Journal of Pest Science

, Volume 90, Issue 1, pp 51–68 | Cite as

Use the insiders: could insect facultative symbionts control vector-borne plant diseases?

  • Julien Chuche
  • Nathalie Auricau-Bouvery
  • Jean-Luc Danet
  • Denis Thiéry


Insect vector-borne plant diseases, particularly those whose causative agents are viral, or phloem- and xylem-restricted bacteria, greatly impact crop losses. Since plants are immobile, the epidemiology of vector-borne diseases greatly depends on insect vectors, which are the only means of dissemination for many pathogens. The effectiveness of a vector-borne pathogen relies upon the vectorial capacity, which is affected by vector density, feeding activity on hosts, longevity before and after pathogen ingestion, duration of the incubation period, and vector competence. During the last decade, research on human vector-borne epidemics has stimulated interest in novel control strategies targeting different parts of the vector cycle, and our purpose here is to draw parallels between this field of research and agronomy. We review the literature on insect vectors of crop diseases and their symbiotic microorganisms with the aim of suggesting future integrated management techniques based on current research on insect-vectored human diseases. Vector transmission is a complex process and different modes of transmission are encountered irrespective of the pathogen. Facultative symbionts have varied effects on life history traits that could be used for vector population control. Symbiont selection, transformation, and their manner of dissemination are important when developing an integrated vector management system based on symbiont manipulation. In the short term, progress on our knowledge of the microflora of insect vectors of plant diseases must be made. In the long term, symbiont manipulation, which has been successfully demonstrated against human insect-vectored diseases, could be adapted to insect-borne plant diseases to increase sustainable crop production.


Symbiont Vector-borne disease Insect Hemiptera Integrated pest management 



First author was funded by French ‘casdar’ research project EchoStol. First and last author’s lab participates in the Labex COTE research project.


  1. Ahmed MZ, Li SJ, Xue X, Yin XJ, Ren SX, Jiggins FM, Greeff JM, Qiu BL (2015) The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission. PLoS Pathog 11:19. doi: 10.1371/journal.ppat.1004672 CrossRefGoogle Scholar
  2. Aksoy S (2003) Control of tsetse flies and trypanosomes using molecular genetics. Vet Parasitol 115:125–145. doi: 10.1016/s0304-4017(03)00203-6 PubMedCrossRefGoogle Scholar
  3. Almeida RPP, Purcell AH (2006) Patterns of Xylella fastidiosa colonization on the precibarium of sharpshooter vectors relative to transmission to plants. Ann Entomol Soc Am 99:884–890. doi: 10.1603/0013-8746(2006)99[884:POXFCO]2.0.CO;2 CrossRefGoogle Scholar
  4. Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE (2010) Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS One 5:e11339. doi: 10.1371/journal.pone.0011339 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189. doi: 10.1146/annurev.micro.59.030804.121041 PubMedCrossRefGoogle Scholar
  6. Beard CB, Cordon-Rosales C, Durvasula RV (2002) Bacterial symbionts of the triatominae and their potential use in control of Chagas disease transmission. Annu Rev Entomol 47:123–141. doi: 10.1146/annurev.ento.47.091201.145144 PubMedCrossRefGoogle Scholar
  7. Bextine B, Lauzon C, Potter S, Lampe D, Miller TA (2004) Delivery of a genetically marked Alcaligenes sp. to the glassy-winged sharpshooter for use in a paratransgenic control strategy. Curr Microbiol 48:327–331. doi: 10.1007/s00284-003-4178-2 PubMedCrossRefGoogle Scholar
  8. Bextine B, Lampe D, Lauzon C, Jackson B, Miller T (2005) Establishment of a genetically marked insect-derived symbiont in multiple host plants. Curr Microbiol 50:1–7. doi: 10.1007/s00284-004-4390-8 PubMedCrossRefGoogle Scholar
  9. Bing XL, Yang J, Zchori-Fein E, Wang XW, Liu SS (2013) Characterization of a newly discovered symbiont in the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl Environ Microbiol 79:569–575. doi: 10.1128/AEM.03030-12 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Boivin G, Hance T, Brodeur J (2012) Aphid parasitoids in biological control. Can J Plant Sci 92:1–12. doi: 10.4141/cjps2011-045 CrossRefGoogle Scholar
  11. Bosque-Pérez NA (2000) Eight decades of maize streak virus research. Virus Res 71:107–121. doi: 10.1016/s0168-1702(00)00192-1 PubMedCrossRefGoogle Scholar
  12. Bové JM, Garnier M (2002) Phloem-and xylem-restricted plant pathogenic bacteria. Plant Sci 163:1083–1098. doi: 10.1016/S0168-9452(03)00033-5 CrossRefGoogle Scholar
  13. Bressan A (2014) Emergence and evolution of Arsenophonus bacteria as insect-vectored plant pathogens. Infect Genet Evol 22:81–90. doi: 10.1016/j.meegid.2014.01.004 PubMedCrossRefGoogle Scholar
  14. Bricault CA, Perry KL (2013) Alteration of intersubunit acid–base pair interactions at the quasi-threefold axis of symmetry of Cucumber mosaic virus disrupts aphid vector transmission. Virology 440:160–170. doi: 10.1016/j.virol.2013.02.020 PubMedCrossRefGoogle Scholar
  15. Briddon RW, Markham PG (2000) Cotton leaf curl virus disease. Virus Res 71:151–159. doi: 10.1016/S0168-1702(00)00195-7 PubMedCrossRefGoogle Scholar
