, Jones SE (2018) Metabolic alterations in the nymphal instars of Diaphorina citri induced by Candidatus Liberibacter asiaticus, the putative pathogen of huanglongbing. PLoS One 13:e0191871

    PubMed  PubMed Central  Google Scholar 

  • Kishk A, Anber HAI, AbdEl-Raof TK et al (2017) RNA interference of carboxyesterases causes nymph mortality in the Asian citrus psyllid, Diaphorina citri. Archives of Insect Biochemistry and Physiology 94:1–13

    Google Scholar 

  • Kruse A, Fattah-Hosseini S, Saha S et al (2017) Combining ’omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut. PLoS One 12:e0179531

    PubMed  PubMed Central  Google Scholar 

  • Kruse A, Ramsey JS, Johnson R et al (2018) Candidatus Liberibacter asiaticus Minimally Alters Expression of Immunity and Metabolism Proteins in Hemolymph of Diaphorina citri, the Insect Vector of Huanglongbing. Journal of Proteome Research 17:2995–3011

    CAS  PubMed  Google Scholar 

  • Liu Y, Guo S, Wang F et al (2019) Tamarixia radiata Behaviour is Influenced by Volatiles from Both Plants and Diaphorina citri Nymphs. Insects 10:141

    PubMed Central  Google Scholar 

  • Lu Z, Killiny N (2017) Huanglongbing pathogen Candidatus Liberibacter asiaticus exploits the energy metabolism and host defence responses of its vector Diaphorina citri. Physiological Entomology 42:319–335

    CAS  Google Scholar 

  • Lu Z jun, Zhou C hua, Yu H, zhong et al (2019) Potential roles of insect Tropomyosin1-X1 isoform in the process of Candidatus Liberibacter asiaticus infection of Diaphorina citri. Journal of Insect Physiology 114:125–135

  • Maluta NKP, Fereres A, Lopes S (2017) Settling preferences of the white fly vector Bemisia tabaci on infected plants varies with virus family and transmission mode. Entomologia Experimentalis et Applicata 165:1–10

    Google Scholar 

  • Mann RS, Pelz-stelinski K, Hermann SL et al (2011) Sexual Transmission of a Plant Pathogenic Bacterium, Candidatus Liberibacter asiaticus, between Conspecific Insect Vectors during Mating. PLoS One 6:e29197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mann RS, Ali JG, Hermann SL et al (2012) Induced Release of a Plant-Defense Volatile ‘Deceptively’ Attracts Insect Vectors to Plants Infected with a Bacterial Pathogen. PLoS One 8:e1002610

    CAS  Google Scholar 

  • Mann M, Fattah-Hosseini S, Ammar ED et al (2018) Diaphorina citri Nymphs Are Resistant to Morphological Changes Induced by “Candidatus Liberibacter asiaticus” in Midgut Epithelial Cells. Infection Immunity 86:1–19

    CAS  Google Scholar 

  • Martini X, Pelz-stelinski KS, Stelinski LL (2014) Plant pathogen-induced volatiles attract parasitoids to increase parasitism of an insect vector. Frontiers in Ecology Evolution 2:1–8

    Google Scholar 

  • Martini X, Hoffmann M, Coy MR et al (2015) Infection of an Insect Vector with a Bacterial Plant Pathogen Increases Its Propensity for Dispersal. PLoS One 10:e0129373

    PubMed  PubMed Central  Google Scholar 

  • Martini X, Coy M, Kuhns E, Stelinski LL (2018) Temporal Decline in Pathogen-Mediated Release of Methyl Salicylate Associated With Decreasing Vector Preference for Infected Over Uninfected Plants. Frontiers in Ecology Evolution 6:185

    Google Scholar 

  • Marutani-Hert M, Hunter WB, Morgan JK (2011) Associated Bacteria of Asian Citrus Psyllid (Hemiptera: Psyllidae: Diaphorina citri). Southwestern Entomologist 36:323–330

    Google Scholar 

  • Mauck KE, Moraes CM, De Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. PNAS 107:3600–3605

  • Mauck KE, Moraes CM, De Mescher MC (2016) Effects of pathogens on sensory-mediated interactions between plants and insect vectors. Current Opinion in Plant Biology 32:53–61

  • Medina RF, Nachappa P, Tamborindeguy C (2011) Differences in bacterial diversity of host-associated populations of Phylloxera notabilis Pergande (Hemiptera: Phylloxeridae) in pecan and water hickory. Journal of Evolutionary Biology 24:761–771

    CAS  PubMed  Google Scholar 

  • Meyer JM, Hoy MA (2007) Wolbachia-Associated Thelytoky in Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae), A Parasitoid of Asian Citrus Psyllid. Florida Entomologist 90:776–779

