A dietary phytochemical alters caste-associated gene expression in honey bees

Science Advances

Volumn 1, Issue 7, 2015, Pages

  Mao, Wenfu ^a   Schuler, Mary A ^b   Berenbaum, May R ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOOD PRODUCTS; GENES;

APIS MELLIFERA; HONEY BEE; INHIBITORY EFFECT; OVARY DEVELOPMENT; P-COUMARIC ACID; PHYTOCHEMICAL; PHYTOCHEMICALS; ROYAL JELLY;

GENE EXPRESSION;

EID: 85027834963     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500795     Document Type: Article

References (36)

1. M. H. Haydak, Honey bee nutrition. Annu. Rev. Entomol. 15, 143-156 (1970).
2. C. D. Michener, The Social Behavior of the Bees (Harvard Univ. Press, Cambridge, MA, 1974).
3. M. Asencot, Y. Lensky, The effect of sugars and juvenile hormone on the differentiation of the female honeybee larvae (Apis mellifera L.) to queens. Life Sci. 18, 693-699 (1976).
4. M. Asencot, Y. Lensky, Juvenile hormone induction of 'queenliness' on female honey bee (Apis mellifera L.) larvae reared on worker jelly and on stored royal jelly. Comp. Biochem. Physiol. B 78, 109-117 (1984).
5. M. Asencot, Y. Lensky, The phagostimulatory effect of sugars on the induction of "queenliness" in female honeybee (Apis mellifera L.) larvae. Comp. Biochem. Physiol. A 81, 203-208 (1985).
6. M. Asencot, Y. Lensky, The effect of soluble sugars in stored royal jelly on the differentiation of female honeybee (Apis mellifera L.) larvae to queens. Insect Biochem. 18, 127-133 (1988).
7. R. E. Page Jr., C. Y.-S. Peng, Aging and development in social insects with emphasis on the honey bee, Apis mellifera. L. Exp. Gerontol. 36, 695-711 (2001).
8. M. Kamakura, Royalactin induces queen differentiation in honeybees. Nature 473,478-483 (2011).
9. S. Oldham, E. Hafen, Insulin/IGF and target of rapamycin signaling: A TOR de force in growth control. Trends Cell Biol. 13, 79-85 (2003).
10. A. Patel, M. K. Fondrk, O. Kaftanoglu, C. Emore, G. Hunt, K. Frederick, G. V. Amdam, The making of a queen: TOR pathway is a key player in diphenic caste development. PLOS One 2, e509 (2007).
11. F. Wolschin, N. S. Mutti, G. V. Amdam, Insulin receptor substrate influences female caste development in honeybees. Biol. Lett. 7, 112-115 (2011).
12. Y. Wang, S. V. Azevedo, K. Hartfelder, G. V. Amdam, Insulin-like peptides (AmILPI and AmlLP2) differentially affect female caste development in the honey bee (Apis mellifera L). J. Exp. Biol. 216, 4347-4357 (2013).
13. R. Kucharski, J. Maleszka, S. Foret, R. Maleszka, Nutritional control of reproductive status in honeybees via DNA methylation. Science 319, 1827-1830 (2008).
14. W. Mao, M. A. Schuler, M. R. Berenbaum, Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. Proc. Natl. Acad. Sci. U.S.A. 110, 8842-8846 (2013).
15. A. Link, F. Balaguer, A. Goel, Cancer chemoprevention by dietary polyphenols: Promising role for epigenetics. Biochem. Pharmacol. 80, 1771-1792 (2010).
16. A. Abbas, W. Patterson III, P. T. Georgel, The epigenetic potentials of dietary polyphenols in prostate cancer management. Biochem. Cell Biol. 91, 361-368 (2013).
17. B. Langmead, S. L. Salzberg, Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
18. M. D. Robinson, D.J. McCarthy, G. K. Smyth, edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
19. D. W. Huang, B. T. Sherman, R. A. Lempicki, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
20. D. W. Huang, B. T. Sherman, R. A. Lempicki, Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).
21. W. Luo, M. S. Friedman, K. Shedden, K. D. Hankenson, P. J. Woolf, GAGE: Generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 10, 161 (2009).
22. W. Luo, C. Brouwer, Pathview: An R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics 29, 1830-1831 (2013).
23. K. King-Jones, M. A. Horner, G. Lam, C. S. Thummel, The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila. Cell Metab. 4, 37-48 (2006).
24. N. S. Mutti, A. G. Dolezal, F. Wolschin, J. S. Mutti, K. S. Gill, G. V. Amdam, IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. J. Exp. Biol. 214, 3977-3984 (2011).
25. S. F. Pernal, R. W. Currie, Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.). Apidologie 31, 387-409 (2000).
26. W. Mao, S. G. Rupasinghe, R. M. Johnson, A. R. Zangerl, M. A. Schuler, M. R. Berenbaum, Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 154, 427-434 (2009).
27. W. Mao, M. A. Schuler, M. R. Berenbaum, CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proc. Natl. Acad. Sci. U.S.A. 108, 12657-12662 (2011).
28. R. M. Johnson, W. Mao, H. S. Pollock, G. Niu, M. A. Schuler, M. R. Berenbaum, Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLOS One 7, e31051 (2012).
29. R. C. Cameron, E. J. Duncan, P. K. Dearden, Biased gene expression in early honeybee larval development. BMC Genomics 14, 903 (2013).
30. K. Randolt, O. Gimple, J. Geissendorfer, J. Reinders, C. Prusko, M.J. Mueller, S. Albert, J. Tautz, H. Beier, Immune-related proteins induced in the hemolymph after aseptic and septic injury differ in honey bee worker larvae and adults. Arch. Insect Biochem. Physiol. 69, 155-167 (2008) .
31. Q. W. T. Chan, A. P. Melathopoulos, S. F. Pernal, L. J. Foster, The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics 10, 387 (2009) .
32. D. Woltedji, Y. Fang, B. Han, M. Feng, R. Li, X. Lu, J. Li, Proteome analysis of hemolymph changes during the larval to pupal development stages of honeybee workers (Apis meiiifera ligustica). J. Proteome Res. 12, 5189-5198 (2013).
33. M. R. Goll, T. H. Bestor, Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74, 481-514 (2005).
34. Y. Wang, M. Jorda, P. L.Jones, R. Maleszka, X. Ling, H. M. Robertson, C. A. Mizzen, M. A. Peinado, G. E. Robinson, Functional CpG methylation system in a social insect.Sc/ence314,645-647 (2006).
35. K. Kuszewska, M. Woyciechowski, Age at which larvae are orphaned determines their development into typical or rebel workers in the honeybee (Apis meiiifera L). PLOS One 10, e0123404 (2015).
36. H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, G. Marth, G. Abecasis, R. Durbin, The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).