  16. Broderick NA, Raffa KF, Handelsman J (2006) Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc Natl Acad Sci USA 103:15196–15199. doi: 10.1073/pnas.0604865103 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66. doi: 10.1111/j.1744-7917.2010.01396.x CrossRefGoogle Scholar
  18. Buchner P (1965) Endosymbiosis of animals with plant microorganisms. Wiley, New YorkGoogle Scholar
  19. Caljon G, De Vooght L, Van den Abbeele J (2013) Options for the delivery of anti-pathogen molecules in arthropod vectors. J Invertebr Pathol 112:S75–S82. doi: 10.1016/j.jip.2012.07.013 PubMedCrossRefGoogle Scholar
  20. Carson R (1962) Silent Spring. Houghton Mifflin Co, BostonGoogle Scholar
  21. Carter W (1973) Insects in relation to plant disease. Wiley, New YorkGoogle Scholar
  22. Carter V, Underhill A, Baber I, Sylla L, Baby M, Larget-Thiery I, Zettor A, Bourgouin C, Langel U, Faye I, Otvos L, Wade JD, Coulibaly MB, Traore SF, Tripet F, Eggleston P, Hurd H (2013) Killer bee molecules: antimicrobial peptides as effector molecules to target sporogonic stages of Plasmodium. PLoS Pathog. doi: 10.1371/journal.ppat.1003790 PubMedPubMedCentralGoogle Scholar
  23. Caspi-Fluger A, Zchori-Fein E (2010) Do plants and insects share the same symbionts? Isr J Plant Sci 58:113–119. doi: 10.1560/ijps.58.2.113 CrossRefGoogle Scholar
  24. Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, Belausov E, Hunter MS, Zchori-Fein E (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc R Soc Biol Sci Ser B 279:1791–1796. doi: 10.1098/rspb.2011.2095 CrossRefGoogle Scholar
  25. Casteel CL, Hansen AK, Walling LL, Paine TD (2012) Manipulation of plant defense responses by the tomato psyllid (Bactericera cockerelli) and its associated endosymbiont Candidatus Liberibacter psyllaurous. PLoS One 7:e35191. doi: 10.1371/journal.pone.0035191 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chatterjee S, Almeida RPP, Lindow S (2008) Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu Rev Phytopathol 46:243–271. doi: 10.1146/annurev.phyto.45.062806.094342 PubMedCrossRefGoogle Scholar
  27. Chen DQ, Montllor CB, Purcell AH (2000) Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol Exp Appl 95:315–323. doi: 10.1046/j.1570-7458.2000.00670.x CrossRefGoogle Scholar
  28. Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, Inbar M, Ghanim M (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97:407–413. doi: 10.1017/s0007485307005159 PubMedCrossRefGoogle Scholar
  29. Chouaia B, Rossi P, Epis S, Mosca M, Ricci I, Damiani C, Ulissi U, Crotti E, Daffonchio D, Bandi C, Favia G (2012) Delayed larval development in Anopheles mosquitoes deprived of Asaia bacterial symbionts. BMC Microbiol 12:S2. doi: 10.1186/1471-2180-12-s1-s2 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet 9:22. doi: 10.1371/journal.pgen.1003896 CrossRefGoogle Scholar
  31. Chuche J, Thiéry D (2014) Biology and ecology of the Flavescence dorée vector Scaphoideus titanus: a review. Agron Sustain Dev 34:381–403. doi: 10.1007/s13593-014-0208-7 CrossRefGoogle Scholar
  32. Coats JR (1994) Risks from natural versus synthetic insecticides. Ann Rev Entomol 39:489–515. doi: 10.1146/annurev.en.39.010194.002421 CrossRefGoogle Scholar
  33. Conord C, Despres L, Vallier A, Balmand S, Miquel C, Zundel S, Lemperiere G, Heddi A (2008) Long-term evolutionary stability of bacterial endosymbiosis in curculionoidea: additional evidence of symbiont replacement in the dryophthoridae family. Mol Biol Evol 25:859–868. doi: 10.1093/molbev/msn027 PubMedCrossRefGoogle Scholar
  34. Cook PE, McMeniman CJ, O’Neill SL (2008) Modifying insect population age structure to control vector-borne disease. In: Aksoy S (ed) Transgenesis and the management of vector-borne disease, vol 627., Advances in experimental medicine and biologySpringer, New York, pp 126–140. doi: 10.1007/978-0-387-78225-6_11 CrossRefGoogle Scholar
  35. Costa AS (1976) Whitefly-transmitted plant diseases. Annu Rev Phytopathol 14:429–449. doi: 10.1146/ CrossRefGoogle Scholar
  36. Croft BA, Brown AWA (1975) Responses of arthropod natural enemies to insecticides. Ann Rev Entomol 20:285–335. doi: 10.1146/annurev.en.20.010175.001441 CrossRefGoogle Scholar
  37. Crotti E, Damiani C, Pajoro M, Gonella E, Rizzi A, Ricci I, Negri I, Scuppa P, Rossi P, Ballarini P, Raddadi N, Marzorati M, Sacchi L, Clementi E, Genchi M, Mandrioli M, Bandi C, Favia G, Alma A, Daffonchio D (2009) Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ Microbiol 11:3252–3264. doi: 10.1111/j.1462-2920.2009.02048.x PubMedCrossRefGoogle Scholar
  38. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, Alma A, Sacchi L, Bourtzis K, Mandrioli M, Cherif A, Bandi C, Daffonchio D (2010) Acetic acid bacteria, newly emerging symbionts of insects. Appl Environ Microbiol 76:6963–6970. doi: 10.1128/aem.01336-10 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Czosnek H, Laterrot H (1997) A worldwide survey of tomato yellow leaf curl viruses. Arch Virol 142:1391–1406. doi: 10.1007/s007050050168 PubMedCrossRefGoogle Scholar
