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Annual Review of Entomology

Volume 69, 2024

The Hidden Secrets of Psylloidea: Biology, Behavior, Symbionts, and Ecology

Abstract

Psyllids constitute a diverse group of sap-feeding Sternorrhyncha that were relatively obscure until it was discovered that a handful of species transmit bacterial plant pathogens. Yet the superfamily Psylloidea is much richer than the sum of its crop-associated vectors, with over 4,000 described species exhibiting diverse life histories and host exploitation strategies. A growing body of research is uncovering fascinating insights into psyllid evolution, biology, behavior, and species interactions. This work has revealed commonalities and differences with better-studied Sternorrhyncha, as well as unique evolutionary patterns of lineage divergence and host use. We are also learning how psyllid evolution and foraging ecology underlie life history traits and the roles of psyllids in communities. At finer scales, we are untangling the web of symbionts across the psyllid family tree, linking symbiont and psyllid lineages, and revealing mechanisms underlying reciprocal exchange between symbiont and host. In this review, we synthesize and summarize key advances within these areas with a focus on free-living (nongalling) Psylloidea.

Keyword(s): adaptation, codivergence, evolution, keystone species, microbiome, plant–insect interactions
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2024-01-25
2024-05-04
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Literature Cited

  1. 1.
    Ammar E-D, Hall DG, Shatters RG Jr. 2013. Stylet morphometrics and citrus leaf vein structure in relation to feeding behavior of the Asian citrus psyllid Diaphorina citri, vector of citrus huanglongbing bacterium. PLOS ONE 8:3e59914
     [Google Scholar]
  2. 2.
    Anderbrant O, Yuvaraj JK, Høgetveit L-A, Nissinen AI, Andersson MN. 2020. Electrophysiological responses of carrot psyllids (Trioza apicalis), in different phases of their life cycle, to volatile carrot and conifer compounds. J. Appl. Entomol. 144:3236–40
     [Google Scholar]
  3. 3.
    Ando Y, Utsumi S, Ohgushi T. 2017. Aphid as a network creator for the plant-associated arthropod community and its consequence for plant reproductive success. Funct. Ecol. 31:3632–41
     [Google Scholar]
  4. 4.
    Arp A, Munyaneza JE, Crosslin JM, Trumble J, Bextine B. 2014. A global comparison of Bactericera cockerelli (Hemiptera: Triozidae) microbial communities. Environ. Entomol. 43:2344–52
     [Google Scholar]
  5. 5.
    Avosani S, Mankin RW, Sullivan TES, Polajnar J, Suckling DM, Mazzoni V 2022. Vibrational communication in psyllids. Biotremology: Physiology, Ecology, and Evolution PSM Hill, V Mazzoni, N Stritih-Peljhan, M Virant-Doberlet, A Wessel 529–46. Berlin: Springer
     [Google Scholar]
  6. 6.
    Bonani JP, Fereres A, Garzo E, Miranda MP, Appezzato-Da-Gloria B, Lopes JRS. 2010. Characterization of electrical penetration graphs of the Asian citrus psyllid, Diaphorina citri, in sweet orange seedlings. Entomol. Exp. Appl. 134:135–49
     [Google Scholar]
  7. 7.
    Borges KM, Cooper WR, Garczynski SF, Thinakaran J, Jensen AS et al. 2017.. “ Candidatus Liberibacter solanacearum” associated with the psyllid, Bactericera maculipennis (Hemiptera: Triozidae). Environ. Entomol. 46:2210–16
     [Google Scholar]
  8. 8.
    Brennan EB, Weinbaum SA. 2001. Stylet penetration and survival of three psyllid species on adult leaves and “waxy” and “de-waxed” juvenile leaves of Eucalyptus globulus. Entomol. Exp. Appl. 100:3355–63
     [Google Scholar]
  9. 9.
    Burckhardt D, Ouvrard D, Percy DM. 2021. An updated classification of the jumping plant-lice (Hemiptera: Psylloidea) integrating molecular and morphological evidence. Eur. J. Taxon. 736:137–82
     [Google Scholar]
  10. 10.
    Burckhardt D, Ouvrard D, Queiroz D, Percy D. 2014. Psyllid host-plants (Hemiptera: Psylloidea): resolving a semantic problem. Fla. Entomol. 97:1242–46
     [Google Scholar]
  11. 11.
    Burckhardt D, Raman A, Schaefer CW, Withers TM 2005. Biology, ecology, and evolution of gall-inducing psyllids (Hemiptera: Psylloidea). Biology, Ecology, and Evolution of Gall-Inducing Arthropods A Raman, CW Schaefer, TM Withers 143–57. Boca Raton, FL: CRC Press
     [Google Scholar]
  12. 12.
    Carlson CR, Ter Horst AM, Johnston JS, Henry E, Falk BW, Kuo Y-W 2022. High-quality, chromosome-scale genome assemblies: comparisons of three Diaphorina citri (Asian citrus psyllid) geographic populations. DNA Res. 29:4dsac027
     [Google Scholar]
  13. 13.
    Chambers GA, Donovan NJ, Bogema DR, Om N, Beattie GAC et al. 2020. Draft genome sequence of a novel “Candidatus Liberibacter” species detected in a Zanthoxylum species from Bhutan. Microbiol. Resour. Announc. 9:40e00897-20
     [Google Scholar]
  14. 13a.
