Nutrigenomics in honey bees: Digital gene expression analysis of pollen's nutritive effects on healthy and varroa-parasitized bees

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Alaux, Cédric ^a   Dantec, Christelle ^b   Parrinello, Hughes ^b   Le Conte, Yves ^a  

^a Laboratoire de Toxicologie Environnementale   (France)

^b INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; VITELLOGENIN; ANTIMICROBIAL CATIONIC PEPTIDE; CARBOHYDRATE; TARGET OF RAPAMYCIN KINASE;

ARTICLE; CONTROLLED STUDY; DIGITAL GENE EXPRESSION ANALYSIS; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE NUMBER; HONEYBEE; LIPID METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIGENOMICS; OXIDATIVE PHOSPHORYLATION; PARASITISM; POLLEN; PROTEIN DEGRADATION; PROTEIN METABOLISM; SUGAR INTAKE; UPREGULATION; VARROA; VIRUS VIRULENCE; ABDOMEN; ANIMAL; BEE; GENETICS; IMMUNOLOGY; LONGEVITY; METABOLISM; PARASITOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; VARROIDAE;

ACARI; ANIMALIA; APIS MELLIFERA; APOIDEA; VARROA; VARROA DESTRUCTOR;

ABDOMEN; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; BEES; CARBOHYDRATES; LONGEVITY; NUTRIGENOMICS; POLLEN; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSCRIPTOME; VARROIDAE;

EID: 80053604381     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-496     Document Type: Article

References (74)