  40. Dale C, Beeton M, Harbison C, Jones T, Pontes M (2006) Isolation, pure culture, and characterization of “Candidatus Arsenophonus arthropodicus,” an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol 72:2997–3004. doi: 10.1128/aem.72.4.2997-3004.2006 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Darby AC, Douglas AE (2003) Elucidation of the transmission patterns of an insect-borne bacterium. Appl Environ Microbiol 69:4403–4407. doi: 10.1128/AEM.69.8.4403-4407.2003 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Darby AC, Chandler SM, Welburn SC, Douglas AE (2005) Aphid-symbiotic bacteria cultured in insect cell lines. Appl Environ Microbiol 71:4833–4839. doi: 10.1128/aem.71.8.4833-4839.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Daugherty MP, Lopes JRS, Almeida RPP (2010) Vector within-host feeding preference mediates transmission of a heterogeneously distributed pathogen. Ecol Entomol 35:350–366. doi: 10.1111/j.1365-2311.2010.01189.x CrossRefGoogle Scholar
  44. De Clerck C, Tsuchida T, Massart S, Lepoivre P, Francis F, Jijakli MH (2014) Combination of genomic and proteomic approaches to characterize the symbiotic population of the banana aphid (Hemiptera: Aphididae). Environ Entomol 43:29–36. doi: 10.1603/en13107 PubMedCrossRefGoogle Scholar
  45. della Torre A, Costantini C, Besansky NJ, Caccone A, Petrarca V, Powell JR, Coluzzi M (2002) Speciation within Anopheles gambiae: the glass is half full. Science 298:115–117. doi: 10.1126/science.1078170 PubMedCrossRefGoogle Scholar
  46. Denholm I, Rowland MW (1992) Tactics for managing pesticide resistance in arthropods: theory and practice. Ann Rev Entomol 37:91–112. doi: 10.1146/annurev.en.37.010192.000515 CrossRefGoogle Scholar
  47. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Ann Rev Entomol 52:81–106. doi: 10.1146/annurev.ento.52.110405.091440 CrossRefGoogle Scholar
  48. Dheilly NM, Poulin R, Thomas F (2015) Biological warfare: microorganisms as drivers of host-parasite interactions. Infect Genet Evol. doi: 10.1016/j.meegid.2015.05.027 PubMedGoogle Scholar
  49. Dowd PF, Shen SK (1990) The contribution of symbiotic yeast to toxin resistance of the cigarette beetle (Lasioderma serricorne). Entomol Exp Appl 56:241–248. doi: 10.1111/j.1570-7458.1990.tb01402.x CrossRefGoogle Scholar
  50. Dunning Hotopp JC, Clark ME, Oliveira DCSG, Foster JM, Fischer P, Munoz Torres MC, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756. doi: 10.1126/science.1142490 PubMedCrossRefGoogle Scholar
  51. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GD (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27. doi: 10.1186/1741-7007-6-27 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Durvasula RV, Sundaram R, Beard CB (2003) Rhodnius prolixus and its symbiont, Rhodococcus rhodnii, a model for paratransgenic control of disease transmission. In: Bourtzis K, Miller TA (eds) Insect Symbiosis. CRC Press, Boca Raton, pp 85–97Google Scholar
  53. Elbaz A, Clavel J, Rathouz PJ, Moisan F, Galanaud JP, Delemotte B, Alperovitch A, Tzourio C (2009) Professional exposure to pesticides and parkinson disease. Ann Neurol 66:494–504. doi: 10.1002/ana.21717 PubMedCrossRefGoogle Scholar
  54. Engelstadter J, Hurst GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149. doi: 10.1146/annurev.ecolsys.110308.120206 CrossRefGoogle Scholar
  55. Everett KDE, Thao ML, Horn M, Dyszynski GE, Baumann P (2005) Novel chlamydiae in whiteflies and scale insects: endosymbionts ‘Candidatus Fritschea bemisiae’ strain Falk and ‘Candidatus Fritschea eriococci’ strain Elm. Int J Syst Evol Microbiol 55:1581–1587. doi: 10.1099/ijs.0.63454-0 PubMedCrossRefGoogle Scholar
  56. Ferrari J, Muller CB, Kraaijeveld AR, Godfray HCJ (2001) Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55:1805–1814. doi: 10.1554/0014-3820(2001)055[1805:CVACIA]2.0.CO;2 PubMedCrossRefGoogle Scholar
  57. Ferrari J, Darby AC, Daniell TJ, Godfray HCJ, Douglas AE (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol Entomol 29:60–65. doi: 10.1111/j.1365-2311.2004.00574.x CrossRefGoogle Scholar
  58. Ferrari J, Scarborough CL, Godfray HCJ (2007) Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153:323–329. doi: 10.1007/s00442-007-0730-2 PubMedCrossRefGoogle Scholar
  59. Ferrari J, West JA, Via S, Godfray HCJ (2012) Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66:375–390. doi: 10.1111/j.1558-5646.2011.01436.x PubMedCrossRefGoogle Scholar
  60. Ferrater J, Jong P, Dicke M, Chen Y, Horgan F (2013) Symbiont-mediated adaptation by planthoppers and leafhoppers to resistant rice varieties. Arthropod Plant Interact 7:591–605. doi: 10.1007/s11829-013-9277-9 CrossRefGoogle Scholar
  61. Frantz A, Calcagno V, Mieuzet L, Plantegenest M, Simon J-C (2009) Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation. Biol J Linn Soc 97:718–727. doi: 10.1111/j.1095-8312.2009.01221.x CrossRefGoogle Scholar
  62. Frydman HM, Li JM, Robson DN, Wieschaus E (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441:509–512. doi: 10.1038/nature04756 PubMedCrossRefGoogle Scholar
  63. Fuente LDL, Burr TJ, Hoch HC (2007) Mutations in type I and type IV pilus biosynthetic genes affect twitching motility rates in Xylella fastidiosa. J Bacteriol 189:7507–7510. doi: 10.1128/jb.00934-07 CrossRefGoogle Scholar
  64. Garnier M, Foissac X, Gaurivaud P, Laigret F, Renaudin J, Saillard C, Bové JM (2001) Mycoplasmas, plants, insect vectors: a matrimonial triangle. Cr Acad Sci III-Vie 324:923–928. doi: 10.1016/S0764-4469(01)01372-5 CrossRefGoogle Scholar
  65. Gehrer L, Vorburger C (2012) Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol Lett 8:613–615. doi: 10.1098/rsbl.2012.0144 PubMedPubMedCentralCrossRefGoogle Scholar