    Cho G, Burckhardt D, Lee S 2022. Check list of jumping plant-lice (Hemiptera: Psylloidea) of the Korean Peninsula. Zootaxa 5177:11–91
     [Google Scholar]
  15. 14.
    Chrostek E, Pelz-Stelinski K, Hurst GDD, Hughes GL. 2017. Horizontal transmission of intracellular insect symbionts via plants. Front. Microbiol. 8:2237
     [Google Scholar]
  16. 15.
    Chu C-C, Hoffmann M, Braswell WE, Pelz-Stelinski KS. 2019. Genetic variation and potential coinfection of Wolbachia among widespread Asian citrus psyllid (Diaphorina citri Kuwayama) populations. Insect Sci. 26:4671–82
     [Google Scholar]
  17. 16.
    Cicero JM, Fisher TW, Qureshi JA, Stansly PA, Brown JK. 2017. Colonization and intrusive invasion of potato psyllid by “Candidatus Liberibacter solanacearum. .” Phytopathology 107:136–49
     [Google Scholar]
  18. 17.
    Cifuentes-Arenas JC, de Goes A, de Miranda MP, Beattie GAC, Lopes SA. 2018. Citrus flush shoot ontogeny modulates biotic potential of Diaphorina citri. PLOS ONE 13:1e0190563
     [Google Scholar]
  19. 18.
    Clark KJ, Pang Z, Trinh J, Wang N, Ma W. 2020. Sec-Delivered Effector 1 (SDE1) of “Candidatus Liberibacter asiaticus” promotes citrus Huanglongbing. Mol. Plant Microbe Interact. 33:121394–404
     [Google Scholar]
  20. 19.
    Cooper W, Swisher Grimm K, Angelella G, Mustafa T. 2023. Acquisition and transmission of “Candidatus Liberibacter solanacearum” differs among Wolbachia-infected and -uninfected haplotypes of Bactericera cockerelli. Plant Dis. In press
    [Google Scholar]
  21. 20.
    Cooper WR, Esparza-Diaz G, Wildung MR, Horton DR, Badillo-Vargas IE, Halbert SE. 2022. Association of two Bactericera species (Hemiptera: Triozidae) with native Lycium spp. (Solanales: Solanaceae) in the potato growing regions of the Rio Grande Valley of Texas. Environ. Entomol. 52:198–107
     [Google Scholar]
  22. 21.
    Cooper WR, Horton DR, Wildung MR, Jensen AS, Thinakaran J et al. 2019. Host and non-host “whistle stops” for psyllids: Molecular gut content analysis by high-throughput sequencing reveals landscape-level movements of Psylloidea (Hemiptera). Environ. Entomol. 48:3554–66
     [Google Scholar]
  23. 22.
    Coutinho-Abreu IV, McInally S, Forster L, Luck R, Ray A. 2014. Odor coding in a disease-transmitting herbivorous insect, the Asian citrus psyllid. Chem. Senses 39:6539–49
     [Google Scholar]
  24. 23.
    Crawford SA, Wilkens S. 1996. Ultrastructural aspects of damage to leaves of Eucalyptus camaldulensis by the psyllid Cardiaspina retator. Micron 27:5359–66
     [Google Scholar]
  25. 24.
    Czarnobai De Jorge B, Hummel HE, Gross J. 2022. Repellent activity of clove essential oil volatiles and development of nanofiber-based dispensers against pear psyllids (Hemiptera: Psyllidae). Insects 13:8743
     [Google Scholar]
  26. 25.
    da Graça JV, Cook G, Ajene IJ, Grout TG, Pietersen G et al. 2022. A review of the “Candidatus Liberibacter africanus” citrus pathosystem in Africa. Phytopathology 112:144–54
     [Google Scholar]
  27. 26.
    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 12:12e0189779
     [Google Scholar]
  28. 27.
    Davidson MM, Butler RC, Taylor NM, Nielsen M-C, Sansom CE, Perry NB. 2014. A volatile compound, 2-undecanone, increases walking but not flying tomato potato psyllid movement toward an odour source. N. Z. Plant Prot. 67:184–90
     [Google Scholar]
  29. 28.
    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 7:11e49330
     [Google Scholar]
  30. 29.
    de Godoy Gasparoto MC, Primiano IV, Bassanezi RB, Lourenço SA, Montesino LH et al. 2022. Prevalent transmission of “Candidatus Liberibacter asiaticus” over “Ca. Liberibacter americanus” in a long-term controlled environment. Phytopathology 112:1180–88
     [Google Scholar]
  31. 30.
    de Oliveira Del Piero FHM, Wilcken CF, Domingues MM, Favoreto AL, Rodella RA et al. 2022. Anatomical indicators of Eucalyptus spp. resistance to Glycaspis brimblecombei (Hemiptera: Aphalaridae). PeerJ 10:e13346
     [Google Scholar]
  32. 31.
    de Souza Pacheco I, Galdeano DM, Maluta NKP, Lopes JRS, Machado MA. 2020. Gene silencing of Diaphorina citri candidate effectors promotes changes in feeding behaviors. Sci. Rep. 10:5992
     [Google Scholar]
  33. 32.
