Differential Gene Transcription in Honeybee (Apis cerana) Larvae Challenged by Chinese Sacbrood Virus (CSBV)
DOI:
https://doi.org/10.13102/sociobiology.v60i4.413-420Keywords:
Apis cerana, qRT – PCR, antiviral immunity, RNAiAbstract
Honey bees are economically important social insect. They are suffering from all kinds of pathogens, especially the virus. In response to pathogens, different immune pathways such as Toll, Imd, Jak-Stat and RNAi are involved. In the present study, the transcription analysis of 32 immune-related genes from Apis cerana challenged by Chinese sacbrood virus (CSBV), the most widely distributed virus in A. cerana, was carried out by qRT-PCR to provide cues for the antiviral mechanism and the effective control of bee viruses. The expression level of 22 genes were statistically changed, including 11 up-regulated genes (catus-2, lys-2, vir, s3a, mta1, faa, vhdl, co-1-iv, ago-1, ago-3, aub) in which 3 (ago-1, ago-3, aub) were related to RNAi pathway, and 11 down-regulated genes (kenny, pgrp-lc, pgrp-s2, abaecin, lys-1, lys-3, domeless, tepa, mlc, dscam, rpl8) related to Toll, Imd, and Jak-Stat pathways. The results indicated CSBV infection in A. cerana may activate a RNA-based antiviral immunity system. This work constituted the first report, under laboratory conditions, about induction of immune related genes in response to CSBV.Downloads
References
Ai, H.X., Yan, X., & Han, R.C. (2012). Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. J. Invertebr. Pathol., 109: 160-164. doi: org/10.1016/j.jip.2011.10.006 DOI: https://doi.org/10.1016/j.jip.2011.10.006
Antúnez, K., Martín-Hernández, R., Prieto, L., Meana, A., Zunino, P., & Higes, M. (2009). Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol., 11: 2284 - 90. doi: 10.1111/j.1462-2920.2009.01953.x DOI: https://doi.org/10.1111/j.1462-2920.2009.01953.x
Aronstein, K.A., Murray, K.D., & Saldivar, E. (2010). Transcriptional responses in honey bee larvae infected with chalkbrood fungus. BMC Genomics, 11: 391. doi: 10.1186/1471-2164-11-391. DOI: https://doi.org/10.1186/1471-2164-11-391
Azzami K., Ritter, W., Tautz, J., & Beier, H. (2012). Infection of honey bees with acute bee paralysis virus does not trigger humoral or cellular immune responses. Arch. Virol., 157: 689 - 702. doi: 10.1007/s00705-012-1223-0 DOI: https://doi.org/10.1007/s00705-012-1223-0
Boutros, M., Agaisse, H. & Perrimon, N. (2002) Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell, 3: 711 - 722. doi: org/10.1016/S1534-5807(02)00325-8 DOI: https://doi.org/10.1016/S1534-5807(02)00325-8
Chaimanee, V., Chantawannakul, P., Chen, Y., Evans, J.D., & Pettis, J.S. (2012) Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J. Insect Physiol. 58: 1090 - 1095. doi: org/10.1016/j.jinsphys.2012.04.016 DOI: https://doi.org/10.1016/j.jinsphys.2012.04.016
Chan, Q.W., Melathopoulos, A.P., Pernal, S.F., & Foster, L.J. (2009). The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics, 10: 387. doi:10.1186/1471-2164-10-387 DOI: https://doi.org/10.1186/1471-2164-10-387
Chen. Y., Zhao, Y., Hammond, J., Hsu, H.T., Evans, J., & Feldlaufer, M. (2004). Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J. Invertebr. Pathol., 87: 84 - 93. doi: org/10.1016/j.jip.2004.07.005 DOI: https://doi.org/10.1016/j.jip.2004.07.005