  66. Ghanim M (2014) A review of the mechanisms and components that determine the transmission efficiency of Tomato yellow leaf curl virus (Geminiviridae; Begomovirus) by its whitefly vector. Virus Res 186:47–54. doi: 10.1016/j.virusres.2014.01.022 PubMedCrossRefGoogle Scholar
  67. Gherna RL, Werren JH, Weisburg W, Cote R, Woese CR, Mandelco L, Brenner DJ (1991) Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the son-killer trait in the parasitic wasp Nasonia vitripennis. Int J Syst Bacteriol 41:563–565. doi: 10.1099/00207713-41-4-563 CrossRefGoogle Scholar
  68. Gnankiné O, Mouton L, Henri H, Terraz G, Houndeté T, Martin T, Vavre F, Fleury F (2012) Distribution of Bemisia tabaci (Homoptera: Aleyrodidae) biotypes and their associated symbiotic bacteria on host plants in West Africa. Insect Conserv Diver 6:411–421. doi: 10.1111/j.1752-4598.2012.00206.x CrossRefGoogle Scholar
  69. Gonella E, Negri I, Marzorati M, Mandrioli M, Sacchi L, Pajoro M, Crotti E, Rizzi A, Clementi E, Tedeschi R, Bandi C, Alma A, Daffonchio D (2011) Bacterial endosymbiont localization in Hyalesthes obsoletus, the insect vector of Bois Noir in Vitis vinifera. Appl Environ Microbiol 77:1423–1435. doi: 10.1128/aem.02121-10 PubMedCrossRefGoogle Scholar
  70. Gonella E, Crotti E, Rizzi A, Mandrioli M, Favia G, Daffonchio D, Alma A (2012) Horizontal transmission of the symbiotic bacterium Asaia sp. in the leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae). BMC Microbiol 12:S4. doi: 10.1186/1471-2180-12-S1-S4 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Gonella E, Pajoro M, Marzorati M, Crotti E, Mandrioli M, Pontini M, Bulgari D, Negri I, Sacchi L, Chouaia B, Daffonchio D, Alma A (2015) Plant-mediated interspecific horizontal transmission of an intracellular symbiont in insects. Sci Rep 5:15811. doi: 10.1038/srep15811 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N, Kontsedalov S, Gershon M, Gal S, Katzir N, Zchori-Fein E (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol 72:3646–3652. doi: 10.1128/AEM.72.5.3646-3652.2006 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M, Brumin M, Sobol I, Czosnek H, Vavre F, Fleury F, Ghanim M (2010) The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J Virol 84:9310–9317. doi: 10.1128/jvi.00423-10 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Grafton-Cardwell EE, Stelinski LL, Stansly PA (2013) Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens. Ann Rev Entomol 58:413–432. doi: 10.1146/annurev-ento-120811-153542 CrossRefGoogle Scholar
  75. Groot TVM, Breeuwer JAJ (2006) Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species. Exp Appl Acarol 39:257–271. doi: 10.1007/s10493-006-9019-0 PubMedCrossRefGoogle Scholar
  76. Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Ann Rev Entomol 61:43–62. doi: 10.1146/annurev-ento-010715-023646 CrossRefGoogle Scholar
  77. Gueguen G, Vavre F, Gnankiné O, Peterschmitt M, Charif D, Chiel E, Gottlieb Y, Ghanim M, Zchori-Fein E, Fleury F (2010) Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol 19:4365–4378. doi: 10.1111/j.1365-294X.2010.04775.x PubMedCrossRefGoogle Scholar
  78. Haapalainen M (2014) Biology and epidemics of Candidatus Liberibacter species, psyllid-transmitted plant-pathogenic bacteria. Ann Appl Biol 165:172–198. doi: 10.1111/aab.12149 CrossRefGoogle Scholar
  79. Hanboonsong Y, Choosai C, Panyim S, Damak S (2002) Transovarial transmission of sugarcane white leaf phytoplasma in the insect vector Matsumuratettix hiroglyphicus (Matsumura). Insect Mol Biol 11:97–103. doi: 10.1046/j.0962-1075.2001.00314.x PubMedCrossRefGoogle Scholar
  80. Hardman JM, Rogers REL, Nyrop JP, Frisch T (1991) Effect of pesticide applications on abundance of European red mite (Acari: tetranychidae) and Tryphlodromus pyri (Acari: phytoseiidae) in Nova Scotian apple orchards. J Econ Entomol 84:570–580CrossRefGoogle Scholar
  81. Harrison BD (1958) Studies on the behavior of potato leaf roll and other viruses in the body of their aphid vector Myzus persicae (Sulz.). Virology 6:265–277. doi: 10.1016/0042-6822(58)90074-6 PubMedCrossRefGoogle Scholar
  82. Hazarika LK, Bhuyan M, Hazarika BN (2009) Insect pests of tea and their management. Ann Rev Entomol 54:267–284. doi: 10.1146/annurev.ento.53.103106.093359 CrossRefGoogle Scholar
  83. Heddi A, Gross R (2011) Proteobacteria as primary endosymbionts of Arthropods. In: Zchori-Fein E, Bourtzis K (eds) Manipulative tenants, Bacteria associated with Arthropods. CRC Press, Boca Raton, pp 1–27Google Scholar
  84. Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P (1999) Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci USA 96:6814–6819. doi: 10.1073/pnas.96.12.6814 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702. doi: 10.1126/science.1162418 PubMedCrossRefGoogle Scholar
  86. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Ann Rev Entomol 45:371–391. doi: 10.1146/annurev.ento.45.1.371 CrossRefGoogle Scholar
  87. Hibino H (1996) Biology and epidemiology of rice viruses. Annu Rev Phytopathol 34:249–274. doi: 10.1146/annurev.phyto.34.1.249 PubMedCrossRefGoogle Scholar
  88. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?—A statistical analysis of current data. FEMS Microbiol Lett 281:215–220. doi: 10.1111/j.1574-6968.2008.01110.x PubMedPubMedCentralCrossRefGoogle Scholar
