1887

Abstract

We have recently shown that Rickettsia , a secondary facultative bacterial symbiont that infects the whitefly B. tabaci is implicated in the transmission of Tomato yellow leaf curl virus (TYLCV). Infection with Rickettsia improved the acquisition and transmission of the virus by B. tabaci adults. Here we performed a transcriptomic analysis with Rickettsia -infected and uninfected B. tabaci adults before and after TYLCV acquisition. The results show a dramatic and specific activation of the immune system in the presence of Rickettsia before TYLCV acquisition. However, when TYLCV was acquired, it induced massive activation of gene expression in the Rickettsia uninfected population, whereas in the Rickettsia -infected population the virus induced massive down-regulation of gene expression. Fitness and choice experiments revealed that while Rickettsia -infected whiteflies are always more attracted to TYLCV-infected plants, this attraction is not always beneficiary for their offspring. These studies further confirm the role of Rickettsia in many aspects of B. tabaci interactions with TYLCV, and possibly serves as an important factor in the dissemination of the virus.

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2019-02-14
2024-04-20
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References

  1. Seal SE, Vandenbosch F, Jeger MJ. Factors Influencing begomovirus evolution and their increasing global significance: implications for sustainable control. CRC Crit Rev Plant Sci 2006; 25:23–46 [View Article]
    [Google Scholar]
  2. Ghanim M. 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 2014; 186:47–54 [View Article][PubMed]
    [Google Scholar]
  3. Islam W, Akutse KS, Qasim M, Khan KA, Ghramh HA et al. Bemisia tabaci-mediated facilitation in diversity of begomoviruses: Evidence from recent molecular studies. Microb Pathog 2018; 123:162–168 [View Article][PubMed]
    [Google Scholar]
  4. Moriones E, Navas-Castillo J. Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res 2000; 71:123–134 [View Article][PubMed]
    [Google Scholar]
  5. S-S L, Colvin J, de Barro PJ. Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there?. J Integr Agr 2012; 11:176–186
    [Google Scholar]
  6. Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M et al. 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 2010; 84:9310–9317 [View Article][PubMed]
    [Google Scholar]
  7. Thao ML, Baumann P. Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 2004; 70:3401–3406 [View Article][PubMed]
    [Google Scholar]
  8. Skaljac M, Zanic K, Ban SG, Kontsedalov S, Ghanim M. Co-infection and localization of secondary symbionts in two whitefly species. BMC Microbiol 2010; 10:142 [View Article][PubMed]
    [Google Scholar]
  9. Marubayashi JM, Kliot A, Yuki VA, Rezende JA, Krause-Sakate R et al. Diversity and localization of bacterial endosymbionts from whitefly species collected in Brazil. PLoS One 2014; 9:e108363 [View Article][PubMed]
    [Google Scholar]
  10. Gueguen G, Vavre F, Gnankine O, Peterschmitt M, Charif D et al. Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. Mol Ecol 2010; 19:4365–4376 [View Article][PubMed]
    [Google Scholar]
  11. Brumin M, Kontsedalov S, Ghanim M. Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 2011; 18:57–66 [View Article]
    [Google Scholar]
  12. Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M et al. The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Manag Sci 2008; 64:789–792 [View Article][PubMed]
    [Google Scholar]
  13. Kliot A, Cilia M, Czosnek H, Ghanim M. Implication of the bacterial endosymbiont Rickettsia spp. in interactions of the whitefly Bemisia tabaci with Tomato yellow leaf curl virus. J Virol 2014; 88:5652–5660 [View Article][PubMed]
    [Google Scholar]
  14. Sheng Q, Vickers K, Zhao S, Wang J, Samuels DC et al. Multi-perspective quality control of Illumina RNA sequencing data analysis. Brief Funct Genomics 2017; 16:194–204 [View Article][PubMed]
    [Google Scholar]
  15. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5:621–628 [View Article][PubMed]
    [Google Scholar]
  16. Götz M, Popovski S, Kollenberg M, Gorovits R, Brown JK et al. Implication of Bemisia tabaci heat shock protein 70 in Begomovirus-whitefly interactions. J Virol 2012; 86:13241–13252 [View Article][PubMed]
    [Google Scholar]
  17. Douglas AE, Bouvaine S, Russell RR. How the insect immune system interacts with an obligate symbiotic bacterium. Proc Biol Sci 2011; 278:333–338 [View Article][PubMed]
    [Google Scholar]
  18. Fang Y, Jiao X, Xie W, Wang S, Wu Q et al. Tomato yellow leaf curl virus alters the host preferences of its vector Bemisia tabaci. Sci Rep 2013; 3:3 [View Article][PubMed]
    [Google Scholar]
  19. Rono MK, Whitten MM, Oulad-Abdelghani M, Levashina EA, Marois E. The major yolk protein vitellogenin interferes with the anti-plasmodium response in the malaria mosquito Anopheles gambiae. PLoS Biol 2010; 8:e1000434 [View Article][PubMed]
    [Google Scholar]
  20. He WB, Li J, Liu SS. Differential profiles of direct and indirect modification of vector feeding behaviour by a plant virus. Sci Rep 2015; 5:5 [View Article][PubMed]
    [Google Scholar]
