Changes in the gene expression profiles of the hypopharyngeal gland of worker honeybees in association with worker behavior and hormonal factors

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Ueno, Takayuki ^a,b   Takeuchi, Hideaki ^a   Kawasaki, Kiyoshi ^b   Kubo, Takeo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b DOSHISHA WOMEN'S COLLEGE OF LIBERAL ARTS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ECDYSONE; ECDYSONE RECEPTOR; ECDYSTERONE; JUVENILE HORMONE; METHOPRENE; INSECT PROTEIN; MESSENGER RNA; TRANSCRIPTOME;

AGE; AMBUFFY GENE; AMMMP1 GENE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; E74 GENE; ECR GENE; EXOCRINE GLAND; GENE; GENE CONTROL; GENE EXPRESSION PROFILING; HBG3 GENE; HONEYBEE; HYPOPHARYNGEAL GLAND; HYPOPHARYNX; MBLK 1 GENE; MOLECULAR MECHANICS; MRJP2 GENE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TASK PERFORMANCE; WORKER (INSECT); ANIMAL; BEE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

APIS MELLIFERA; APOIDEA; BASIDIOMYCOTA;

ANIMALS; BEES; BEHAVIOR, ANIMAL; ECDYSONE; ECDYSTERONE; HYPOPHARYNX; INSECT PROTEINS; JUVENILE HORMONES; METHOPRENE; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84939151134     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130206     Document Type: Article

References (67)

1. Wilson EO. The insect societies. Cambridge, Massachusetts: Harvard university press; 1971.
2. Wheeler DE, Frederik Nijhout H. Soldier determination in Pheidole bicarinata: Effect of methoprene on caste and size within castes. Journal of Insect Physiology. 1983;29(11):847-54. http://dx.doi.org/10. 1016/0022-1910 (83) 90151-8
3. Miura T, Kamikouchi A, Sawata M, Takeuchi H, Natori S, Kubo T, et al. Soldier caste-specific gene expression in the mandibular glands of Hodotermopsis japonica (Isoptera: termopsidae). Proceedings of the National Academy of Sciences of the United States of America. 1999;96(24):13874-9. Epub 1999/11/26. PMID: 10570166; PubMed Central PMCID: PMC24158.
4. LeBoeuf AC, Benton R, Keller L. The molecular basis of social behavior: models, methods and advances. Current opinion in neurobiology. 2013;23(1):3-10. Epub 2012/09/22. doi: 10.1016/j.conb. 2012.08.008 PMID: 22995551.
5. Hartfelder K, Emlen DJ. Endocrine control of insect polyphenism. UK: Oxford; 2012. 464-522 p.
6. Winston ML. The biology of the honey bee. Cambridge, Massachusetts: Harvard university press; 1987. PMID: 17784300
7. Lindauer M. Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z Vergl Physiol. 1952;34(4):299-345. doi: 10.1007/bf00298048
8. Sakagami S. Untersuchungen uber die Arbeitsteilung in einen Zwergvolk der Honigbienen. Beitrage zur Biologie des Bienenvolkes, Apis mellifera L. I Jpn J Zool. 1953;11:117-85.
9. Sigg D, Thompson CM, Mercer AR. Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.). The Journal of neuroscience: the official journal of the Society for Neuroscience. 1997;17(18):7148-56. Epub 1997/09/15. PMID: 9278549.
10. Nilsen KA, Ihle KE, Frederick K, Fondrk MK, Smedal B, Hartfelder K, et al. Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology. The Journal of experimental biology. 2011;214(Pt 9):1488-97. Epub 2011/04/15. doi: 10.1242/jeb.050393 PMID: 21490257; PubMed Central PMCID: PMC3076075.
11. Robinson GE. Effects of a juvenile hormone analogue on honey bee foraging behaviour and alarm pheromone production. Journal of Insect Physiology. 1985;31(4):277-82. http://dx.doi.org/10.1016/0022-1910 (85) 90003-4
12. Kubo T, Sasaki M, Nakamura J, Sasagawa H, Ohashi K, Takeuchi H, et al. Change in the expression of hypopharyngeal-gland proteins of the worker honeybees (Apis mellifera L.) with age and/or role. Journal of biochemistry. 1996;119(2):291-5. Epub 1996/02/01. PMID: 8882720.