    Döring TF, Kirchner SM. 2022. A model for colour preference behaviour of spring migrant aphids. Philos. Trans. R. Soc. Lond. B 377:186220210283
     [Google Scholar]
  34. 33.
    Dossi FCA, da Silva EP, Cônsoli FL. 2014. Population dynamics and growth rates of endosymbionts during Diaphorina citri (Hemiptera, Liviidae) ontogeny. Microb. Ecol. 68:4881–89
     [Google Scholar]
  35. 34.
    Farnier K, Davies NW, Steinbauer MJ. 2018. Not led by the nose: Volatiles from undamaged Eucalyptus hosts do not influence psyllid orientation. Insects 9:4166
     [Google Scholar]
  36. 35.
    Farnier K, Dyer AG, Steinbauer MJ. 2014. Related but not alike: Not all Hemiptera are attracted to yellow. Front. Ecol. Evol. 2:67
     [Google Scholar]
  37. 36.
    Farnier K, Dyer AG, Taylor GS, Peters RA, Steinbauer MJ. 2015. Visual acuity trade-offs and microhabitat-driven adaptation of searching behaviour in psyllids (Hemiptera: Psylloidea: Aphalaridae). J. Exp. Biol. 218:Pt 101564–71
     [Google Scholar]
  38. 37.
    Farnier K, Steinbauer MJ. 2016. Elevated anthocyanins protect young Eucalyptus leaves from high irradiance but also indicate foliar nutritional quality to visually attuned psyllids. Ecol. Entomol. 41:2168–81
     [Google Scholar]
  39. 38.
    Frampton RA, Thompson SM, Kalamorz F, David C, Addison SM, Smith GR. 2018. Draft genome sequence of a “Candidatus Liberibacter europaeus” strain assembled from broom psyllids (Arytainilla spartiophila) from New Zealand. Genome Announc. 6:20e00430-18
     [Google Scholar]
  40. 39.
    Fromont C, Riegler M, Cook JM. 2016. Phylogeographic analyses of bacterial endosymbionts in fig homotomids (Hemiptera: Psylloidea) reveal codiversification of both primary and secondary endosymbionts. FEMS Microbiol. Ecol. 92:12fiw205
     [Google Scholar]
  41. 40.
    Fromont C, Riegler M, Cook JM. 2017. Relative abundance and strain diversity in the bacterial endosymbiont community of a sap-feeding insect across its native and introduced geographic range. Microb. Ecol. 74:3722–34
     [Google Scholar]
  42. 41.
    Fukatsu T, Nikoh N. 1998. Two intracellular symbiotic bacteria from the mulberry psyllid Anomoneura mori (Insecta, Homoptera). Appl. Environ. Microbiol. 64:103599–606
     [Google Scholar]
  43. 42.
    Gallinger J, Jarausch B, Jarausch W, Gross J. 2020. Host plant preferences and detection of host plant volatiles of the migrating psyllid species Cacopsylla pruni, the vector of European stone fruit yellows. J. Pest Sci. 93:1461–75
     [Google Scholar]
  44. 43.
    George J, Ammar E-D, Hall DG, Lapointe SL. 2017. Sclerenchymatous ring as a barrier to phloem feeding by Asian citrus psyllid: evidence from electrical penetration graph and visualization of stylet pathways. PLOS ONE 12:3e0173520
     [Google Scholar]
  45. 44.
    George J, Paris TM, Allan SA, Lapointe SL, Stelinski LL. 2020. UV reflective properties of magnesium oxide increase attraction and probing behavior of Asian citrus psyllids (Hemiptera: Liviidae). Sci. Rep. 10:1890
     [Google Scholar]
  46. 45.
    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. 6:33418
     [Google Scholar]
  47. 46.
    Ghosh S, Sela N, Kontsedalov S, Lebedev G, Haines LR, Ghanim M. 2020. An intranuclear Sodalis-like symbiont and Spiroplasma coinfect the carrot psyllid, Bactericera trigonica (Hemiptera, Psylloidea). Microorganisms 8:5692
     [Google Scholar]
  48. 47.
    Gilby AR, McKellar JW, Beaton CD. 1976. The structure of lerps: carbohydrate, lipid, and protein components. J. Insect Physiol. 22:5689–96
     [Google Scholar]
  49. 48.
    Grimm KDS, Horton DR, Lewis TM, Garczynski SF, Jensen AS, Charlton BA. 2022. Identification of three new “Candidatus Liberibacter solanacearum” haplotypes in four psyllid species (Hemiptera: Psylloidea). Sci. Rep. 12:20618
     [Google Scholar]
  50. 49.
    Guédot C, Horton DR, Landolt PJ. 2010. Sex attraction in Bactericera cockerelli (Hemiptera: Triozidae). Environ. Entomol. 39:41302–8
     [Google Scholar]
  51. 50.
    Haapalainen M, Wang J, Latvala S, Lehtonen MT, Pirhonen M, Nissinen AI. 2018. Genetic variation of “Candidatus Liberibacter solanacearum” Haplotype C and identification of a novel haplotype from Trioza urticae and stinging nettle. Phytopathology 108:8925–34
     [Google Scholar]
  52. 51.
    Hall AAG, Morrow JL, Fromont C, Steinbauer MJ, Taylor GS et al. 2016. Codivergence of the primary bacterial endosymbiont of psyllids versus host switches and replacement of their secondary bacterial endosymbionts. Environ. Microbiol. 18:82591–603
     [Google Scholar]
  53. 52.
