Implication of the bacterial endosymbiont rickettsia spp. in interactions of the whitefly bemisia tabaci with tomato yellow leaf curl virus

Journal of Virology

Volumn 88, Issue 10, 2014, Pages 5652-5660

  Kliot, Adi ^a,b   Cilia, Michelle ^c   Czosnek, Henryk ^b   Ghanim, Murad ^a  

^a VOLCANI CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; ENDOSYMBIONT; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; MIDGUT; NONHUMAN; ORGANISMAL INTERACTION; PLANT VIRUS; PRIORITY JOURNAL; RICKETTSIA; RICKETTSIACEAE INFECTION; SWEET POTATO WHITEFLY; TOMATO YELLOW LEAF CURL VIRUS; VIRUS CONCENTRATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; BEGOMOVIRUS; CARRIER STATE; GASTROINTESTINAL TRACT; HEMIPTERA; MICROBIAL INTERACTIONS; RICKETTSIA; SYMBIOSIS;

EID: 84899072609     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00071-14     Document Type: Article

References (43)

1. Czosnek H, Ghanim M. 2012. Back to basics: are begomoviruses whitefly pathogens? J. Integrative Agric. 11:225-234. http://dx.doi.org/10.1016 /S2095-3119(12)60007-0.
2. Ghanim M, Morin S, Zeidan M, Czosnek H. 1998. Evidence for transovarial transmission of tomato yellow leaf curl virus by its vector, the whitefly Bemisia tabaci. Virology 240:295-303. http://dx.doi.org/10.1006/viro .1997.8937.
3. Liu B, Preisser EL, Chu D, Pan H, Xie W, Wang S, Wu Q, Zhou X, Zhang Y. 2013. Multiple forms of vector manipulation by a plantinfecting virus: Bemisia tabaci and Tomato yellow leaf curl virus. J. Virol. 87:4929-4937. http://dx.doi.org/10.1128/JVI.03571-12.
4. Ghanim M, Morin S, Czosnek H. 2001. Rate of Tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91:188-196. http://dx.doi.org /10.1094/PHYTO.2001.91.2.188.
5. Cicero JM, Brown JK. 2011. Functional anatomy of whitefly organs associated with Squash leaf curl virus (Geminiviridae: Begomovirus) transmission by the B biotype of Bemisia tabaci (Aleyrodidae: Hemiptera). Ann. Entomol. Soc. Am. 104:261-279. http://dx.doi.org /10.1603/AN10075.
6. Cicero JM, Brown JK. 2011. The anatomy of the accessory salivary glands of the whitefly Bemisia tabaci (Aleyrodidae: Hemiptera), and correlations to begomovirus transmission. Ann. Entomol. Soc. Am. 104:280-286. http://dx.doi.org/10.1603/AN10171.
7. Brown JK, Czosnek H. 2002. Whitefly-transmitted viruses, p 65-100. In Advances in botanical research. Academic Press, Inc, New York, NY.
8. Czosnek H, Ghanim M. 2002. The circulative pathway of begomoviruses in the whitefly vector Bemisia tabaci: insights from studies with Tomato yellow leaf curl virus. Ann. Appl. Biol. 140:215-231. http://dx.doi.org/10 .1111/j.1744-7348.2002.tb00175.x.
9. Hunter WB, Hiebert E, Webb SE, Tsai JK, JEP. 1998. Location of geminiviruses in the whitefly Bemisia tabaci (Homoptera: Aleyrodidae). Plant Dis. 82:1147-1151. http://dx.doi.org/10.1094/PDIS.1998 .82.10.1147.
10. Cicero JM, Hiebert E, Webb SE. 1995. The alimentary canal of Bemisia tabaci and Trialeurodes abutilonea (Homoptera, Sternorrhyncha): histology, ultrastructure, and correlations to function. Zoomorphology 115:31-39. http://dx.doi.org/10.1007/BF00397932.
11. Burrows ME, Caillaud MC, Smith DM, Benson EC, Gildow FE, Gray SM. 2006. Genetic regulation of polerovirus and luteovirus transmission in the aphid Schizaphis graminum. Phytopathology 96:828-837. http://dx .doi.org/10.1094/PHYTO-96-0828.