  89. Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256. doi: 10.1126/science.1199410 PubMedCrossRefGoogle Scholar
  90. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, Muzzi F, Greenfield M, Durkan M, Leong YS, Dong Y, Cook H, Axford J, Callahan AG, Kenny N, Omodei C, McGraw EA, Ryan PA, Ritchie SA, Turelli M, O’Neill SL (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454–457. doi: 10.1038/nature10356 PubMedCrossRefGoogle Scholar
  91. Hogenhout SA, Ammar E-D, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359. doi: 10.1146/annurev.phyto.022508.092135 PubMedCrossRefGoogle Scholar
  92. Hughes GL, Allsopp PG, Webb RI, Ri Yamada, Iturbe-Ormaetxe I, Brumbley SM, O’Neill SL (2011) Identification of yeast associated with the planthopper, Perkinsiella saccharicida: potential applications for Fiji leaf gall control. Curr Microbiol 63:392–401. doi: 10.1007/s00284-011-9990-5 PubMedCrossRefGoogle Scholar
  93. Huo Y, Liu W, Zhang F, Chen X, Li L, Liu Q, Zhou Y, Wei T, Fang R, Wang X (2014) Transovarial transmission of a plant virus is mediated by vitellogenin of its insect vector. PLoS Pathog. doi: 10.1371/journal.ppat.1003949 PubMedPubMedCentralGoogle Scholar
  94. Hurst GDD, Jiggins FM (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis 6:329–336. doi: 10.3201/eid0604.000402 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Imo M (2013) Host race formation in Hyalesthes obsoletus (Signoret 1865). Johannes Gutenberg-Universität, MainzGoogle Scholar
  96. Jeger MJ, Holt J, Bosch FVD, Madden LV (2004) Epidemiology of insect-transmitted plant viruses: modelling disease dynamics and control interventions. Physiol Entomol 29:291–304. doi: 10.1111/j.0307-6962.2004.00394.x CrossRefGoogle Scholar
  97. Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc R Soc Biol Sci Ser B 277:2311–2319. doi: 10.1098/rspb.2010.0214 CrossRefGoogle Scholar
  98. Kambris Z, Cook PE, Phuc HK, Sinkins SP (2009) Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326:134–136. doi: 10.1126/science.1177531 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Syst 33:641–664. doi: 10.1146/annurev.ecolsys.33.010802.150443 CrossRefGoogle Scholar
  100. Kashima T, Nakamura T, Tojo S (2006) Uric acid recycling in the shield bug, Parastrachia japonensis (Hemiptera: Parastrachiidae), during diapause. J Insect Physiol 52:816–825. doi: 10.1016/j.jinsphys.2006.05.003 PubMedCrossRefGoogle Scholar
  101. Kawakita H, Saiki T, Wei W, Mitsuhashi W, Watanabe K, Sato M (2000) Identification of mulberry dwarf phytoplasmas in the genital organs and eggs of leafhopper Hishimonoides sellatiformis. Phytopathology 90:909–914. doi: 10.1094/PHYTO.2000.90.8.909 PubMedCrossRefGoogle Scholar
  102. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci USA 109:8618–8622. doi: 10.1073/pnas.1200231109 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Larkin P, Kleven S, Banks P (2002) Utilizing Bdv2, the Thinopyrum intermedium source of BYDV resistance, to develop wheat cultivars. In: Henry M, McNab A (eds) Barley yellow dwarf disease: recent advances and future strategies. Proceedings International Symposium Mexico, 1–5 September, 2002 CIMMYT, pp 60–63Google Scholar
  104. Laven H (1967) Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216:383–384. doi: 10.1038/216383a0 PubMedCrossRefGoogle Scholar
  105. Lee IM, Davis RE, Gundersen-Rindal DE (2000) Phytoplasma: Phytopathogenic mollicutes. Annu Rev Microbiol 54:221–255. doi: 10.1146/annurev.micro.54.1.221 PubMedCrossRefGoogle Scholar
  106. Lefèvre C, Charles H, Vallier A, Delobel B, Farrell B, Heddi A (2004) Endosymbiont phylogenesis in the Dryophthoridae weevils: evidence for bacterial replacement. Mol Biol Evol 21:965–973. doi: 10.1093/molbev/msh063 PubMedCrossRefGoogle Scholar
  107. Legg JP, Shirima R, Tajebe LS, Guastella D, Boniface S, Jeremiah S, Nsami E, Chikoti P, Rapisarda C (2014) Biology and management of Bemisia whitefly vectors of cassava virus pandemics in Africa. Pest Manag Sci 70:1446–1453. doi: 10.1002/ps.3793 PubMedCrossRefGoogle Scholar
  108. Leonardo TE (2004) Removal of a specialization-associated symbiont does not affect aphid fitness. Ecol Lett 7:461–468. doi: 10.1111/j.1461-0248.2004.00602.x CrossRefGoogle Scholar
  109. Leonardo TE, Muiru GT (2003) Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc R Soc Biol Sci Ser B 270:S209–S212. doi: 10.1098/rsbl.2003.0064 CrossRefGoogle Scholar
  110. Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G, Verheggen FJ, Francis F, Brostaux Y, Felton GW, Haubruge E (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun 2:348. doi: 10.1038/ncomms1347 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Libbrecht R, Gwynn DM, Fellowes MDE (2007) Aphidius ervi preferentially attacks the green morph of the pea aphid, Acyrthosiphon pisum. J Insect Behav 20:25–32. doi: 10.1007/s10905-006-9055-y CrossRefGoogle Scholar
  112. Losey JE, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388:269–272. doi: 10.1038/40849 CrossRefGoogle Scholar
  113. Lu P, Bian G, Pan X, Xi Z (2012) Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 6:e1754. doi: 10.1371/journal.pntd.0001754 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Łukasik P, van Asch M, Guo H, Ferrari J, Godfray CJ (2013) Unrelated facultative endosymbionts protect aphids against a fungal pathogen. Ecol Lett 16:214–218. doi: 10.1111/ele.12031 PubMedCrossRefGoogle Scholar