    CAS  Google Scholar 

  • Minard G, Mavingui P, Moro CV (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasites Vectors 6:146

    PubMed  PubMed Central  Google Scholar 

  • Molki B, Ha PT, Mohamed A et al (2019) Physiochemical changes mediated by “Candidatus Liberibacter asiaticus” in Asian citrus psyllids. Scientific Reports 9:16375

    PubMed  PubMed Central  Google Scholar 

  • Nachappa P, Levy J, Pierson E, Tamborindeguy C (2014) Correlation between ‘“Candidatus Liberibacter solanacearum”’ infection levels and fecundity in its psyllid vector. Journal of Invertebrate Pathology 115:55–61

    PubMed  Google Scholar 

  • Nakabachi A, Nikoh N, Oshima K et al (2013a) Horizontal gene acquisition of Liberibacter plant pathogens from a bacteriome-confined endosymbiont of their psyllid vector. PLoS One 8:e82612

    PubMed  PubMed Central  Google Scholar 

  • Nakabachi A, Ueoka R, Oshima K et al (2013) Defensive bacteriome symbiont with a drastically reduced genome. Current Biology 23:1478–1484

    CAS  PubMed  Google Scholar 

  • Nakjang S, Ndeh DA, Wipat A et al (2012) A Novel Extracellular Metallopeptidase Domain Shared by Animal Host-Associated Mutualistic and Pathogenic Microbes. PLoS One 7:e30287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nehela Y, Killiny N (2018) Infection with phytopathogenic bacterium inhibits melatonin biosynthesis, decreases longevity of its vector, and suppresses the free radical-defense. Journal of Pineal Research 65:e12511

    PubMed  Google Scholar 

  • Nehela Y, Hijaz F, Elzaawely AA et al (2018) Citrus phytohormonal response to Candidatus Liberibacter asiaticus and its vector Diaphorina citri. Physiological and Molecular Plant Pathology 102:24–35

    CAS  Google Scholar 

  • Nouri S, Salem N, Nigg JC, Falk BW (2016) Diverse Array of New Viral Sequences Identified in Worldwide Populations of the Asian Citrus Psyllid (Diaphorina citri) Using Viral Metagenomics. Journal of Virology 90:2434–2445

    CAS  PubMed Central  Google Scholar 

  • Nouri S, Matsumura EE, Kuo Y, Falk BW (2018) Insect-specific viruses: from discovery to potential translational applications. Current Opinion in Virology 33:33–41

    PubMed  Google Scholar 

  • Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. PNAS 100:1803–1807

    CAS  PubMed  Google Scholar 

  • Orlovskis Z, Canale MC, Thole V et al (2015) Insect-borne plant pathogenic bacteria: getting a ride goes beyond physical contact. Current Opinion in Insect Science 9:16–23

    PubMed  Google Scholar 

  • Parra RP, Alves GR, Jose A, Diniz F (2016) Tamarixia radiata (Hymenoptera: Eulophidae) x Diaphorina citri (Hemiptera: Liviidae): Mass Rearing and Potential Use of the Parasitoid in Brazil. Journal of Integrated Pest Management 7:1–11

    Google Scholar 

  • Patt JM, Robbins PS, Niedz R et al (2018) Exogenous application of the plant signalers methyl jasmonate and salicylic acid induces changes in volatile emissions from citrus foliage and influences the aggregation behavior of Asian citrus psyllid (Diaphorina citri), vector of Huanglongbing. PLoS One 13:e0193724

    PubMed  PubMed Central  Google Scholar 

  • Pelz-stelinski AKS, Brlansky RH, Ebert TA et al (2010) Transmission Parameters for Candidatus Liberibacter asiaticus by Asian Citrus Psyllid (Hemiptera: Psyllidae). Journal of Economic Entomology 103:1531–1541

    CAS  PubMed  Google Scholar 

  • Pelz-Stelinski KS, 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 109:371–376

  • Perilla-Henao LM, Casteel CL (2016) Vector-Borne Bacterial Plant Pathogens: Interactions with Hemipteran Insects and Plants. Frontiers in Plant Sciences 7:1163

    Google Scholar 

  • Pradit N, Mescher MC, De Moraes CM, Rodriguez-Saona C (2019) Phytoplasma Infection of Cranberry Affects Development and Oviposition, but Not Host-Plant Selection, of the Insect Vector Limotettix vaccinii. Journal of Chemical Ecology

  • Priya NG, Ojha A, Kajla MK et al (2012) Host Plant Induced Variation in Gut Bacteria of Helicoverpa armigera. PLoS One 7:e30768

    PubMed  Google Scholar 

  • Purcell AH (1982) Insect vector relationships with procaryotic plant pathogens. Annual Review of Phytopathology 20:397–417