Chen, Y.P., Pettis, J.S., Collins, A., & Feldlaufer, M.F. (2006). Prevalence and transmission of honeybee viruses. Appli. Environm. Microbiol., 72: 606 - 611. doi: 10.1128/AEM.72.1.606-611.2006 DOI: https://doi.org/10.1128/AEM.72.1.606-611.2006
Christophides, G.K., Vlachou, D., & Kafatos, F.C. (2004). Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol. Rev., 198: 127 - 148. doi: 10.1111/j.0105-2896.2004.0127.x DOI: https://doi.org/10.1111/j.0105-2896.2004.0127.x
Clem, R.J. (2005). The role of apoptosis in defense against baculovirus infection in insects. Curr. Top. Microbiol. Immunol., 289: 113 - 29. doi: 10.1007/3-540-27320-4_5 DOI: https://doi.org/10.1007/3-540-27320-4_5
Ding, S.W. (2010). RNA-based antiviral immunity. Nat. Rev. Immunol., 10: 632 - 644. doi:10.1038/nri2824 DOI: https://doi.org/10.1038/nri2824
Dostert, C., Jouanguy, E., Irving, P., Troxler, L., Galiana-Arnoux, D., Hetru, C., Hoffmann, J.A., & Imler, J.L. (2005). The jak-stat signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat. Immunol., 6: 946 - 953. doi:10.1038/ni1237 DOI: https://doi.org/10.1038/ni1237
Dussaubat, C., Brunet, J.L., Higes, M., Colbourne, J.K., & Lopez, J. (2012). Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS ONE 7(5): e37017. doi:10.1371/journal.pone.0037017 DOI: https://doi.org/10.1371/journal.pone.0037017
Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H., Kanost, M., Thompson, G.J., Zou, Z., & Hultmark, D. (2006). Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol., 15: 645 - 656. doi: 10.1111/j.1365-2583.2006.00682.x DOI: https://doi.org/10.1111/j.1365-2583.2006.00682.x
Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J.A., & Imler, J.L. (2006). Essential function in vivo for dicer-2 in host defense against RNA viruses in drosophila. Nat. Immunol., 7: 590 - 597. doi:10.1038/ni1335 DOI: https://doi.org/10.1038/ni1335
Galiana-Arnoux, D., Deddouche, S., & Imler, J.L. (2007). Antiviral immunity in drosophila. J. Soc. Biol., 201: 359 - 365. doi: org/10.1016/j.coi.2009.01.007 DOI: https://doi.org/10.1051/jbio:2007906
Gallai, N., Salles, J.M., Settele, J., & Vaissière, B.E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ., 68: 810 - 821. doi: org/10.1016/j.ecolecon.2008.06.014 DOI: https://doi.org/10.1016/j.ecolecon.2008.06.014
Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., Morales, J.M., Bommarco, R., Cunningham, S.A., Carvalheiro, L.G., Chacoff, N.P., Dudenhoffer, J.H., Greenleaf, S.S., Holzschuh, A., Isaacs, R., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L.A., Potts, S.G., Ricketts, T.H., Szentgyorgyi, H., Viana, B.F., Westphal, C., Winfree, R., & Klein, A.M. (2011). Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett., 14: 1062-1072. doi: 10.1111/j.1461-0248.2011.01669.x DOI: https://doi.org/10.1111/j.1461-0248.2011.01669.x
Garrido, P.M., Antúnez, K., Martín, M., Porrini, M.P., Zunino, P., & Eguaras, M.J. (2013). Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides. J. Insect Physiol., 59: 113-119. doi: org/10.1016/j.jinsphys.2012.10.019 DOI: https://doi.org/10.1016/j.jinsphys.2012.10.019