  115. Ma WJ, Vavre F, Beukeboom LW (2014) Manipulation of arthropod sex determination by endosymbionts: diversity and molecular mechanisms. Sex Dev 8:59–73. doi: 10.1159/000357024 PubMedCrossRefGoogle Scholar
  116. Maia IG, Haenni A-L, Bernardi F (1996) Potyviral HC-Pro: a multifunctional protein. J Gen Virol 77:1335–1341. doi: 10.1099/0022-1317-77-7-1335 PubMedCrossRefGoogle Scholar
  117. Marzorati M, Alma A, Sacchi L, Pajoro M, Palermo S, Brusetti L, Raddadi N, Balloi A, Tedeschi R, Clementi E, Corona S, Quaglino F, Bianco PA, Beninati T, Bandi C, Daffonchio D (2006) A novel bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of flavescence dorée in Vitis vinifera. Appl Environ Microbiol 72:1467–1475. doi: 10.1128/AEM.72.2.1467-1475.2006 PubMedPubMedCentralCrossRefGoogle Scholar
  118. McGraw EA, O’Neill SL (2013) Beyond insecticides: new thinking on an ancient problem. Nat Rev Microbiol 11:181–193. doi: 10.1038/nrmicro2968 PubMedCrossRefGoogle Scholar
  119. Miller WA, Rasochová L (1997) Barley yellow dwarf viruses. Annu Rev Phytopathol 35:167–190. doi: 10.1146/annurev.phyto.35.1.167 PubMedCrossRefGoogle Scholar
  120. Moll RM, Romoser WS, Modrakowski MC, Moncayo AC, Lerdthusnee K (2001) Meconial peritrophic membranes and the fate of midgut bacteria during mosquito (Diptera: Culicidae) metamorphosis. J Med Entomol 38:29–32. doi: 10.1603/0022-2585-38.1.29 PubMedCrossRefGoogle Scholar
  121. Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195. doi: 10.1046/j.1365-2311.2002.00393.x CrossRefGoogle Scholar
  122. Moran NA (2006) Symbiosis. Curr Biol 16:R866–871. doi: 10.1016/j.cub.2006.09.019 PubMedCrossRefGoogle Scholar
  123. Moran NA, Dunbar HE (2006) Sexual acquisition of beneficial symbionts in aphids. Proc Natl Acad Sci USA 103:12803–12806. doi: 10.1073/pnas.0605772103 PubMedPubMedCentralCrossRefGoogle Scholar
  124. Moran NA, Degnan PH, Santos SR, Dunbar HE, Ochman H (2005) The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA 102:16919–16926. doi: 10.1073/pnas.0507029102 PubMedPubMedCentralCrossRefGoogle Scholar
  125. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190. doi: 10.1146/annurev.genet.41.110306.130119 PubMedCrossRefGoogle Scholar
  126. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, van den Hurk AF, Ryan PA, O’Neill SL (2009) A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139:1268–1278. doi: 10.1016/j.cell.2009.11.042 PubMedCrossRefGoogle Scholar
  127. Murdock CC, Blanford S, Hughes GL, Rasgon JL, Thomas MB (2014) Temperature alters Plasmodium blocking by Wolbachia. Sci Rep. doi: 10.1038/srep03932 PubMedPubMedCentralGoogle Scholar
  128. Nault LR (1997) Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Am 90:522–541. doi: 10.1093/aesa/90.5.521 CrossRefGoogle Scholar
  129. O’Connor L, Plichart C, Sang AC, Brelsfoard CL, Bossin HC, Dobson SL (2012) Open release of male mosquitoes infected with a Wolbachia biopesticide: field performance and infection containment. PLoS Negl Trop Dis 6:e1797. doi: 10.1371/journal.pntd.0001797 PubMedPubMedCentralCrossRefGoogle Scholar
  130. Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43. doi: 10.1017/s0021859605005708 CrossRefGoogle Scholar
  131. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807. doi: 10.1073/pnas.0335320100 PubMedPubMedCentralCrossRefGoogle Scholar
  132. Oliver KM, Campos J, Moran NA, Hunter MS (2008) Population dynamics of defensive symbionts in aphids. Proc R Soc Biol Sci Ser B 275:293–299. doi: 10.1098/rspb.2007.1192 CrossRefGoogle Scholar
  133. Oliver KM, Degnan PH, Hunter MS, Moran NA (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325:992–994. doi: 10.1126/science.1174463 PubMedCrossRefGoogle Scholar
  134. Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Ann Rev Entomol 55:247–266. doi: 10.1146/annurev-ento-112408-085305 CrossRefGoogle Scholar
  135. Ordon F, Habekuss A, Kastirr U, Rabenstein F, Kühne T (2009) Virus resistance in cereals: sources of resistance, genetics and breeding. J Phytopathol 157:535–545. doi: 10.1111/j.1439-0434.2009.01540.x CrossRefGoogle Scholar
  136. Pannebakker BA, Pijnacker LP, Zwaan BJ, Beukeboom LW (2004) Cytology of Wolbachia-induced parthenogenesis in Leptopilina clavipes (Hymenoptera: Figitidae). Genome 47:299–303. doi: 10.1139/G03-137 PubMedCrossRefGoogle Scholar
  137. Patil CD, Borase HP, Salunke BK, Patil SV (2013) Alteration in Bacillus thuringiensis toxicity by curing gut flora: novel approach for mosquito resistance management. Parasitol Res 112:3283–3288. doi: 10.1007/s00436-013-3507-z PubMedCrossRefGoogle Scholar
  138. Pérez-Brocal V, Gil R, Ramos S, Lamelas A, Postigo M, Michelena JM, Silva FJ, Moya A, Latorre A (2006) A small microbial genome: the end of a long symbiotic relationship? Science 314:312–313. doi: 10.1126/science.1130441 PubMedCrossRefGoogle Scholar
  139. Perlman SJ, Hunter MS, Zchori-Fein E (2006) The emerging diversity of Rickettsia. Proc R Soc Biol Sci Ser B 273:2097–2106. doi: 10.1098/rspb.2006.3541 CrossRefGoogle Scholar
  140. Polin S, Le Gallic J-Fo, Simon J-C, Tsuchida T, Outreman Y (2015) Conditional reduction of predation risk associated with a facultative symbiont in an insect. PLoS One 10:e0143728. doi: 10.1371/journal.pone.0143728
  141. Pontes MH, Dale C (2006) Culture and manipulation of insect facultative symbionts. Trends Microbiol 14:406–412. doi: 10.1016/j.tim.2006.07.004 PubMedCrossRefGoogle Scholar