    Google Scholar 

  • Ramsey JS, Johnson RS, Hoki JS et al (2015) Metabolic Interplay between the Asian Citrus Psyllid and Its Profftella Symbiont: An Achilles ’ Heel of the Citrus Greening Insect Vector. 1–21

  • Ramsey JS, Chavez JD, Johnson R et al (2017) Protein interaction networks at the host-microbe interface in Diaphorina citri, the insect vector of the citrus greening pathogen. Royal Society Open Science 4:160545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ren S-L, Li Y-H, Zhou Y-T et al (2016) Effects of Candidatus Liberibacter asiaticus on the fitness of the vector Diaphorina citri. Journal of Applied Microbiology 121:1718–1726

    PubMed  Google Scholar 

  • Ren S-L, Li Y-H, Ou D et al (2018) Localization and dynamics of Wolbachia infection in Asian citrus psyllid Diaphorina citri, the insect vector of the causal pathogens of Huanglongbing. Microbiology Open 7:e00561

    PubMed  Google Scholar 

  • Saha S, Hunter WB, Reese J et al (2012) Survey of Endosymbionts in the Diaphorina citri Metagenome and Assembly of a Wolbachia wDi Draft Genome. PLoS One 7:e50067

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simon J-C, Alenc E, Guy E et al (2015) Genomics of adaptation to host-plants in herbivorous insects. Briefings in Functional Genomics 14:413–423

    CAS  PubMed  Google Scholar 

  • Song X, Peng A, Ling J et al (2019) Composition and change in the microbiome of Diaphorina citri infected with Candidatus Liberibacter asiaticus in China. International Journal of Tropical Insect Science, 1–8

  • Stelinski LL (2019) Ecological Aspects of the Vector-Borne Bacterial Disease, Citrus Greening (Huanglongbing): Dispersal and Host Use by Asian Citrus Psyllid. Diaphorina citri Kuwayama Insects 10:208

  • Subandiyah S, Nikoh N, Tsuyumu S et al (2000) Complex Endosymbiotic Microbiota of the Citrus Psyllid Diaphorina citri (Homoptera: Psylloidea). Zoological Sciences 17:983–989

    Google Scholar 

  • Sule H, Muhamad R, Omar D, Hee AK-W (2012) Response of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to Volatiles Emitted from Leaves of Two Rutaceous Plants. The Journal of Agricultural Science 4:152–159

    Google Scholar 

  • Sun YX, Zhu BJ, Tang L et al (2017) Cathepsin O is involved in the innate immune response and metamorphosis of Antheraea pernyi. Journal of Invertebrate Pathology 150:6–14

    CAS  PubMed  Google Scholar 

  • Tamborindeguy C, Huot OB, Ibanez F, Levy J (2017) The influence of bacteria on multi-trophic interactions among plants, psyllids, and pathogen. Insect Sciences 24:961–974

    Google Scholar 

  • Teck SLC, Fatimah A, Beattie A et al (2011) Influence of Host Plant Species and Flush Growth Stage on the Asian Citrus Psyllid. Diaphorina citri Kuwayama American Journal of Agricultural Biological Sciences 6:536–543

  • Teixeira DDC, Saillard C, Eveillard S et al (2005) “Candidatus Liberibacter americanus”, associated with citrus huanglongbing (greening disease) in São Paulo State, Brazil. International Journal of Systematic and Evolutionary Microbiology 55:1857–1862

    CAS  PubMed  Google Scholar 

  • Teulier L, Weber JM, Crevier J, Darveau CA (2016) Proline as a fuel for insect flight: Enhancing carbohydrate oxidation in hymenopterans. Proceedings of the Royal Society B: Biological Sciences. 283: 20160333

  • Tiwari S, Gondhalekar a D, Mann RS et al (2011) Characterization of five CYP4 genes from Asian citrus psyllid and their expression levels in Candidatus Liberibacter asiaticus-infected and uninfected psyllids. Insect Molecular Biology 20:733–744

    CAS  PubMed  Google Scholar 

  • Tiwari S, Pelz-Stelinski K, Mann RS, Stelinski LL (2011) Glutathione Transferase and Cytochrome P450 (General Oxidase) Activity Levels in Candidatus Liberibacter Asiaticus-Infected and Uninfected Asian Citrus Psyllid (Hemiptera: Psyllidae). Annals of the Entomological Society of America 104:297–305

    CAS  Google Scholar 

  • Tiwari S, Pelz-Stelinski K, Stelinski LL (2011c) Effect of Candidatus Liberibacter asiaticus infection on susceptibility of Asian citrus psyllid, Diaphorina citri, to selected insecticides. Pest Management Sciences 67:94–99

    CAS  Google Scholar 

  • Tiwari S, Killiny N, Mann RS et al (2012) Abdominal color of the Asian citrus psyllid, Diaphorina citri, is associated with susceptibility to various insecticides. Pest Management Science 69:535–541