Ghosh, R.C., Ball, B.V., Willcocks, M.M., & Carter, M.J. (1999). The nucleotide sequence of sacbrood virus of the honey bee: an insect picorna-like virus. J. Gen. Virol., 80: 1541-1549. DOI: https://doi.org/10.1099/0022-1317-80-6-1541
Gorg, A., Postel, W., Domscheit, A., & Günther, S. (1988). Two-dimensional electrophoresis with immobilized pH gradients of leaf proteins from barley (Hordeum vulgare): method, reproducibility and genetic aspects. Electrophoresis. 9: 681- 692. DOI: https://doi.org/10.1002/elps.1150091103
Gregorc, A., Evans, J.D., Scharf, M., & Ellis, J.D. (2012). Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). J. Insect Physiol., 58: 1042-1049. doi: org/10.1016/j.jinsphys.2012.03.015 DOI: https://doi.org/10.1016/j.jinsphys.2012.03.015
Gregory, P.G., Evans, J.D., Rinderer, T. & De Guzman, L. (2005) Conditional immune-gene suppression of honeybees parasitized by Varroa mites. J. Insect Sci., 5: 1 - 5. DOI: https://doi.org/10.1673/031.005.0701
Hamiduzzaman, M.M., Sinia, A., Guzman-Novoa, E., Guzman-Novoa, E., & Goodwin, P.H. (2012). Entomopatho genic fungi as potential biocontrol agents of the ecto-parasitic mite, Varroa destructor, and their effect on the immune response of honey bees (Apis mellifera L.). J. Invertebr. Pathol., 111: 237 - 243. doi: org/10.1016/j.jip.2012.09.001 DOI: https://doi.org/10.1016/j.jip.2012.09.001
Han, B., Zhang, L., Feng, M., Fang, Y., & Li, J.K. (2013). An integrated proteomics reveals pathological mechanism of honeybee (Apis cerena) sacbrood disease. J. Proteome Res., 12: 1881-1897. doi: 10.1021/pr301226d DOI: https://doi.org/10.1021/pr301226d
Hoffmann, J.A. (2003). The immune response of Drosophila. Nature, 426: 33 - 38. doi:10.1038/nature02021 DOI: https://doi.org/10.1038/nature02021
Honey Bee Genome Sequencing Consortium. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 443: 931 - 949. doi: 10.1038/nature05260 DOI: https://doi.org/10.1038/nature05260
Hultmark, D. (2003). Drosophila immunity: Paths and patterns. Curr. Opin. Immunol., 15: 12 - 19. doi: org/10.1016/S0952-7915(02)00005-5 DOI: https://doi.org/10.1016/S0952-7915(02)00005-5
Keene, K.M., Foy, B.D., Sanchez-Vargas, I., Beaty, B.J., Blair, C.D., & Olson, K.E. (2004). RNA interference acts as a natural antiviral response to o’nyong-nyong virus (alphavirus; Togaviridae) infection of anopheles gambiae. Proc. Natl. Acad Sci. USA, 101: 17240 - 17245. doi: 10.1073/pnas.0406983101 DOI: https://doi.org/10.1073/pnas.0406983101
Kemp, C., & Imler, J.L. (2009). Antiviral immunity in drosophila. Curr. Opin. Immunol., 21: 3 - 9. doi: org/10.1016/j.coi.2009.01.007 DOI: https://doi.org/10.1016/j.coi.2009.01.007
Liu, X.J., Zhang, Y., Yan, X., & Han, R.C. (2010). Prevention of chinese sacbrood virus infection in Apis cerana using RNA interference. Curr. Microbiol., 61: 422 - 428. doi: 10.1007/s00284-010-9633-2 DOI: https://doi.org/10.1007/s00284-010-9633-2
Lourenço, A.P., Guidugli-Lazzarini, K.R., Freitas, F.C., Bitondi, M.M., Simões, Z.L., Parker, R., Guarna, M.M., Melathopoulos, A.P., Moon, K.M., White, R., Huxter, E., Pernal, S.F., & Foster, L.J. (2013). Bacterial infection activates the immune system response and dysregulates microRNA expression in honey bees. Insect Biochem. Mol. Biol., 43: 474 - 482. doi: org/10.1016/j.ibmb.2013.03.001 DOI: https://doi.org/10.1016/j.ibmb.2013.03.001
Ma, M.X., Li, M., Cheng, J., Yang, S., Wang, S.D., & Li, P.F. (2011). Molecular and biological characterization of Chinese sacbrood virus LN isolate. Comp. Funct. Genomics, doi:10.1155/2011/409386 DOI: https://doi.org/10.1155/2011/409386
Patel, A., Fondrk, M.K., Kaftanoglu, O., Emore, C., Hunt, G., Frederick, K., & Amdam, G.V. (2007). The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE, 2: e509. doi: 10.1371/journal.pone.0000509 DOI: https://doi.org/10.1371/journal.pone.0000509
Royet, J., Reichhart, J.-M., & HoVmann, J.A. (2005). Sensing and signaling during infection in Drosophila. Curr. Opin. Immunol., 17: 11 - 17. doi: org/10.1016/j.coi.2004.12.002 DOI: https://doi.org/10.1016/j.coi.2004.12.002
Scharlaken, B., de Graaf, D.C., & Goossens, K. (2008). Differential gene expression in the honeybee head after a bacterial challenge. Dev. Comp. Immunol., 32: 883 - 889. doi: org/10.1016/j.dci.2008.01.010 DOI: https://doi.org/10.1016/j.dci.2008.01.010
Stenbak, C.R., Ryu, J.H., Leulier, F., Pili-Floury, S., Parquet, C., Herve, M., Chaput, C., Boneca, I.G., Lee, W.J., Lemaitre, B. & Mengin-Lecreulx, D. (2004). Peptidoglycan molecular requirements allowing detection by the Drosophila immune deficiency pathway. J. Immunol., 173: 7339 - 7348. Retrived from: http://www.jimmunol.org/content/173/12/7339.short DOI: https://doi.org/10.4049/jimmunol.173.12.7339
van RiJ, R.P., Saleh, M.C., Berry, B., Foo, C., Houk, A., Antoniewski, C., & Andino, R. (2006). The RNA silencing endonuclease argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev., 20: 2985 - 2995. doi: 10.1101/gad.1482006 DOI: https://doi.org/10.1101/gad.1482006
Werner, T., Borge-Renberg, K., Hultmark, D., Mellroth, P. & Steiner, H. (2003). Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysaccharide and peptidoglycan. J. Biol. Chem., 278: 26319 - 26322. doi: 10.1074/jbc.C300184200 DOI: https://doi.org/10.1074/jbc.C300184200
Xu, Y., Huang, L., Fu, S., Wu, J., & Zhou, X. (2012). Population diversity of rice stripe virus-derived siRNAs in three different hosts and RNAi-based antiviral immunity in Laodelphgax striatellus. PLoS One, 7: e46238. doi: 10.1371/journal.pone.0046238 DOI: https://doi.org/10.1371/journal.pone.0046238
Yan, X., Chen, J.H., & Han, R.C. (2009). Detection of Chinese sacbrood virus (CSBV) in Apis cerana by RT-PCR method. Sociobiology, 53: 687 - 694.
Yan, X., & Han, R.C. (2008). Diagnostic technologies of common pathogens of honeybees in China. Chin. Bull. Entomol., 45: 483 - 488. Retrived from: http://en.cnki.com.cn/Article_en/CJFDTOTAL-KCZS200803039.htm
Yang, X.L., & Cox-Foster, D.L. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proc. Natl. Acad Sci. USA, 102: 7470 - 7475. doi: 10.1073/pnas.0501860102 DOI: https://doi.org/10.1073/pnas.0501860102
Zhang, Y., Liu, X.J., Zhang, W.Q., & Han, R.C. (2010). Differential gene expression of the honey bees Apis mellifera and A. cerana induced by Varroa destructor infection. J. Insect Physiol., 56: 1207 - 1218. doi: org/10.1016/j.jinsphys.2010.03.019 DOI: https://doi.org/10.1016/j.jinsphys.2010.03.019
Downloads
Published
How to Cite
Issue
Section
License
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).

eISSN 2447-8067