  142. Powles SB (2008) Evolved glyphosate-resistant weeds around the world: lessons to be learnt. Pest Manag Sci 64:360–365. doi: 10.1002/ps.1525 PubMedCrossRefGoogle Scholar
  143. Purcell AH (1979) Evidence for noncirculative transmission of Pierce’s disease bacterium by sharpshooter leafhoppers. Phytopathology. doi: 10.1094/Phyto-69-393 Google Scholar
  144. Quenouille J, Vassilakos N, Moury B (2013) Potato virus Y: a major crop pathogen that has provided major insights into the evolution of viral pathogenicity. Mol Plant Pathol 14:439–452. doi: 10.1111/mpp.12024 PubMedCrossRefGoogle Scholar
  145. Rana VS, Singh ST, Priya NG, Kumar J, Rajagopal R (2012) Arsenophonus GroEL interacts with CLCuV and is localized in midgut and salivary gland of whitefly B. tabaci. PLoS One 7:e42168. doi: 10.1371/journal.pone.0042168 PubMedPubMedCentralCrossRefGoogle Scholar
  146. Rancès E, Ye YH, Woolfit M, McGraw EA, O’Neill SL (2012) The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 8:e1002548. doi: 10.1371/journal.ppat.1002548 PubMedPubMedCentralCrossRefGoogle Scholar
  147. Rasgon JL, Scott TW (2004) Impact of population age structure on Wolbachia transgene driver efficacy: ecologically complex factors and release of genetically modified mosquitoes. Insect Biochem Mol Biol 34:707–713. doi: 10.1016/j.ibmb.2004.03.023 PubMedCrossRefGoogle Scholar
  148. Riehle MA, Jacobs-Lorena M (2005) Using bacteria to express and display anti-parasite molecules in mosquitoes: current and future strategies. Insect Biochem Mol Biol 35:699–707. doi: 10.1016/j.ibmb.2005.02.008 PubMedCrossRefGoogle Scholar
  149. Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M (1992) Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc R Soc Biol Sci Ser B 250:91–98. doi: 10.1098/rspb.1992.0135 CrossRefGoogle Scholar
  150. Russell JA, Latorre A, Sabater-Munoz B, Moya A, Moran NA (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12:1061–1075. doi: 10.1046/j.1365-294X.2003.01780.x PubMedCrossRefGoogle Scholar
  151. Russell JA, Weldon S, Smith AH, Kim KL, Hu Y, Lukasik P, Doll S, Anastopoulos I, Novin M, Oliver KM (2013) Uncovering symbiont-driven genetic diversity across North American pea aphids. Mol Ecol 22:2045–2059. doi: 10.1111/mec.12211 PubMedCrossRefGoogle Scholar
  152. Sacchi L, Genchi M, Clementi E, Bighardi E, Avanzati AM, Pajoro M, Negri I, Marzorati M, Gonella E, Alma A, Daffonchio D, Bandi C (2008) Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera : Cicadellidae): details of transovarial transmission of Cardinium sp and yeast-like endosymbionts. Tissue Cell 40:231–242. doi: 10.1016/j.tice.2007.12.005 PubMedCrossRefGoogle Scholar
  153. Salar P, Sémétey O, Danet J-L, Boudon-Padieu E, Foissac X (2010) ‘Candidatus Phlomobacter fragariae’ and the proteobacterium associated with the low sugar content syndrome of sugar beet are related to bacteria of the arsenophonus clade detected in hemipteran insects. Eur J Plant Pathol 126:123–127. doi: 10.1007/s10658-009-9520-5 CrossRefGoogle Scholar
  154. Salar P, Charenton C, Foissac X, Malembic-Maher S (2013) Multiplication kinetics of Flavescence dorée phytoplasma in broad bean. Effect of phytoplasma strain and temperature. Eur J Plant Pathol 135:371–381. doi: 10.1007/s10658-012-0093-3 CrossRefGoogle Scholar
  155. Sandström JP, Russell JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228. doi: 10.1046/j.1365-294X.2001.01189.x PubMedCrossRefGoogle Scholar
  156. Sasaki T, Kawamura M, Ishikawa H (1996) Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. J Insect Physiol 42:125–129. doi: 10.1016/0022-1910(95)00086-0 CrossRefGoogle Scholar
  157. Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781. doi: 10.1126/science.1120180 PubMedCrossRefGoogle Scholar
  158. Sémétey O, Gatineau F, Bressan A, Boudon-Padieu E (2007) Characterization of a γ-3 proteobacteria responsible for the syndrome “Basses Richesses” of sugar beet transmitted by Pentastiridius sp. (Hemiptera, Cixiidae). Phytopathology 97:72–78. doi: 10.1094/phyto-97-0072 PubMedCrossRefGoogle Scholar
  159. Simon JC, Carre S, Boutin M, Prunier-Leterme N, Sabater-Munoz B, Latorre A, Bournoville R (2003) Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc R Soc Biol Sci Ser B 270:1703–1712. doi: 10.1098/rspb.2003.2430 CrossRefGoogle Scholar
  160. Soto MJ, Gilbertson RL (2003) Distribution and rate of lovement of the Curtovirus Beet mild curly top virus (Family Geminiviridae) in the beet leafhopper. Phytopathology 93:478–484. doi: 10.1094/phyto.2003.93.4.478 PubMedCrossRefGoogle Scholar
  161. Stavrinides J, McCloskey JK, Ochman H (2009) Pea aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae. Appl Environ Microbiol 75:2230–2235. doi: 10.1128/aem.02860-08 PubMedPubMedCentralCrossRefGoogle Scholar
  162. Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102. doi: 10.1146/annurev.micro.53.1.71 PubMedCrossRefGoogle Scholar
  163. Tajebe LS, Guastella D, Cavalieri V, Kelly SE, Hunter MS, Lund OS, Legg JP, Rapisarda C (2015) Diversity of symbiotic bacteria associated with Bemisia tabaci (Homoptera: Aleyrodidae) in cassava mosaic disease pandemic areas of Tanzania. Ann Appl Biol 166:297–310. doi: 10.1111/aab.12183 CrossRefGoogle Scholar