    Hansen AK, Sanchez AN, Kwak Y. 2022. Divergent host-microbe interaction and pathogenesis proteins detected in recently identified Liberibacter species. Microbiol. Spectr 10:4e0209122
     [Google Scholar]
  54. 53.
    Hansen AK, Trumble JT, Stouthamer R, Paine TD. 2008. A new Huanglongbing species, “Candidatus Liberibacter psyllaurous,” found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Appl. Environ. Microbiol. 74:185862–65
     [Google Scholar]
  55. 54.
    Harrison K, Mendoza-Herrera A, Levy JG, Tamborindeguy C. 2021. Lasting consequences of psyllid (Bactericera cockerelli L.) infestation on tomato defense, gene expression, and growth. BMC Plant Biol. 21:114
     [Google Scholar]
  56. 55.
    Haythorpe KM, McDonald PG. 2010. Non-lethal foraging by bell miners on a herbivorous insect: potential implications for forest health. Austral Ecol. 35:4444–50
     [Google Scholar]
  57. 56.
    Higgins SA, Mann M, Heck M. 2022. Strain tracking of “Candidatus Liberibacter asiaticus,” the citrus greening pathogen, by high-resolution microbiome analysis of Asian citrus psyllids. Phytopathology 112:112273–87
     [Google Scholar]
  58. 57.
    Hodkinson ID. 2009. Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J. Nat. Hist. 43:1–265–179
     [Google Scholar]
  59. 58.
    Hollis D. 2004. Australian Psylloidea: Jumping Plant Lice and Lerp Insects. Canberra: Aust. Biol. Res. Study
  60. 59.
    Hosseinzadeh S, Shams-Bakhsh M, Mann M, Fattah-Hosseini S, Bagheri A et al. 2019. Distribution and variation of bacterial endosymbiont and “Candidatus Liberibacter asiaticus” titer in the huanglongbing insect vector, Diaphorina citri Kuwayama. Microb. Ecol. 78:1206–22
     [Google Scholar]
  61. 60.
    Husnik F, Nikoh N, Koga R, Ross L, Duncan RP et al. 2013. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153:71567–78
     [Google Scholar]
  62. 61.
    Jarausch B, Tedeschi R, Sauvion N, Gross J, Jarausch W 2019. Psyllid vectors. Phytoplasmas: Plant Pathogenic Bacteria, Vol. II Transmission and Management of Phytoplasma-Associated Diseases A Bertaccini, PG Weintraub, GP Rao, N Mori 53–78. Berlin: Springer
     [Google Scholar]
  63. 62.
    Kristoffersen L, Larsson MC, Anderbrant O. 2008. Functional characteristics of a tiny but specialized olfactory system: olfactory receptor neurons of carrot psyllids (Homoptera: Triozidae). Chem. Senses 33:9759–69
     [Google Scholar]
  64. 63.
    Kruse A, Fattah-Hosseini S, Saha S, Johnson R, Warwick E 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 12:6e0179531
     [Google Scholar]
  65. 64.
    Kube M, Schneider B, Kuhl H, Dandekar T, Heitmann K et al. 2008. The linear chromosome of the plant-pathogenic mycoplasma “Candidatus Phytoplasma mali. .” BMC Genom. 9:306
     [Google Scholar]
  66. 65.
    Kwak Y, Argandona JA, Degnan PH, Hansen AK. 2022. Chromosomal-level assembly of Bactericera cockerelli reveals rampant gene family expansions impacting genome structure, function and insect-microbe-plant-interactions. Mol. Ecol. Resour. 23:1233–52
     [Google Scholar]
  67. 66.
    Kwak Y, Sun P, Meduri VR, Percy DM, Mauck KE, Hansen AK. 2021. Uncovering symbionts across the psyllid tree of life and the discovery of a new Liberibacter species, “Candidatus” Liberibacter capsica. Front. Microbiol. 12:739763
     [Google Scholar]
  68. 67.
    Lambert JD, Moran NA. 1998. Deleterious mutations destabilize ribosomal RNA in endosymbiotic bacteria. PNAS 95:84458–62
     [Google Scholar]
  69. 68.
    Lambert KTA, Reid N, Loyn RH, McDonald PG. 2022. Understanding and managing the role of bell miners (Manorina melanophrys) in forest dieback: a review of the ecological and management evidence. For. Ecol. Manag. 523:120470
     [Google Scholar]
  70. 69.
    Liao Y-C, Percy DM, Yang M-M. 2022. Biotremology: vibrational communication of Psylloidea. Arthropod Struct. Dev. 66:101138
     [Google Scholar]
  71. 70.
    Lin C-Y, Achor D, Levy A. 2021. Intracellular life cycle of “Candidatus Liberibacter asisticus” inside psyllid gut cells. Phytopathology 112:145–53
     [Google Scholar]
  72. 71.
    Lubanga UK, Drijfhout FP, Farnier K, Steinbauer MJ. 2016. The long and the short of mate attraction in a psylloid: Do semiochemicals mediate mating in Aacanthocnema dobsoni Froggatt?. J. Chem. Ecol. 42:2163–72
     [Google Scholar]
  73. 72.