13. Sasagawa H, Sasaki M, Okada I. Hormonal control of the division of labor in adult honeybees (Apis mellifera L.) I. Effect of methopreneon corpora allata and hypopharyngeal gand, and its α-glucosidase activity. Appl Ent Zool 1989;24(1):66-77.
14. Ohashi K, Natori S, Kubo T. Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L. European journal of biochemistry/FEBS. 1997;249(3):797-802. Epub 1997/12/12. PMID: 9395329.
15. Ohashi K, Sawata M, Takeuchi H, Natori S, Kubo T. Molecular cloning of cDNA and analysis of expression of the gene for alpha-glucosidase from the hypopharyngeal gland of the honeybee Apis mellifera L. Biochemical and biophysical research communications. 1996;221(2):380-5. Epub 1996/04/16. doi: 10.1006/bbrc.1996.0604 PMID: 8619864.
16. Ohashi K, Natori S, Kubo T. Expression of amylase and glucose oxidase in the hypopharyngeal gland with an age-dependent role change of the worker honeybee (Apis mellifera L.). European journal of biochemistry/FEBS. 1999;265(1):127-33. Epub 1999/09/22. PMID: 10491166.
17. Hrassnigg N, Crailsheim K. Adaptation of hypopharyngeal gland development to the brood status of honeybee (Apis mellifera L.) colonies. J Insect Physiol. 1998;44(10):929-39. Epub 2003/05/29. PMID: 12770429.
18. Ohashi K, Sasaki M, Sasagawa H, Nakamura J, Natori S, Kubo T. Functional flexibility of the honey bee hypopharyngeal gland in a dequeened colony. Zoological science. 2000;17(8):1089-94. Epub 2008/06/05. doi: 10.2108/zsj.17.1089 PMID: 18522463.
19. Ueno T, Nakaoka T, Takeuchi H, Kubo T. Differential gene expression in the hypopharyngeal glands of worker honeybees (Apis mellifera L.) associated with an age-dependent role change. Zoological science. 2009;26(8):557-63. Epub 2009/09/02. doi: 10.2108/zsj.26.557 PMID: 19719408.
20. Robinson GE, Page RE Jr, Strambi C, Strambi A. Hormonal and genetic control of behavioral integration in honey bee colonies. Science. 1989;246(4926):109-12. Epub 1989/10/06. doi: 10.1126/science. 246.4926.109 PMID: 17837770.
21. Sullivan JP, Fahrbach SE, Robinson GE. Juvenile hormone paces behavioral development in the adult worker honey bee. Hormones and behavior. 2000;37(1):1-14. Epub 2000/03/14. doi: 10.1006/hbeh. 1999.1552 PMID: 10712853.
22. Rutz W, Gerig L, Wille H, Lüscher M. The function of juvenile hormone in adult worker honeybees, Apis mellifera. Journal of Insect Physiology. 1976;22(11):1485-91. http://dx.doi.org/10.1016/0022-1910 (76) 90214-6
23. Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, et al. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(17):7128-33. Epub 2007/04/18. doi: 10.1073/pnas.0701909104 PMID: 17438290; PubMed Central PMCID: PMC1852330.
24. Wang Y, Brent CS, Fennern E, Amdam GV. Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS genetics. 2012;8(6):e1002779. Epub 2012/07/05. doi: 10.1371/journal.pgen. 1002779 PMID: 22761585; PubMed Central PMCID: PMC3386229.
25. Toth AL, Kantarovich S, Meisel AF, Robinson GE. Nutritional status influences socially regulated foraging ontogeny in honey bees. The Journal of experimental biology. 2005;208(Pt 24):4641-9. Epub 2005/12/06. doi: 10.1242/jeb.01956 PMID: 16326945.
26. Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV. The gene vitellogenin has multiple coordinating effects on social organization. PLoS biology. 2007;5(3):e62. Epub 2007/03/08. doi: 10.1371/journal. pbio.0050062 PMID: 17341131; PubMed Central PMCID: PMC1808115.
27. Wang Y, Amdam GV, Rueppell O, Wallrichs MA, Fondrk MK, Kaftanoglu O, et al. PDK1 and HR46 gene homologs tie social behavior to ovary signals. PloS one. 2009;4(4):e4899. Epub 2009/04/03. doi: 10.1371/journal.pone.0004899 PMID: 19340296; PubMed Central PMCID: PMC2659776.
28. Wang Y, Kaftanoglu O, Siegel AJ, Page RE Jr, Amdam GV. Surgically increased ovarian mass in the honey bee confirms link between reproductive physiology and worker behavior. J Insect Physiol. 2010;56(12):1816-24. Epub 2010/08/07. doi: 10.1016/j.jinsphys.2010.07.013 PMID: 20688074.
29. Amdam GV, Page RE Jr, Fondrk MK, Brent CS. Hormone response to bidirectional selection on social behavior. Evolution & development. 2010;12(5):428-36. Epub 2010/10/05. doi: 10.1111/j.1525-142X. 2010.00429.x PMID: 20883212; PubMed Central PMCID: PMC2992874.
30. Wang Y, Kocher SD, Linksvayer TA, Grozinger CM, Page RE Jr, Amdam GV. Regulation of behaviorally associated gene networks in worker honey bee ovaries. The Journal of experimental biology. 2012;215(Pt 1):124-34. Epub 2011/12/14. doi: 10.1242/jeb.060889 PMID: 22162860; PubMed Central PMCID: PMC3233392.
31. Takeuchi H, Kage E, Sawata M, Kamikouchi A, Ohashi K, Ohara M, et al. Identification of a novel gene, Mblk-1, that encodes a putative transcription factor expressed preferentially in the large-type Kenyon cells of the honeybee brain. Insect molecular biology. 2001;10(5):487-94. Epub 2002/03/08. PMID: 11881813.
32. Paul RK, Takeuchi H, Matsuo Y, Kubo T. Gene expression of ecdysteroid-regulated gene E74 of the honeybee in ovary and brain. Insect molecular biology. 2005;14(1):9-15. Epub 2005/01/25. doi: 10. 1111/j.1365-2583.2004.00524.x PMID: 15663771.
33. Takeuchi H, Paul RK, Matsuzaka E, Kubo T. EcR-A expression in the brain and ovary of the honeybee (Apis mellifera L.). Zoological science. 2007;24(6):596-603. Epub 2007/09/18. doi: 10.2108/zsj.24.596 PMID: 17867861.
34. Yamazaki Y, Shirai K, Paul RK, Fujiyuki T, Wakamoto A, Takeuchi H, et al. Differential expression of HR38 in the mushroom bodies of the honeybee brain depends on the caste and division of labor. FEBS letters. 2006;580(11):2667-70. Epub 2006/05/02. doi: 10.1016/j.febslet.2006.04.016 PMID: 16647071.
35. Yamazaki Y, Kiuchi M, Takeuchi H, Kubo T. Ecdysteroid biosynthesis in workers of the European honeybee Apis mellifera L. Insect biochemistry and molecular biology. 2011;41(5):283-93. Epub 2011/02/01. doi: 10.1016/j.ibmb.2011.01.005 PMID: 21277979.
36. Lee CY, Wendel DP, Reid P, Lam G, Thummel CS, Baehrecke EH. E93 directs steroid-triggered programmed cell death in Drosophila. Molecular cell. 2000;6(2):433-43. Epub 2000/09/13. PMID: 10983989.
37. Yin VP, Thummel CS. Mechanisms of steroid-triggered programmed cell death in Drosophila. Seminars in cell & developmental biology. 2005;16(2):237-43. Epub 2005/03/31. doi: 10.1016/j.semcdb.2004. 12.007 PMID: 15797834.