    PubMed  Google Scholar 

  • Vahling CM, Duan Y, Lin H (2010) Characterization of an ATP translocase identified in the destructive plant pathogen “Candidatus Liberibacter asiaticus.” Journal of Bacteriology 192:834–840

  • Vaidyanathan R, Scott TW (2006) Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11:1643–1651

    CAS  PubMed  Google Scholar 

  • Vyas M, Fisher TW, He R et al (2015) Asian Citrus Psyllid Expression Profiles Suggest Candidatus Liberibacter Asiaticus-Mediated Alteration of Adult Nutrition and Metabolism, and of Nymphal Development and Immunity. PLoS One 10:e0130328

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Wang N, Pierson EA, Setubal C et al (2017) The Candidatus Liberibacter-Host Interface: Insights into Pathogenesis Mechanisms and Disease Control. Annual Review of Phytopathology 55:1–32

    CAS  Google Scholar 

  • Wenninger EJ, Stelinski LL, Hall DG (2008) Behavioral evidence for a female-produced sex attractant in Diaphorina citri. Entomologia Experimentalis et Applicata 128:450–459

    Google Scholar 

  • Wenninger EJ, Stelinski LL, Hall DG (2009) Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants. Environmental Entomology 38:225–234

    PubMed  Google Scholar 

  • Wenninger EJ, Stelinski LL, Hall DG (2009) Relationships Between Adult Abdominal Color and Reproductive Potential in Diaphorina citri (Hemiptera: Psyllidae). Annals of the Entomological Society of America 102:476–483

    Google Scholar 

  • Wu F, Cen Y, Deng X et al (2015) Movement of Diaphorina citri (Hemiptera: Liviidae) adults between huanglongbing-infected and healthy citrus. Florida Entomologist 98:410–416

    Google Scholar 

  • Wu T, Luo X, Xu C et al (2016) Feeding behavior of Diaphorina citri and its transmission of ‘Candidatus Liberibacter asiaticus’ to citrus. Entomologia Experimentalis et Applicata 161:104–111

    Google Scholar 

  • Wu F, Huang J, Xu M et al (2018) Host and environmental factors influencing ‘Candidatus Liberibacter asiaticus’ acquisition in Diaphorina citri. Pest Management Sciences 74:2738–2746

    CAS  Google Scholar 

  • Yu X, Gowda S, Killiny N (2017) Double stranded RNA delivery through soaking, mediates silencing of the muscle protein 20 and increases mortality to the Asian citrus psyllid, Diaphorina citri. Pest Management Sciences 73:1846–1853

    CAS  Google Scholar 

  • Yu X, Killiny N (2018) Effect of silencing a boule homologue on the survival and reproduction of Asian citrus psyllid Diaphorina citri. Physiological Entomology 1–8

  • Yu H-Z, Huang Y-L, Li N-Y et al (2019) Potential roles of two Cathepsin genes, DcCath-L and DcCath-O in the innate immune response of Diaphorina citri. Journal of Asia-Pacific Entomology 22:1060–1069

    Google Scholar 

  • Zanardi OZ, Volpe HXL, Favaris AP et al (2018) Putative sex pheromone of the Asian citrus psyllid, Diaphorina citri, breaks down into an attractant. Scientific Reports 8:1–11

    CAS  Google Scholar 

  • Zhou G, Isoe J, Day WA, Miesfeld RL (2011) Alpha-COPI Coatomer Protein Is Required for Rough Endoplasmic Reticulum Whorl Formation in Mosquito Midgut Epithelial Cells. PLoS One 6:e18150

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Wang H, Zeng X, Xue P (2013) Differences in Selection Behaviors and Chemical Cues of adult Asian Citrus Psyllids, Diaphorina citri, on Healthy and Huanglongbing-Infected Young Shoots of Citrus Plants. The Journal of Agricultural Science 5:83–91

    Google Scholar 

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Acknowledgements

This work has been supported by INCT Citrus (CNPQ 465440/2014–2 and FAPESP 2014/50880–0). DMG received CNPQ postdoctoral fellow (103228/2018-7); LMG and GRA are currently postdoctoral fellows (FAPESP 2019/01901-8 and FAPESP 2016/24998-9). MR is supported by the Florida State legislative funding for the UF/IFAS Citrus Initiative. DT is funded by the USDA NIFA-SCRI award number 2019-70016-29096. DMG and ISP contributed equally to this work.

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Galdeano, D.M., de Souza Pacheco, I., Alves, G.R. et al. Friend or foe? Relationship between ‘Candidatus Liberibacter asiaticus’ and Diaphorina citri. Trop. plant pathol. 45, 559–571 (2020). https://doi.org/10.1007/s40858-020-00375-4

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