    Luft PA, Paine TD, Walker GP. 2001. Interactions of colonisation density and leaf environments on survival of Trioza eugeniae nymphs. Ecol. Entomol. 26:3263–70
     [Google Scholar]
  74. 73.
    Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski KS et al. 2012. Induced release of a plant-defense volatile “deceptively” attracts insect vectors to plants infected with a bacterial pathogen. PLOS Pathog. 8:3e1002610
     [Google Scholar]
  75. 74.
    Mauck KE, Sun P, Meduri V, Hansen AK. 2019. New Ca. Liberibacter psyllaurous haplotype resurrected from a 49-year-old specimen of Solanum umbelliferum: a native host of the psyllid vector. Sci. Rep. 9:9530
     [Google Scholar]
  76. 75.
    Mayer CJ, Jarausch B, Jarausch W, Jelkmann W, Vilcinskas A, Gross J. 2009. Cacopsylla melanoneura has no relevance as a vector of apple proliferation in Germany. Phytopathology 99:6729–38
     [Google Scholar]
  77. 76.
    McCalla KA, Milosavljević I, Hoddle MS. 2023. A low-toxicity baiting program precipitates collapse of Argentine ant and ant-associated hemipteran pest populations in commercial citrus. Biol. Control 177:105105
     [Google Scholar]
  78. 77.
    Meiners JM, Griswold TL, Harris DJ, Ernest SKM. 2017. Bees without flowers: Before peak bloom, diverse native bees find insect-produced honeydew sugars. Am. Nat. 190:2281–91
     [Google Scholar]
  79. 78.
    Mi X, Feng G, Hu Y, Zhang J, Chen L et al. 2021. The global significance of biodiversity science in China: an overview. Natl. Sci. Rev. 8:7nwab032
     [Google Scholar]
  80. 79.
    Mishra S, Ghanim M. 2022. Interactions of Liberibacter species with their psyllid vectors: molecular, biological and behavioural mechanisms. Int. J. Mol. Sci. 23:74029
     [Google Scholar]
  81. 80.
    Mittelberger C, Obkircher L, Oettl S, Oppedisano T, Pedrazzoli F et al. 2017. The insect vector Cacopsylla picta vertically transmits the bacterium “Candidatus Phytoplasma mali” to its progeny. Plant Pathol. 66:61015–21
     [Google Scholar]
  82. 81.
    Moreno A, Miranda MP, Fereres A. 2021. Psyllids as major vectors of plant pathogens. Entomol. Gen. 41:5419–38
     [Google Scholar]
  83. 82.
    Morris J, Shiller J, Mann R, Smith G, Yen A, Rodoni B. 2017. Novel “Candidatus Liberibacter” species identified in the Australian eggplant psyllid, Acizzia solanicola. Microb. Biotechnol. 10:4833–44
     [Google Scholar]
  84. 83.
    Morrow JL, Hall AAG, Riegler M. 2017. Symbionts in waiting: the dynamics of incipient endosymbiont complementation and replacement in minimal bacterial communities of psyllids. Microbiome 5:158
     [Google Scholar]
  85. 84.
    Morrow JL, Om N, Beattie GAC, Chambers GA, Donovan NJ et al. 2020. Characterization of the bacterial communities of psyllids associated with Rutaceae in Bhutan by high throughput sequencing. BMC Microbiol. 20:215
     [Google Scholar]
  86. 85.
    Nachappa P, Levy J, Pierson E, Tamborindeguy C. 2014. Correlation between “Candidatus Liberibacter solanacearum” infection levels and fecundity in its psyllid vector. J. Invertebr. Pathol. 115:55–61
     [Google Scholar]
  87. 86.
    Nachappa P, Shapiro AA, Tamborindeguy C. 2012. Effect of “Candidatus Liberibacter solanacearum” on fitness of its insect vector, Bactericera cockerelli (Hemiptera: Triozidae), on tomato. Phytopathology 102:141–46
     [Google Scholar]
  88. 87.
    Nakabachi A, Inoue H, Hirose Y. 2022. High-resolution microbiome analyses of nine psyllid species of the family Triozidae identified previously unrecognized but major bacterial populations, including Liberibacter and Wolbachia of Supergroup O. Microbes Environ. 37:4ME22078
     [Google Scholar]
  89. 88.
    Nakabachi A, Inoue H, Hirose Y. 2022. Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids. BMC Microbiol. 22:15
     [Google Scholar]
  90. 89.
    Nakabachi A, Malenovský I, Gjonov I, Hirose Y. 2020. 16S rRNA sequencing detected Profftella, Liberibacter, Wolbachia, and Diplorickettsia from relatives of the Asian citrus psyllid. Microb. Ecol. 80:2410–22
     [Google Scholar]
  91. 90.
    Nakabachi A, Piel J, Malenovský I, Hirose Y. 2020. Comparative genomics underlines multiple roles of Profftella, an obligate symbiont of psyllids: providing toxins, vitamins, and carotenoids. Genome Biol. Evol. 12:111975–87
     [Google Scholar]
  92. 91.
    Nakabachi A, Ueoka R, Oshima K, Teta R, Mangoni A et al. 2013. Defensive bacteriome symbiont with a drastically reduced genome. Curr. Biol. 23:151478–84
     [Google Scholar]
  93. 92.
    Nakabachi A, Yamashita A, Toh H, Ishikawa H, Dunbar HE et al. 2006. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314:5797267
     [Google Scholar]
  94. 93.