38. Hartfelder K, Bitondi MMG, Santana WC, Simões ZLP. Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? Insect biochemistry and molecular biology. 2002;32(2):211-6. http://dx.doi.org/10.1016/S0965-1748 (01) 00100-XPMID: 11755066
39. Lee CY, Clough EA, Yellon P, Teslovich TM, Stephan DA, Baehrecke EH. Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Current biology: CB. 2003;13(4):350-7. Epub 2003/02/21. PMID: 12593803.
40. Petryk A, Warren JT, Marques G, Jarcho MP, Gilbert LI, Kahler J, et al. Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(24):13773-8. Epub 2003/11/12. doi: 10.1073/pnas.2336088100 PMID: 14610274; PubMed Central PMCID: PMC283497.
41. Rachinsky A, Strambi C, Strambi A, Hartfelder K. Caste and metamorphosis: hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. General and comparative endocrinology. 1990;79(1):31-8. Epub 1990/07/01. PMID: 2354779.
42. Koelle MR, Talbot WS, Segraves WA, Bender MT, Cherbas P, Hogness DS. The Drosophila EcR gene encodes an ecdysone receptor, a new member of the steroid receptor superfamily. Cell. 1991;67(1):59-77. Epub 1991/10/04. PMID: 1913820.
43. Baehrecke EH, Thummel CS. The Drosophila E93 gene from the 93F early puff displays stage- and tissuespecific regulation by 20-hydroxyecdysone. Developmental biology. 1995;171(1):85-97. Epub 1995/09/01. doi: 10.1006/dbio.1995.1262 PMID: 7556910.
44. Ashok M, Turner C, Wilson TG. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proceedings of the National Academy of Sciences of the United States of America. 1998;95(6):2761-6. Epub 1998/04/18. PMID: 9501163; PubMed Central PMCID: PMC19642.
45. Konopova B, Jindra M. Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(25):10488-93. Epub 2007/06/01. doi: 10.1073/pnas. 0703719104 PMID: 17537916; PubMed Central PMCID: PMC1965540.
46. Minakuchi C, Namiki T, Shinoda T. Kruppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Developmental biology. 2009;325(2):341-50. Epub 2008/11/18. doi: 10.1016/j.ydbio. 2008.10.016 PMID: 19013451.
47. Miura K, Oda M, Makita S, Chinzei Y. Characterization of the Drosophila Methoprene-tolerant gene product. Juvenile hormone binding and ligand-dependent gene regulation. The FEBS journal. 2005;272(5):1169-78. Epub 2005/02/22. doi: 10.1111/j.1742-4658.2005.04552.x PMID: 15720391.
48. Parthasarathy R, Tan A, Palli SR. bHLH-PAS family transcription factor methoprene-tolerant plays a key role in JH action in preventing the premature development of adult structures during larval-pupal metamorphosis. Mechanisms of development. 2008;125(7):601-16. Epub 2008/05/03. doi: 10.1016/j. mod.2008.03.004 PMID: 18450431; PubMed Central PMCID: PMC2486318.
49. Schuh R, Aicher W, Gaul U, Cote S, Preiss A, Maier D, et al. A conserved family of nuclear proteins containing structural elements of the finger protein encoded by Kruppel, a Drosophila segmentation gene. Cell. 1986;47(6):1025-32. Epub 1986/12/26. PMID: 3096579.
50. Wilson TG, Fabian J. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Developmental biology. 1986;118(1):190-201. Epub 1986/11/01. PMID: 3095161.
51. Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE. Influence of gene action across different time scales on behavior. Science. 2002;296(5568):741-4. Epub 2002/04/27. doi: 10.1126/science. 1069911 PMID: 11976457.
52. Whitfield CW, Cziko AM, Robinson GE. Gene expression profiles in the brain predict behavior in individual honey bees. Science. 2003;302(5643):296-9. Epub 2003/10/11. doi: 10.1126/science.1086807 PMID: 14551438.
53. Lehman HK, Schulz DJ, Barron AB, Wraight L, Hardison C, Whitney S, et al. