Changes in Alternative Splicing in Apis Mellifera Bees Fed Apis Cerana Royal Jelly

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The Western honey bee (Apis mellifera) is a social insect characterized by caste differentiation in which the queen bee and worker bees display marked differences in morphology, behavior, reproduction, and longevity despite their identical genomes. The main causative factor in caste differentiation is the food fed to queen larvae, termed royal jelly (RJ). Alternative splicing (AS) is an important RNA-mediated post-transcriptional process in eukaryotes. Here we report AS changes in A. mellifera after being fed either A. mellifera RJ or A. cerana RJ. The results demonstrated that the RJ type affected 4 types of AS in adult A. mellifera: exon skipping, intron retention, alternative 5’ splice sites, and alternative 3’splice sites. After feeding with A. cerana RJ, AS occurred in many genes in adult A. mellifera that encode proteins involved in development, growth, the tricarboxylic acid cycle, and substance metabolism. This study provides the first evidence that heterospecific RJ can influence the AS of many genes related to honey bee development and growth.

Barchuk A. R., Cristino A. S., Kucharski R., Costa L. F., Simões Z. L., Maleszka R. (2007) Molecular determinants of caste differentiation in the highly eusocial honey bee Apis mellifera. BMC Developmental Biology 7: 70. DOI:10.1186/1471-213X-7-70

Black D. L. (2003) Mechanisms of alternative premessenger RNA splicing. Annual Review of Biochemistry 72: 291-336. DOI: 10.1146/annurev.biochem. 72.121801.161720

Calderone N. W. (2012) Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992-2009. PLoS One 7(5): e37235. DOI: 10.1371/journal.pone.0037235

Drapeau M. D., Albert S., Kucharski R., Prusko C., Maleszka R. (2006) Evolution of the Yellow/Major Royal Jelly Protein family and the emergence of social behavior in honeybees. Genome Research 16(11): 1385-1394. DOI: 10.1101/gr.5012006

Fang Y., Feng M., Li J. K. (2010) Royal jelly proteome comparison between A. mellifera ligustica and A. cerana cerana. Journal of Proteome Research 9: 2207-2215. DOI: 10.1021/pr900979h

Foret S., Kucharski R., Pellegrini M., Feng S., Jacobsen S. E., Robinson G. E., Maleszka R. (2012) DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honeybees. Proceedings of the National Academy of Sciences of the USA 109(13): 4968-4973. DOI: 10.1073/pnas.1202392109

Guan C., Zeng Z. J., Wang Z. L., Yan W. Y., Pan Q. Z. (2013) Expression of sir2, hdac1 and ash2 in honey bee (Apis mellifera L.) queens and workers. Journal of Apicultural Science 57(1): 67-73. DOI: 10.2478/jas-2013-0008

Huang S., Zhang J., Li R., Zhang W., He Z., Lam T. W., Peng Z., Yiu S. M. (2011) SOAP splice: Genome- wide ab initiodetection of splice junctions from RNA-seq data. Frontiers in Genetics 2: 46-58. DOI: 10.3389/fgene.2011.00046

Jarosch A., Stolle E., Crewe R. M., Moritz R. F. (2011) Alternative splicing of a single transcription factor drives selfish reproductive behavior in honeybee workers (Apis mellifera). Proceedings of the National Academy of Sciences of the USA 108(37): 15282-15287. DOI: 10.1073/pnas.1109343108

Kamakura M. (2011) Royalactin induces queen differentiation in honeybees. Nature 473(7348): 478-483. DOI: 10.1038/nature10093

Li Y., Li-Byarlay H., Burns P., Borodovsky M., Robinson G. E., Ma J. (2012) TrueSight: a new algorithm for splice junction detection using RNA-seq. Nucleic Acids Research 41(4): e51. DOI: 10.1093/nar/gks1311

Lyko F., Foret S., Kucharski R., Wolf S., Falckenhayn C., Maleszka R. (2010) The honeybee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biology 9: e1000506. DOI: 10.1371/journal. pbio.1000506

Modrek B., Lee C. (2002) A genomic view of alternative splicing. Nature Genetics 30(1): 13-19. DOI:10.1038/ ng0102-13

Oldroyd B. P., Wongsiri S. (2006) Asian honey bees biology, conservation and human interactions. Harvard University Press. Cambridge Massachusetts. London. 340 pp.

Peng Y. S., Fang Z. Y., Xu S. Y., Ge L. S. (1987) The resistance mechanism of the Asian honey bee, Apis cerana cerana Fabr., to ectoparasitic mite, Varroa jacbsoni Oudemans. Journal of Invertebrate Pathology 47: 54-60. DOI: 10.1016/0022-2011(87)90125-x

Qu N., Jiang J., Sun L., Lai C., Sun L., Wu X. (2008) Proteomic characterization of royal jelly proteins in Chinese (Apis cerana cerana) and European (Apis mellifera) honeybees. Biochemistry (Moscow) 73(6): 676-680. DOI: 10.1134/S0006297908060072

Seeley T. D. (1989) The honeybee colony as a superorganism. American Scientist 77: 546- 553.

Shi Y. Y., Wu X. B., Huang Z. Y., Wang Z. L., Yan W. Y., Zeng Z. J. (2012) Epigenetic modification of gene expression in honey bees by heterospecific gland secretions. PLoS One 7(8): e43727. DOI: 10.1371/journal.pone.0043727

StatView v 5.01. SAS Institute. Gary, NC, USA.

Viuda-Martos M., Ruiz-Navajas Y., Fernández-López J., Pérez- Alvarez J. A. (2008) Functional properties of honey, propolis, and royal jelly. Journal of Food Science 73(9): R117-R124. DOI: 10.1111/j.1750-3841.2008.00966.x

Wang Z., Chatterjee D., Jeon H. Y., Akerman M., Vander Heiden M. G., Cantley L. C., Krainer A. R. (2012) Exon-centric regulation of pyruvate kinase M alternative splicing via mutually exclusive exons. Journal of Molecular Cell Biology 4(2): 79-87. DOI: 10.1093/jmcb/mjr030

Weaver N. (1957) Effects of larval honey bee age on dimorphic differentiation of the female honeybee. Annals of the Entomological Society of America 50: 283-294.

Weaver N. (1966) Physiology of caste determination. Annual Review of Entomology 11: 79-102. DOI: 10.1146/ annurev.en.11.010166.000455

Winston M. L. (1987) Biology of the honey bee. Harvard University Press. Cambridge. 281 pp.

Wu J., Li J. K. (2010) Proteomic analysis of the honeybee (Apis mellifera L.) caste differentiation between worker and queen larvae. Scientia Agricultura Sinica 43(5): 176-181.

Xie X. B., Peng W. J., Zeng Z. J. (2008) Breeding of miteresistant honeybee by using nutritional crossbreed technology. Scientia Agricultura Sinica 41(5): 1530-1535.

Zeng Z. J., Zou Y., Guo D. S., Yan W. Y. (2006) Comparison studies of DNA and RNA in royal jelly from Apis mellifera and Apis cerana. Indian Bee Journal 68(1/4): 18-21.

Zeng Z. J., Jiang Y. S., Hu F. L., Xu B. H., Su S. K. (2009) Apiculture. China Agriculture Press. Beijing. 134 pp.

Journal of Apicultural Science

The Journal of Research Institute of Horticulture and Apicultural Research Association

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