    Nehlin G, Valterová I, Borg-Karlson AK. 1994. Use of conifer volatiles to reduce injury caused by carrot psyllid, Trioza apicalis, Förster (Homoptera, Psylloidea). J. Chem. Ecol. 20:3771–83
     [Google Scholar]
  95. 94.
    Nelson AS, Mooney KA. 2022. The evolution and ecology of interactions between ants and honeydew-producing hemipteran insects. Annu. Rev. Ecol. Evol. Syst. 53:379–402
     [Google Scholar]
  96. 95.
    Nissinen AI, Haapalainen M, Jauhiainen L, Lindman M, Pirhonen M. 2014. Different symptoms in carrots caused by male and female carrot psyllid feeding and infection by “Candidatus Liberibacter solanacearum. .” Plant Pathol. 63:4812–20
     [Google Scholar]
  97. 96.
    Nokkala C, Kuznetsova VG, Rinne V, Nokkala S. 2019. Description of two new species of the genus Cacopsylla Ossiannilsson, 1970 (Hemiptera, Psylloidea) from northern Fennoscandia recognized by morphology, cytogenetic characters and COI barcode sequence. Comp. Cytogenet. 13:4367–82
     [Google Scholar]
  98. 97.
    Nováková E, Hypsa V, Moran NA. 2009. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 9:143
     [Google Scholar]
  99. 98.
    Ouvrard D, Burckhardt D, Azar D, Grimaldi D. 2010. Non-jumping plant-lice in Cretaceous amber (Hemiptera: Sternorrhyncha: Psylloidea). Syst. Entomol. 35:1172–80
     [Google Scholar]
  100. 99.
    Ouvrard D, Chalise P, Percy DM. 2015. Host-plant leaps versus host-plant shuffle: a global survey reveals contrasting patterns in an oligophagous insect group (Hemiptera, Psylloidea). Syst. Biodivers. 13:5434–54
     [Google Scholar]
  101. 100.
    Ouvrard D, Roskov Y, Ower G, Orrell T, Nicolson D et al. 2019. Species 2000 & ITIS Catalogue of Life, 2019 Annual Checklist Rep. Species 2000 Reading, UK:
  102. 101.
    Paris TM, Allan SA, Udell BJ, Stansly PA. 2017. Evidence of behavior-based utilization by the Asian citrus psyllid of a combination of UV and green or yellow wavelengths. PLOS ONE 12:12e0189228
     [Google Scholar]
  103. 102.
    Patt JM, Meikle WG, Mafra-Neto A, Sétamou M, Mangan R et al. 2011. Multimodal cues drive host-plant assessment in Asian citrus psyllid (Diaphorina citri). Environ. Entomol. 40:61494–502
     [Google Scholar]
  104. 103.
    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). Ann. Entomol. Soc. Am. 109:3371–76
     [Google Scholar]
  105. 104.
    Percy DM. 2003. Radiation, diversity, and host-plant interactions among island and continental legume-feeding psyllids. Evolution 57:112540–56
     [Google Scholar]
  106. 105.
    Percy DM. 2017. Making the most of your host: the Metrosideros-feeding psyllids (Hemiptera, Psylloidea) of the Hawaiian Islands. ZooKeys 649:1–163
     [Google Scholar]
  107. 106.
    Percy DM, Crampton-Platt A, Sveinsson S, Lemmon AR, Lemmon EM et al. 2018. Resolving the psyllid tree of life: phylogenomic analyses of the superfamily Psylloidea (Hemiptera). Syst. Entomol. 43:4762–76
     [Google Scholar]
  108. 107.
    Percy DM, Cronk QCB. 2022. Psyllid honeydew as a Bombus food source in the boreal landscape. Ecol. Entomol. 47:4713–18
     [Google Scholar]
  109. 108.
    Percy DM, Page RDM, Cronk QCB. 2004. Plant-insect interactions: Double-dating associated insect and plant lineages reveals asynchronous radiations. Syst. Biol. 53:1120–27
     [Google Scholar]
  110. 109.
    Pierre MO, Salvatierra-Miranda J, Rivera MJ, Etxeberria E, Gonzalez P, Vincent CI. 2021. White and red-dyed kaolin particle films reduce Asian citrus psyllid populations, delay huanglongbing infection, and increase citrus growth. Crop Prot. 150:105792
     [Google Scholar]
  111. 110.
    Raddadi N, Gonella E, Camerota C, Pizzinat A, Tedeschi R 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. Environ. Microbiol. 13:2414–26
     [Google Scholar]
  112. 111.
    Ramsey JS, Ammar E-D, Mahoney J, Rivera K, Johnson R et al. 2021. Host plant adaptation drives changes in Diaphorina citri proteome regulation, proteoform expression and transmission of Candidatus Liberibacter asiaticus, the citrus greening pathogen. Phytopathology 112:101–15
     [Google Scholar]
  113. 112.
    Raven PH, Miller SE. 2020. Here today, gone tomorrow. Science 370:6513149
     [Google Scholar]
  114. 113.
    Ren S-L, Li Y-H, Ou D, Guo Y-J, Qureshi JA et al. 2018. Localization and dynamics of Wolbachia infection in Asian citrus psyllid Diaphorina citri, the insect vector of the causal pathogens of Huanglongbing. Microbiologyopen 7:3e00561
     [Google Scholar]
  115. 114.
