Bidirectional Transfer of RNAi between Honey Bee and : Gene Silencing Reduces Population

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The mite Varroa destructor is an obligatory ectoparasite of the honey bee (Apis mellifera) and is one of the major threats to apiculture worldwide. We previously reported that honey bees fed on double-stranded RNA (dsRNA) with a sequence homologous to that of the Israeli acute paralysis virus are protected from the viral disease. Here we show that dsRNA ingested by bees is transferred to the Varroa mite and from mite on to a parasitized bee. This cross-species, reciprocal exchange of dsRNA between bee and Varroa engendered targeted gene silencing in the latter, and resulted in an over 60% decrease in the mite population. Thus, transfer of gene-silencing-triggering molecules between this invertebrate host and its ectoparasite could lead to a conceptually novel approach to Varroa control.

Vyšlo v časopise: Bidirectional Transfer of RNAi between Honey Bee and : Gene Silencing Reduces Population. PLoS Pathog 8(12): e32767. doi:10.1371/journal.ppat.1003035
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003035

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Zdroje

1. GallaiN, SallesJM, SetteleJ, VaissiereBE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68: 810–821.

2. GenerschE (2010) Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology 87: 87–97.

3. RosenkranzP, AumeierP, ZiegelmannB (2010) Biology and control of Varroa destructor. Journal of Invertebrate Pathology 103: S96–S119.

4. Guzman-NovoaE, EcclesL, CalveteY, McGowanJ, KellyPG, et al. (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 41: 443–450.

5. NavajasM, MigeonA, AlauxC, Martin-MagnietteML, RobinsonGE, et al. (2008) Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 9: 301.

6. ShenMQ, CuiLW, OstiguyN, Cox-FosterD (2005) Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. Journal of General Virology 86: 2281–2289.

7. Di PriscoG, PennacchioF, CaprioE, BoncristianiHF, EvansJD, et al. (2011) Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. Journal of General Virology 92: 151–155.

8. GisderS, AumeierP, GenerschE (2009) Deformed wing virus: replication and viral load in mites (Varroa destructor). Journal of General Virology 90: 463–467.

9. ShimanukiH, CalderoneNW, KnoxDA (1994) Parasitic mite syndrome-the symptoms. American Bee Journal 134: 827–828.

10. BoeckingO, GenerschE (2008) Varroosis - the ongoing crisis in bee keeping. Journal Fur Verbraucherschutz Und Lebensmittelsicherheit-Journal of Consumer Protection and Food Safety 3: 221–228.

11. PettisJS (2004) A scientific note on Varroa destructor resistance to coumaphos in the United States. Apidologie 35: 91–92.

12. ThompsonHM, BrownMA, BallRF, BewMH (2002) First report of Varroa destructor resistance to pyrethroids in the UK. Apidologie 33: 357–366.

13. Mozes-KochR, SlabezkiY, EfratH, KalevH, KamerY, et al. (2000) First detection in Israel of fluvalinate resistance in the varroa mite using bioassay and biochemical methods. Experimental and Applied Acarology 24: 35–43.

14. MaggiMD, RuffinengoSR, NegriP, EguarasMJ (2010) Resistance phenomena to amitraz from populations of the ectoparasitic mite Varroa destructor of Argentina. Parasitology Research 107: 1189–1192.

15. FireA, XuS, MontgomeryMK, KostasSA, DriverSE, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811.

16. HannonGJ (2002) RNA interference. Nature 418: 244–251.

17. de la FuenteJ, KocanKM, AlmazanC, BlouinEF (2007) RNA interference for the study and genetic manipulation of ticks. Trends in Parasitology 23: 427–433.

18. BaumJA, BogaertT, ClintonW, HeckGR, FeldmannP, et al. (2007) Control of coleopteran insect pests through RNA interference. Nature Biotechnology 25: 1322–1326.

19. FairbairnDJ, CavallaroAS, BernardM, Mahalinga-IyerJ, GrahamMW, et al. (2007) Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 226: 1525–1533.

20. YadavBC, VeluthambiK, SubramaniamK (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Molecular and Biochemical Parasitology 148: 219–222.

21. SteevesRM, ToddTC, EssigJS, TrickHN (2006) Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Functional Plant Biology 33: 991–999.

22. RechaviO, MinevichG, HobertO (2011) Transgenerational inheritance of an acquired small RNA-based antiviral response in C. elegans. Cell 147: 1248–1256.

23. BuckleyBA, BurkhartKB, GuSG, SpracklinG, KershnerA, et al. (2012) A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. Nature 489: 447–451.

24. CampbellEM, BudgeGE, BowmanAS (2010) Gene-knockdown in the honey bee mite Varroa destructor by a non-invasive approach: studies on a glutathione S-transferase. Parasites & Vectors 3: 73.

25. AronsteinK, PankiwT, SaldivarE (2006) SID-I is implicated in systemic gene silencing in the honey bee. Journal of Apicultural Research 45: 20–24.

26. PatelA, FondrkMK, KaftanogluO, EmoreC, HuntG, et al. (2007) The making of a queen: TOR pathway is a key player in diphenic caste development. Plos One 2: e509.

27. NunesFMF, SimoesZLP (2009) A non-invasive method for silencing gene transcription in honeybees maintained under natural conditions. Insect Biochemistry and Molecular Biology 39: 157–160.

28. MuttiNS, DolezalAG, WolschinF, MuttiJS, GillKS, et al. (2011) IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. Journal of Experimental Biology 214: 3977–3984.

29. MaoriE, PaldiN, ShafirS, KalevH, TsurE, et al. (2009) IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion. Insect Molecular Biology 18: 55–60.

30. LiuXJ, ZhangY, YanX, HanRC (2010) Prevention of Chinese Sacbrood Virus infection in Apis cerana using RNA interference. Current Microbiology 61: 422–428.

31. PaldiN, GlickE, OlivaM, ZilberbergY, AubinL, et al. (2010) Effective gene silencing in a microsporidian parasite associated with honeybee (Apis mellifera) colony declines. Applied and Environmental Microbiology 76: 5960–5964.

32. HunterW, EllisJ, VanengelsdorpD, HayesJ, WesterveltD, et al. (2010) Large-scale field application of RNAi technology reducing Israeli Acute Paralysis Virus disease in honey bees (Apis mellifera, Hymenoptera: Apidae). Plos Pathogens 6: e1001160.

33. CornmanRS, SchatzMC, JohnstonJS, ChenY-P, PettisJ, et al. (2010) Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. Bmc Genomics 11: 602.

34. FaganLL, NelsonWR, MeenkenED, HowlettBG, WalkerMK, et al. (2012) Varroa management in small bites. Journal of Applied Entomology 136: 473–475.

35. AkyolE, YeninarH (2011) The effects of Varroa (Varroa destructor) infestation level on wintering ability and survival rates of honeybee (Apis mellifera L.) colonies. Journal of Animal and Veterinary Advances 10: 1427–1430.

36. JaroschA, MoritzR (2011) RNA interference in honeybees: off-target effects caused by dsRNA. Apidologie 43: 128–138.

37. Sambrook J, DW R (2001) Molecular cloning: a laboratory manual. Cold spring harbor laboratory press. pp. A8.9–A8.10

38. ShafirS, MendaG, SmithBH (2005) Caste-specific differences in risk sensitivity in honeybees, Apis mellifera. Animal Behaviour 69: 859–868.

39. YuanJS, ReedA, ChenF, StewartCN (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7: 85.