  164. Tedeschi R, Ferrato V, Rossi J, Alma A (2006) Possible phytoplasma transovarial transmission in the psyllids Cacopsylla melanoneura and Cacopsylla pruni. Plant Pathol 55:18–24. doi: 10.1111/j.1365-3059.2005.01292.x CrossRefGoogle Scholar
  165. Thao ML, Clark MA, Baumann L, Brennan EB, Moran NA, Baumann P (2000) Secondary endosymbionts of psyllids have been acquired multiple times. Curr Microbiol 41:300–304. doi: 10.1007/s002840010138 PubMedCrossRefGoogle Scholar
  166. Thierry M, Becker N, Hajri A, Reynaud B, Lett JM, Delatte H (2011) Symbiont diversity and non-random hybridization among indigenous (Ms) and invasive (B) biotypes of Bemisia tabaci. Mol Ecol 20:2172–2187. doi: 10.1111/j.1365-294X.2011.05087.x PubMedCrossRefGoogle Scholar
  167. Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989. doi: 10.1126/science.1094611 PubMedCrossRefGoogle Scholar
  168. Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon J-C, Fukatsu T (2010) Symbiotic bacterium modifies aphid body color. Science 330:1102–1104. doi: 10.1126/science.1195463 PubMedCrossRefGoogle Scholar
  169. Tsuchida T, Koga R, Matsumoto S, Fukatsu T (2011) Interspecific symbiont transfection confers a novel ecological trait to the recipient insect. Biol Lett 7:245–248. doi: 10.1098/rsbl.2010.0699 PubMedCrossRefGoogle Scholar
  170. Turelli M (2010) Cytoplasmic incompatibility in populations with overlapping generations. Evolution 64:232–241. doi: 10.1111/j.1558-5646.2009.00822.x PubMedCrossRefGoogle Scholar
  171. Turley AP, Moreira LA, O’Neill SL, McGraw EA (2009) Wolbachia infection reduces blood-feeding success in the dengue fever mosquito, Aedes aegypti. PLoS Negl Trop Dis 3:e516. doi: 10.1371/journal.pntd.0000516 PubMedPubMedCentralCrossRefGoogle Scholar
  172. van den Berg MA (1990) The citrus psylla, Trioza erytreae (Del Guercio) (Hemiptera: Triozidae): a review. Agric Ecosyst Environ 30:171–194. doi: 10.1016/0167-8809(90)90104-L CrossRefGoogle Scholar
  173. van den Bosch F, Gilligan CA (2008) Models of fungicide resistance dynamics. Annu Rev Phytopathol 46:123–147. doi: 10.1146/annurev.phyto.011108.135838 PubMedCrossRefGoogle Scholar
  174. van den Heuvel JFJM, Hogenhout SA, van der Wilk F (1999) Recognition and receptors in virus transmission by arthropods. Trends Microbiol 7:71–76. doi: 10.1016/s0966-842x(98)01434-6 PubMedCrossRefGoogle Scholar
  175. Vorburger C (2014) The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids. Insect Sci 21:251–264. doi: 10.1111/1744-7917.12067 PubMedGoogle Scholar
  176. Vorburger C, Sandrock C, Gouskov A, Castaneda LE, Ferrari J (2009) Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host–parasitoid interaction. Evolution 63:1439–1450. doi: 10.1111/j.1558-5646.2009.00660.x PubMedCrossRefGoogle Scholar
  177. Vorburger C, Gehrer L, Rodriguez P (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biol Lett 6:109–111. doi: 10.1098/rsbl.2009.0642 PubMedCrossRefGoogle Scholar
  178. Wang Z, Su X-M, Wen J, Jiang L-Y, Qiao G-X (2014) Widespread infection and diverse infection patterns of Wolbachia in Chinese aphids. Insect Sci 21:313–325. doi: 10.1111/1744-7917.12102 PubMedCrossRefGoogle Scholar
  179. Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B 270:1857–1865. doi: 10.1098/rspb.2003.2425 CrossRefGoogle Scholar
  180. Weintraub PG, Beanland L (2006) Insect vectors of phytoplasmas. Ann Rev Entomol 51:91–111. doi: 10.1146/annurev.ento.51.110104.151039 CrossRefGoogle Scholar
  181. Welburn SC, Maudlin I, Ellis DS (1987) In vitro cultivation of rickettsia-like-organisms from Glossina spp. Ann Trop Med Parasitol 81:331–335PubMedCrossRefGoogle Scholar
  182. Weldon SR, Strand MR, Oliver KM (2013) Phage loss and the breakdown of a defensive symbiosis in aphids. Proc R Soc Biol Sci Ser B 280:20122103. doi: 10.1098/rspb.2012.2103
  183. Werren JH (1997) Biology of Wolbachia. Ann Rev Entomol 42:587–609. doi: 10.1146/annurev.ento.42.1.587 CrossRefGoogle Scholar
  184. Whitfield AE, Ullman DE, German TL (2005) Tospovirus-thrips interactions. Annu Rev Phytopathol 43:459–489. doi: 10.1146/annurev.phyto.43.040204.140017 PubMedCrossRefGoogle Scholar
  185. Wilkes TE, Darby AC, Choi JH, Colbourne JK, Werren JH, Hurst GDD (2010) The draft genome sequence of Arsenophonus nasoniae, son-killer bacterium of Nasonia vitripennis, reveals genes associated with virulence and symbiosis. Insect Mol Biol 19:59–73. doi: 10.1111/j.1365-2583.2009.00963.x PubMedCrossRefGoogle Scholar
  186. Zchori-Fein E, Brown JK (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 95:711–718. doi: 10.1603/0013-8746(2002)095[0711:DOPAWB]2.0.CO;2 CrossRefGoogle Scholar
  187. Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40 % of terrestrial arthropod species are infected. PLoS One 7:3. doi: 10.1371/journal.pone.0038544 CrossRefGoogle Scholar
  188. Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol Rev 90:89–111. doi: 10.1111/brv.12098 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Julien Chuche
    • 1
    • 3
  • Nathalie Auricau-Bouvery
    • 2
  • Jean-Luc Danet
    • 2
  • Denis Thiéry
    • 1
  1. 1.INRA, UMR 1065 Santé et Agroécologie du Vignoble, Bordeaux Sciences Agro, ISVVVillenave d’Ornon CedexFrance
  2. 2.INRA, UMR 1332 Biologie du Fruit et PathologieUniversité de BordeauxVillenave d’Ornon CedexFrance
  3. 3.Department of BiologyMaynooth UniversityCounty KildareIreland

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