1. Lopez-Maury L, Marguerat S, Bahler J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat Rev Genet 2008, 9(8):583-593.
2. Grewal SS. Insulin/TOR signaling in growth and homeostasis: a view from the fly world. Int J Biochem Cell Biol 2009, 41(5):1006-1010. 10.1016/j.biocel.2008.10.010, 18992839.
3. Field CJ, Johnson IR, Schley PD. Nutrients and their role in host resistance to infection. J Leukoc Biol 2002, 71:16-32.
4. Li P, Yin YL, Li D, Kim SW, Wu G. Amino acids and immune function. Brit J Nutr 2007, 98:237-252. 10.1017/S000711450769936X, 17403271.
5. Kaput J, Rodriguez RL. Nutritional genomics: the next frontier in the postgenomic era. Physiol Genomics 2004, 16(2):166-177.
6. Müller M, Kersten S. Nutrigenomics: goals and strategies. Nat Rev Genet 2003, 4(4):315-322. 10.1038/nrg1047, 12671662.
7. Brodschneider R, Crailsheim K. Nutrition and health in honey bees. Apidologie 2010, 41:278-294.
8. Honey Bee Genome Sequencing Consortium Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443:931-949. 10.1038/nature05260, 2048586, 17073008, Honey Bee Genome Sequencing Consortium.
9. Roulston TH, Buchmann SL. A phylogenetic reconsideration of the pollen starch-pollination correlation. Evol Ecol Res 2000, 2:627-643.
10. Roulston TH, Cane JH. Pollen nutritional content and digestibility for animals. Plant Syst Evol 2000, 222:187-209.
11. Stanley RG, Linskens HF. Pollen: Biology, biochemistry, management. 1974, Heidelberg, Germany: Springer.
12. Haydak MH. Honey bee nutrition. Annu Rev Entomol 1970, 15:143-156.
13. Wahl O, Ulm K. Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia 1983, 59:106-128.
14. Rinderer TE, Elliott KD. Worker honey bee response to infection with Nosema apis. J Econ Entomol 1977, 70:431-433.
15. Rinderer TE, Rothenbuhler WC, Gochnauer TA. The influence of pollen on the susceptibility of honey-bee larvae to Bacillus larvae. J Invertebr Pathol 1974, 23:347-350. 10.1016/0022-2011(74)90100-1, 4833177.
16. Degrandi-Hoffman G, Chen Y, Huang E, Huang MH. The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). J Insect Physiol 2010, 56:1184-1191. 10.1016/j.jinsphys.2010.03.017, 20346950.
17. Alaux C, Ducloz F, Crauser D, Le Conte Y. Diet effects on honeybee immunocompetence. Biol Lett 2010, 6:562-565. 10.1098/rsbl.2009.0986, 2936196, 20089536.
18. Sammataro D, Gerson U, Needham G. Parasitic mites of honey bees: life history, implications, and impact. Annu Rev Entomol 2000, 45:519-548. 10.1146/annurev.ento.45.1.519, 10761588.
19. Bowen-Walker PL, Martin SJ, Gunn A. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J Invertebr Pathol 1999, 73:101-106. 10.1006/jipa.1998.4807, 9878295.
20. Bowen-Walker PL, Gunn A. The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomol Exp Appl 2001, 101:207-217.
21. Yang X, Cox-Foster DL. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci USA 2005, 102(21):7470-7475. 10.1073/pnas.0501860102, 1140434, 15897457.
22. Zhang Y, Liu X, Zhang W, Han R. Differential gene expression of the honey bees Apis mellifera and A. cerana induced by Varroa destructor infection. J Insect Physiol 2010, 56(9):1207-1218. 10.1016/j.jinsphys.2010.03.019, 20346951.
23. Navajas M, Migeon A, Alaux C, Martin-Magniette M, Robinson G, Evans J, Cros-Arteil S, Crauser D, Le Conte Y. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 2008, 9:301. 10.1186/1471-2164-9-301, 2447852, 18578863.
24. Anisimov SV. Serial Analysis of Gene Expression (SAGE): 13 years of application in research. Curr Pharm Biotechnol 2008, 9(5):338-350. 10.2174/138920108785915148, 18855686.
25. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 2008, 18(9):1509-1517. 10.1101/gr.079558.108, 2527709, 18550803.
26. 't Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, de Menezes RX, Boer JM, van Ommen GJ, den Dunnen JT. Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 2008, 36:e141. 10.1093/nar/gkn705, 2588528, 18927111.
27. Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM, van Oers MM. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J Gen Virol 2004, 85(Pt 12):3747-3755.