12. Ghanim M, Rosell RC, Campbell LR, Czosnek H, Brown JK, Ullman DE. 2001. Digestive, salivary, and reproductive organs of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) B type. J. Morphol. 248:22-40. http://dx.doi.org/10.1002/jmor.1018.
13. Gildow FE, Rochow WF. 1980. Role of accessory salivary glands in aphid transmission of Barley yellow dwarf virus. Virology 104:97-108. http://dx .doi.org/10.1016/0042-6822(80)90368-2.
14. Caciagli P, Medina Piles V, Marian D, Vecchiati M, Masenga V, Mason G, Falcioni T, Noris E. 2009. Virion stability is important for the circulative transmission of Tomato yellow leaf curl Sardinia virus by Bemisia tabaci, but virion access to salivary glands does not guarantee transmissibility. J. Virol. 83:5784-5795. http://dx.doi.org/10.1128/JVI.02267-08.
15. Chavez JD, Cilia M, Weisbrod CR, Ju HJEng Gray JKSM, Bruce JE. 2012. Cross-linking measurements of the Potato leafroll virus reveal protein interaction topologies required for virion stability, aphid transmission, and virus-plant interactions. J. Proteome Res. 11:2968-2981. http: //dx.doi.org/10.1021/pr300041t.
16. Cilia M, Tamborindeguy C, Fish T, Howe K, Thannhauser TW, Gray S. 2011. Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. J. Virol. 85:2148-2166. http://dx.doi.org/10.1128/JVI .01504-10.
17. Götz M, Popovski S, Kollenberg M, Gorovitz R, Brown JK, Cicero J, Czosnek H, Winter S, Ghanim M. 2012. Implication of Bemisia tabaci heat shock protein 70 in begomovirus-whitefly interactions. J. Virol. 86: 13241-13252. http://dx.doi.org/10.1128/JVI.00880-12.
18. Seddas P, Boissinot S, Strub JM, Van Dorsselaer A, Van Regenmortel MH, Pattus F. 2004. Rack-1, GAPDH3, and actin: proteins of Myzus persicae potentially involved in the transcytosis of beet western yellows virus particles in the aphid. Virology 325:399-412. http://dx.doi.org/10 .1016/j.virol.2004.05.014.
19. Baumann P. 2005. Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59:155-189. http://dx .doi.org/10.1146/annurev.micro.59.030804.121041.
20. 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. http://dx.doi.org/10.1128/AEM .72.5.3646-3652.2006.
21. 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. http://dx.doi.org/10.1128/JVI .00423-10.
22. Brumin M, Levy M, Ghanim M. 2012. Transovarial transmission of Rickettsia spp. and organ-specific infection of the whitefly Bemisia tabaci. Appl. Environ. Microbiol. 78:5565-5574. http://dx.doi.org/10.1128/AEM .01184-12.
23. Gottlieb Y, Ghanim M, Gueguen G, Kontsedalov S, Vavre F, Fleury F, Zchori-Fein E. 2008. Inherited intracellular ecosystem: symbiotic bacteria share bacteriocytes in whiteflies. FASEB J. 22:2591-2599. http://dx.doi.org /10.1096/fj.07-101162.
24. 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. http://dx.doi.org/10.1126/science.1199410.
25. Brumin M, Kontsedalov S, Ghanim M. 2011. Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci. 18:57-66. http://dx.doi.org/10.1111/j.1744-7917.2010.01396.x.
26. Sánchez-Campos S, Navas-Castillo J, Camero R, Soria C, Diaz J, Moriones E. 1999. Displacement of tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology 89:1038-1043. http://dx.doi.org/10.1094/PHYTO.1999.89.11.1038.
27. Gray SM, Power AG, Smith DM, Seaman AJ, Altman NS. 1991. Aphid transmission of barley yellow dwarf virus: acquisition access periods and virus concentration requirements. Phytopathology 81:539-545. http://dx .doi.org/10.1094/Phyto-81-539.
28. Chay CA, Gunasinge UB, Dinesh-Kumar SP, Miller WA, Gray SM. 1996. Aphid transmission and systemic plant infection determinants of barley yellow dwarf luteovirus-PAV are contained in the coat protein readthrough domain and 17-kDa protein, respectively. Virology 219:57-65. http://dx.doi.org/10.1006/viro.1996.0222.
29. Lucio-Zavaleta E, Smith DM, Gray SM. 2001. Variation in transmission efficiency among barley yellow dwarf virus-RMV isolates and clones of the normally inefficient aphid vector, Rhopalosiphum padi. Phytopathology 91:792-796. http://dx.doi.org/10.1094/PHYTO.2001.91.8.792.
30. Lee L, Palukaitis P, Gray SM. 2002. Host-dependent requirement for the Potato leafroll virus 17-kDa protein in virus movement. Mol. Plant-Microbe Interact. 15:1086-1094. http://dx.doi.org/10.1094/MPMI.2002 .15.10.1086.
31. Jiang Y, Walker G. 2003. Electrical penetration graphs of the nymphal stage of Bemisia argentifolii. Entomol. Exp. Appl. 109:101-111. http://dx .doi.org/10.1046/j.1570-7458.2003.00093.x.
32. Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M, Ghanim M. 2008. The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest. Manag. Sci. 64:789-792. http://dx.doi.org/10.1002/ps.1595.
33. Skaljac M, Zanic K, Ban SG, Kontsedalov S, Ghanim M. 2010. Coinfection and localization of secondary symbionts in two whitefly species. BMC Microbiol. 10:142. http://dx.doi.org/10.1186/1471-2180-10-142.
34. Rubinstein G, Czosnek H. 1997. Long-term association of tomato yellow leaf curl virus with its whitefly vector Bemisia tabaci: effect on the insect transmission capacity, longevity, and fecundity. J. Gen. Virol. 78(Pt 10): 2683-2689.
35. Luan JB, Li JM, Varela N, Wang YL, Li FF, Bao YY, Zhang CX, Liu SS, Wang XW. 2011. Global analysis of the transcriptional response of whitefly to tomato yellow leaf curl China virus reveals the relationship of coevolved adaptations. J. Virol. 85:3330-3340. http://dx.doi.org/10.1128 /JVI.02507-10.
36. Ghanim M, Brumin M, Popovski S. 2009. A simple, rapid and inexpensive method for localization of Tomato yellow leaf curl virus and Potato leafroll virus in plant and insect vectors. J. Virol. Methods 159:311-314. http://dx.doi.org/10.1016/j.jviromet.2009.04.017.
37. Skaljac M, Ghanim M. 2010. Coinfection and localization of secondary symbionts in two whitefly species. Isr. J. Plant Sci. 58:103-111. http://dx .doi.org/10.1560/IJPS.58.2.103.
38. 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. http://dx.doi.org/10.1038/nature10356.
39. 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. http://dx.doi.org/10 .1016/j.cell.2009.11.042.
40. Rances 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. http://dx.doi.org/10.1371/journal .ppat.1002548.
41. Zhang G, Hussain M, O'Neill SL, Asgari S. 2013. Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to gangue virus inhibition in Aedes aegypti Proc. Natl. Acad. Sci. U. S. A. 110:10276-10281. http://dx.doi.org/10.1073/pnas.1303603110.
42. 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. http://dx.doi.org/10.1126/science.1177531.
43. Suh E, Mercer DR, Fu Y, Dobson SL. 2009. Pathogenicity of lifeshortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Appl. Environ. Microbiol. 75:7783-7788. http://dx.doi.org /10.1128/AEM.01331-09.