  21. Pan H, Chu D, Liu B, Shi X, Guo L et al. Differential effects of an exotic plant virus on its two closely related vectors. Sci Rep 2013; 3:3 [View Article][PubMed]
    [Google Scholar]
  22. Czosnek H, Ghanim M. Back to basics: are begomoviruses whitefly pathogens?. J Integr Agric 2012; 11:225–234 [View Article]
    [Google Scholar]
  23. Liu B, Preisser EL, Chu D, Pan H, Xie W et al. Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and Tomato yellow leaf curl virus. J Virol 2013; 87:4929–4937 [View Article][PubMed]
    [Google Scholar]
  24. Jahan SMH, Lee G-S, Lee S, Lee K-Y. Acquisition of Tomato yellow leaf curl virus enhances attraction of Bemisia tabaci to green light emitting diodes. J Asia Pac Entomol 2014; 17:79–82 [View Article]
    [Google Scholar]
  25. Pinheiro PV, Kliot A, Ghanim M, Cilia M. Is there a role for symbiotic bacteria in plant virus transmission by insects?. Curr Opin Insect Sci 2015; 8:69–78 [View Article]
    [Google Scholar]
  26. Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K et al. Symbiont-mediated insecticide resistance. Proc Natl Acad Sci USA 2012; 109:8618–8622 [View Article][PubMed]
    [Google Scholar]
  27. Su Q, Xie W, Wang S, Wu Q, Liu B et al. The endosymbiont Hamiltonella increases the growth rate of its host Bemisia tabaci during periods of nutritional stress. PLoS One 2014; 9:e89002 [View Article][PubMed]
    [Google Scholar]
  28. Su Q, Oliver KM, Xie W, Wu Q, Wang S et al. The whitefly-associated facultative symbiont Hamiltonella defensa suppresses induced plant defences in tomato. Funct Ecol 2015; 29:1007–1018 [View Article]
    [Google Scholar]
  29. Chen G, Pan H, Xie W, Wang S, Wu Q et al. Virus infection of a weed increases vector attraction to and vector fitness on the weed. Sci Rep 2013; 3:3 [View Article][PubMed]
    [Google Scholar]
  30. Rajabaskar D, Bosque-Pérez NA, Eigenbrode SD. Preference by a virus vector for infected plants is reversed after virus acquisition. Virus Res 2014; 186:32–37 [View Article][PubMed]
    [Google Scholar]
  31. Alvarez AE, Garzo E, Verbeek M, Vosman B, Dicke M et al. Infection of potato plants with potato leafroll virus changes attraction and feeding behaviour of Myzus persicae. Entomol Exp Appl 2007; 125:135–144 [View Article]
    [Google Scholar]
  32. Ghanim M, Morin S, Zeidan M, Czosnek H. Evidence for transovarial transmission of Tomato yellow leaf curl virus by its vector, the whitefly Bemisia tabaci. Virology 1998; 240:295–303 [View Article][PubMed]
    [Google Scholar]
  33. Engelmann F. Insect vitellogenin: identification, biosynthesis, and role in vitellogenesis. Adv Insect Physiol 1979; 14:49–108
    [Google Scholar]
  34. Guo JY, Dong SZ, Yang XL, Cheng L, Wan FH et al. Enhanced vitellogenesis in a whitefly via feeding on a begomovirus-infected plant. PLoS One 2012; 7:e43567 [View Article][PubMed]
    [Google Scholar]
  35. Guo JY, Cheng L, Ye GY, Fang Q, Guo JY. Feeding on a begomovirus-infected plant enhances fecundity via increased expression of an insulin-like peptide in the whitefly, MEAM1. Arch Insect Biochem Physiol 2014; 85:164–179 [View Article][PubMed]
    [Google Scholar]
  36. Wei J, He YZ, Guo Q, Guo T, Liu YQ et al. Vector development and vitellogenin determine the transovarial transmission of begomoviruses. Proc Natl Acad Sci USA 2017; 114:6746–6751 [View Article][PubMed]
    [Google Scholar]
  37. Wang ZZ, Bing XL, Liu SS, Chen XX. RNA interference of an antimicrobial peptide, Btdef, reduces Tomato yellow leaf curl China virus accumulation in the whitefly Bemisia tabaci. Pest Manag Sci 2017; 73:1421–1427 [View Article][PubMed]
    [Google Scholar]
  38. de Gregorio E, Spellman PT, Rubin GM, Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci USA 2001; 98:12590–12595 [View Article][PubMed]
    [Google Scholar]
  39. Geng L, Qian LX, Shao RX, Liu YQ, Liu SS et al. Transcriptome profiling of whitefly guts in response to Tomato yellow leaf curl virus infection. Virol J 2018; 15:14 [View Article][PubMed]
    [Google Scholar]
  40. Hariton Shalev A, Sobol I, Ghanim M, Liu SS, Czosnek H. The whitefly Bemisia tabaci Knottin-1 Gene is implicated in regulating the quantity of Tomato yellow leaf curl virus Ingested and Transmitted by the Insect. Viruses 2016; 8:205 [View Article][PubMed]
    [Google Scholar]
  41. Wang LL, Wang XR, Wei XM, Huang H, Wu JX et al. The autophagy pathway participates in resistance to Tomato yellow leaf curl virus infection in whiteflies. Autophagy 2016; 12:1560–1574 [View Article][PubMed]
    [Google Scholar]
  42. Park SG, Lee SM, Jung G. Antisense oligodeoxynucleotides targeted against molecular chaperonin Hsp60 block human hepatitis B virus replication. J Biol Chem 2003; 278:39851–39857 [View Article][PubMed]
    [Google Scholar]
  43. Li R, Yu C, Li Y, Lam TW, Yiu SM et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 2009; 25:1966–1967 [View Article][PubMed]
    [Google Scholar]
  44. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res 1997; 7:986–995 [View Article][PubMed]
    [Google Scholar]
  45. Wickham H. ggplot2. wiley interdiscip. Rev Comput Stat 2011; 3:180–185 [View Article]
    [Google Scholar]
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