28. Fujiyuki T, Ohka S, Takeuchi H, Ono M, Nomoto A, Kubo T. Prevalence and phylogeny of Kakugo virus, a novel insect picorna-like virus that infects the honeybee (Apis mellifera L.), under various colony conditions. J Virol 2006, 80(23):11528-11538. 10.1128/JVI.00754-06, 1642587, 16971448.
29. Liu F, Li W, Li Z, Zhang S, Chen S, Su S. High-abundance mRNAs in Apis mellifera: comparison between nurses and foragers. J Insect Physiol 2011, 57:(274-279). 10.1016/j.jinsphys.2010.11.015, 21115016.
30. Wang XW, Luan JB, Li JM, Bao YY, Zhang CX, Liu SS. De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 2010, 11:400. 10.1186/1471-2164-11-400, 2898760, 20573269.
31. Wang Z, Dong D, Ru B, Young RL, Han N, Guo T, Zhang S. Digital gene expression tag profiling of bat digits provides robust candidates contributing to wing formation. BMC Genomics 2010, 11:619. 10.1186/1471-2164-11-619, 3017863, 21054883.
32. Alaux C, Le Conte Y, Adams HA, Rodriguez-Zas S, Grozinger CM, Sinha S, Robinson GE. Regulation of brain gene expression in honey bees by brood pheromone. Genes Brain Behav 2009, 8(3):309-319. 10.1111/j.1601-183X.2009.00480.x, 19220482.
33. Engels E. Occurrence and significance of vitellogenins in female castes of social Hymenoptera. Am Zool 1974, 14:1229-1237.
34. Tanaka ED, Hartfelder K. The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Struct Dev 2004, 33(4):431-442. 10.1016/j.asd.2004.06.006, 18089049.
35. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci USA 2007, 104(17):7128-7133. 10.1073/pnas.0701909104, 1852330, 17438290.
36. Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci USA 2006, 103(4):962-967. 10.1073/pnas.0502681103, 1347965, 16418279.
37. Bitondi MMG, Simões ZLP. The relationship between level of pollen in the diet, vitellogenin and juvenile hormone titres in Africanized Apis mellifera workers. J Apic Res 1996, 35:27-36.
38. Amdam GV, Hartfelder K, Norberg K, Hagen A, Omholt SW. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering?. J Econ Entomol 2004, 97:741-747. 10.1603/0022-0493(2004)097[0741:APIWHB]2.0.CO;2, 15279246.
39. Orgad S, Nelson H, Segal D, Nelson N. Metal ions suppress the abnormal taste behavior of the Drosophila mutant malvolio. J Exp Biol 1998, 201(Pt 1):115-120.
40. Ben-Shahar Y, Dudek NL, Robinson GE. Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor. J Exp Biol 2004, 207(Pt 19):3281-3288.
41. Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U, Gmeinbauer R, Schöffmann B. Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. J Insect Physiol 1992, 38:409-419.
42. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 2006, 15:645-656. 10.1111/j.1365-2583.2006.00682.x, 1847501, 17069638.
43. Pernal SF, Currie RW. Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.). Apidologie 2000, 31:387-409.
44. Garedew A, Schmolz E, Lamprecht I. The energy and nutritional demand of the parasitic life of the mite Varroa destructor. Apidologie 2004, 35:419-430.
45. de Groot AP. Protein and amino acid requirements of the hone y bee (Apis mellifica L.). Physiol Comp Oecol 1953, 3:197-285.
46. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Leopold P. A nutrient sensor mechanism controls Drosophila growth. Cell 2003, 114(6):739-749. 10.1016/S0092-8674(03)00713-X, 14505573.
47. Oldham S, Hafen E. Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol 2003, 13(2):79-85. 10.1016/S0962-8924(02)00042-9, 12559758.
48. Münch D, Amdam GV. The curious case of aging plasticity in honey bees. FEBS Lett 2010, 584(12):2496-2503. 10.1016/j.febslet.2010.04.007, 20385132.
49. Wang Y, Amdam GV, Rueppell O, Wallrichs M, Fondrk MK, Kaftanoglu O, Page REJ. PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS ONE 2009, 4:e4899. 10.1371/journal.pone.0004899, 2659776, 19340296.
50. Ament SA, Corona M, Pollock HS, Robinson GE. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc Natl Acad Sci USA 2008, 105:4226-4231. 10.1073/pnas.0800630105, 2393790, 18337502.
51. Wang Y, Mutti NS, Ihle KE, Siegel A, Dolezal AG, Kraftanoglu O, Amdam GV. Down-regulation of honeybee IRS gene biases behavior toward food rich in protein. PLoS Genet 2010, 6:e1000896. 10.1371/journal.pgen.1000896, 2848551, 20369023.