    Reyes Caldas PA, Zhu J, Breakspear A, Thapa SP, Toruño TY et al. 2022. Effectors from a bacterial vector-borne pathogen exhibit diverse subcellular localization, expression profiles and manipulation of plant defense. Mol. Plant Microbe Interact. 35:1067–80
     [Google Scholar]
  116. 115.
    Sengoda VG, Munyaneza JE, Crosslin JM, Buchman JL, Pappu HR. 2010. Phenotypic and etiological differences between psyllid yellows and zebra chip diseases of potato. Am. J. Potato Res. 87:141–49
     [Google Scholar]
  117. 116.
    Sharma A, Raman A. 2022. Gall-inducing Psylloidea (Insecta: Hemiptera)-plant interactions. J. Plant Interact. 17:1580–94
     [Google Scholar]
  118. 117.
    Sharma A, Raman A, Taylor GS, Fletcher MJ, Nicol H. 2015. Bionomics and feeding impact of Ctenarytaina eucalypti (Hemiptera: Psylloidea: Aphalaridae) on Eucalyptus globulus (Myrtaceae) in the central tablelands of New South Wales. Aust. Entomol. 54:2159–71
     [Google Scholar]
  119. 118.
    Siewert C, Luge T, Duduk B, Seemüller E, Büttner C et al. 2014. Analysis of expressed genes of the bacterium “Candidatus phytoplasma Mali” highlights key features of virulence and metabolism. PLOS ONE 9:4e94391
     [Google Scholar]
  120. 119.
    Sloan DB, Moran NA. 2012. Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol. Biol. Evol. 29:123781–92
     [Google Scholar]
  121. 120.
    Sloan DB, Nakabachi A, Richards S, Qu J, Murali SC et al. 2014. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol. Biol. Evol. 31:4857–71
     [Google Scholar]
  122. 121.
    Smith JM, Horton BM, Haslem A, Steinbauer MJ. 2021. The functional roles of psyllid abundance and assemblage on bird-associated forest defoliation. Oecologia 197:1201–11
     [Google Scholar]
  123. 122.
    Soroker V, Talebaev S, Harari AR, Wesley SD. 2004. The role of chemical cues in host and mate location in the pear psylla Cacopsylla bidens (Homoptera: Psyllidae). J. Insect Behav. 17:5613–26
     [Google Scholar]
  124. 123.
    Spaulding AW, von Dohlen CD. 1998. Phylogenetic characterization and molecular evolution of bacterial endosymbionts in psyllids (Hemiptera: Sternorrhyncha). Mol. Biol. Evol. 15:111506–13
     [Google Scholar]
  125. 124.
    Steinbauer MJ. 2013. Shoot feeding as a nutrient acquisition strategy in free-living psylloids. PLOS ONE 8:10e77990
     [Google Scholar]
  126. 125.
    Steinbauer MJ, Burns AE, Hall A, Riegler M, Taylor GS. 2014. Nutritional enhancement of leaves by a psyllid through senescence-like processes: insect manipulation or plant defence?. Oecologia 176:41061–74
     [Google Scholar]
  127. 126.
    Steinbauer MJ, Farnier K, Taylor GS, Salminen J-P. 2016. Effects of eucalypt nutritional quality on the Bog gum-Victorian metapopulation of Ctenarytaina bipartita and implications for host and range expansion. Ecol. Entomol. 41:2211–25
     [Google Scholar]
  128. 127.
    Stockton DG, Martini X, Patt JM, Stelinski LL. 2016. The influence of learning on host plant preference in a significant phytopathogen vector, Diaphorina citri. PLOS ONE 11:3e0149815
     [Google Scholar]
  129. 128.
    Stukenberg N, Poehling H-M. 2019. Blue-green opponency and trichromatic vision in the greenhouse whitefly (Trialeurodes vaporariorum) explored using light emitting diodes. Ann. Appl. Biol. 175:2146–63
     [Google Scholar]
  130. 129.
    Subandiyah S, Nikoh N, Tsuyumu S, Somowiyarjo S, Fukatsu T. 2000. Complex endosymbiotic microbiota of the citrus psyllid Diaphorina citri (Homoptera: Psylloidea). Zoolog. Sci. 17:7983–89
     [Google Scholar]
  131. 130.
    Sumner-Kalkun JC, Highet F, Arnsdorf YM, Back E, Carnegie M et al. 2020.. “ Candidatus Liberibacter solanacearum” distribution and diversity in Scotland and the characterisation of novel haplotypes from Craspedolepta spp. (Psyllidae: Aphalaridae). Sci. Rep. 10:16567
     [Google Scholar]
  132. 131.
    Tamames J, Gil R, Latorre A, Peretó J, Silva FJ, Moya A. 2007. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol. Biol. 7:181
     [Google Scholar]
  133. 132.
    Taylor GS. 1985. The taxonomic status of Schedotrioza multitudinea (Maskell) (Psylloidea: Triozidae) with notes on its biology. Aust. J. Entomol. 24:4305–12
     [Google Scholar]
  134. 133.