52. Amdam GV. Social context, stress, and plasticity of aging. Aging Cell 2011, 10(1):18-27. 10.1111/j.1474-9726.2010.00647.x, 21070589.
53. Hennig KM, Colombani J, Neufeld TP. TOR coordinates bulk and targeted endocytosis in the Drosophila melanogaster fat body to regulate cell growth. J Cell Biol 2006, 173(6):963-974. 10.1083/jcb.200511140, 1950482,1950482, 16785324.
54. Li L, Edgar BA, Grewal SS. Nutritional control of gene expression in Drosophila larvae via TOR, Myc and a novel cis-regulatory element. BMC Cell Biol 2010, 11:7. 10.1186/1471-2121-11-7, 2827378, 20089194.
55. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004, 18(16):1926-1945. 10.1101/gad.1212704, 15314020.
56. Grewal SS, Evans JR, Edgar BA. Drosophila TIF-IA is required for ribosome synthesis and cell growth and is regulated by the TOR pathway. J Cell Biol 2007, 179:1105-1113. 10.1083/jcb.200709044, 2140016, 18086911.
57. Guertin DA, Guntur KV, Bell GW, Thoreen CC, Sabatini DM. Functional genomics identifies TOR-regulated genes that control growth and division. Curr Biol 2006, 16(10):958-970. 10.1016/j.cub.2006.03.084, 16713952.
58. Tiefenbock SK, Baltzer C, Egli NA, Frei C. The Drosophila PGC-1 homologue Spargel coordinates mitochondrial activity to insulin signalling. Embo J 2009, 29(1):171-183. 2808377, 19910925.
59. Baltzer C, Tiefenbock SK, Marti M, Frei C. Nutrition controls mitochondrial biogenesis in the Drosophila adipose tissue through Delg and cyclin D/Cdk4. PLoS ONE 2009, 4(9):e6935. 10.1371/journal.pone.0006935, 2735006, 19742324.
60. Schneider P, Drescher W. The influence of Varroa jacobsoni Oud. on weight, development of weight and hypopharyngeal glands, and longevity of Apis mellifera L. Apidologie 1987, 18:101-110.
61. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 2009, 4:44-57.
62. Martin D, Brun C, Remy E, Mouren P, Thieffry D, Jacq B. GOToolBox: functional analysis of gene datasets based on Gene Ontology. Genome Biol 2004, 5(12):R101. 10.1186/gb-2004-5-12-r101, 545796, 15575967.
63. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 2004, 14(10):885-890. 10.1016/j.cub.2004.03.059, 2754830, 15186745.
64. Corona M, Hughes KA, Weaver DB, Robinson GE. Gene expression patterns associated with queen honey bee longevity. Mech Ageing Dev 2005, 126(11):1230-1238. 10.1016/j.mad.2005.07.004, 16139867.
65. Sun J, Tower J. FLP recombinase-mediated induction of Cu/Zn-superoxide dismutase transgene expression can extend the life span of adult Drosophila melanogaster flies. Mol Cell Biol 1999, 19(1):216-228. 83880, 9858546.
66. Orr WC, Mockett RJ, Sohal RS. Overexpression of glutathione reductase extends survival in transgenic Drosophila melanogaster under hyperoxia but not normoxia. Faseb J 1999, 13(13):1733-1742.
67. Woodward B. Protein, calories, and immune defenses. Nutr Rev 1998, 56(1 Pt 2):S84-92.
68. Lee KP, Simpson SJ, Wilson K. Dietary protein-quality influences melanization and immune function in an insect. Funct Ecol 2008, 22:1052-1061.
69. Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Biol Sci 2006, 273(1588):823-829.
70. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86(6):973-983. 10.1016/S0092-8674(00)80172-5, 8808632.
71. Yue C, Schroder M, Gisder S, Genersch E. Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol 2007, 88(Pt 8):2329-2336.
72. Vizioli J, Salzet M. Antimicrobial peptides from animals: focus on invertebrates. Trends Pharmacol Sci 2002, 23(11):494-496. 10.1016/S0165-6147(02)02105-3, 12413797.
73. Fievet J, Tentcheva D, Gauthier L, de Miranda J, Cousserans F, Colin ME, Bergoin M. Localization of deformed wing virus infection in queen and drone Apis mellifera L. Virol J 2006, 3:16. 10.1186/1743-422X-3-16, 1475838, 16569216.
74. Bradford JR, Hey Y, Yates T, Li Y, Pepper SD, Miller CJ. A comparison of massively parallel nucleotide sequencing with oligonucleotide microarrays for global transcription profiling. BMC Genomics 2010, 11:282. 10.1186/1471-2164-11-282, 2877694, 20444259.