    Tedeschi R, Bertaccini A 2019. Transovarial transmission in insect vectors. Phytoplasmas: Plant Pathogenic Bacteria, Vol. II Transmission and Management of Phytoplasma-Associated Diseases A Bertaccini, PG Weintraub, GP Rao, N Mori 115–30. Berlin: Springer
     [Google Scholar]
  135. 134.
    Tedeschi R, Ferrato V, Rossi J, Alma A. 2006. Possible phytoplasma transovarial transmission in the psyllids Cacopsylla melanoneura and Cacopsylla pruni. Plant Pathol. 55:118–24
     [Google Scholar]
  136. 135.
    Teresani G, Hernández E, Bertolini E, Siverio F, Marroquín C et al. 2015. Search for potential vectors of “Candidatus Liberibacter solanacearum”: population dynamics in host crops. Span. J. Agric. Res. 13:11002
     [Google Scholar]
  137. 136.
    Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. 2000. Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl. Environ. Microbiol. 66:72898–905
     [Google Scholar]
  138. 137.
    Thapa SP, De Francesco A, Trinh J, Gurung FB, Pang Z et al. 2020. Genome-wide analyses of Liberi-bacter species provides insights into evolution, phylogenetic relationships, and virulence factors. Mol. Plant Pathol. 21:5716–31
     [Google Scholar]
  139. 138.
    Thinakaran J, Pierson EA, Longnecker M, Tamborindeguy C, Munyaneza JE et al. 2015. Settling and ovipositional behavior of Bactericera cockerelli (Hemiptera: Triozidae) on solanaceous hosts under field and laboratory conditions. J. Econ. Entomol. 108:3904–16
     [Google Scholar]
  140. 139.
    Valterová I, Nehlin G, Borg-Karlson A-K. 1997. Host plant chemistry and preferences in egg-laying Trioza apicalis (Homoptera, Psylloidea). Biochem. Syst. Ecol. 25:6477–91
     [Google Scholar]
  141. 140.
    Volpe HXL, Zanardi OZ, Magnani RF, Luvizotto RAG, Esperança V et al. 2020. Behavioral responses of Diaphorina citri to host plant volatiles in multiple-choice olfactometers are affected in interpretable ways by effects of background colors and airflows. PLOS ONE 15:7e0235630
     [Google Scholar]
  142. 141.
    Weil T, Ometto L, Esteve-Codina A, Gómez-Garrido J, Oppedisano T et al. 2020. Linking omics and ecology to dissect interactions between the apple proliferation phytoplasma and its psyllid vector Cacopsylla melanoneura. Insect Biochem. Mol. Biol. 127:103474
     [Google Scholar]
  143. 142.
    Wenninger EJ, Stelinski LL, Hall DG. 2008. Behavioral evidence for a female-produced sex attractant in Diaphorina citri. Entomol. Exp. Appl. 128:3450–59
     [Google Scholar]
  144. 143.
    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. Environ. Entomol. 38:1225–34
     [Google Scholar]
  145. 144.
    White TCR. 2015. Senescence-feeders: a new trophic sub-guild of insect herbivores. J. Appl. Entomol. 139:1–211–22
     [Google Scholar]
  146. 145.
    Wu Z-Z, Qu M-Q, Chen M-S, Lin J-T. 2021. Proteomic and transcriptomic analyses of saliva and salivary glands from the Asian citrus psyllid, Diaphorina citri. J. Proteom. 238:104136
     [Google Scholar]
  147. 146.
    Yamada T, Hamada M, Floreancig P, Nakabachi A. 2019. Diaphorin, a polyketide synthesized by an intracellular symbiont of the Asian citrus psyllid, is potentially harmful for biological control agents. PLOS ONE 14:5e0216319
     [Google Scholar]
  148. 147.
    Yang M-M, Raman A. 2007. Diversity, richness, and patterns of radiation among gall-inducing psyllids (Hemiptera: Psylloidea) in the Orient and Eastern Palearctic. Orient. Insects 41:155–65
     [Google Scholar]
  149. 148.
    Yen AL. 2002. Short-range endemism and Australian Psylloidea (Insecta: Hemiptera) in the genera Glycaspis and Acizzia (Psyllidae). Invertebr. Syst. 16:4631–39
     [Google Scholar]
  150. 149.
    Yu X, Killiny N. 2018. The secreted salivary proteome of Asian citrus psyllid Diaphorina citri. Physiol. Entomol. 43:4324–33
     [Google Scholar]
  151. 150.
    Yuvaraj JK, Andersson MN, Steinbauer MJ, Farnier K, Anderbrant O. 2013. Specificity and sensitivity of plant odor-detecting olfactory sensory neurons in Ctenarytaina eucalypti (Sternorrhyncha: Psyllidae). J. Insect Physiol. 59:5542–51
     [Google Scholar]
  152. 151.
    Zanardi OZ, Volpe HXL, Favaris AP, Silva WD, Luvizotto RAG et al. 2018. Putative sex pheromone of the Asian citrus psyllid, Diaphorina citri, breaks down into an attractant. Sci. Rep. 8:455
     [Google Scholar]
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The Hidden Secrets of Psylloidea: Biology, Behavior, Symbionts, and Ecology
Annual Review of Entomology 69, 277 (2024); https://doi.org/10.1146/annurev-ento-120120-114738
/content/journals/10.1146/annurev-ento-120120-114738
/content/journals/10.1146/annurev-ento-120120-114738
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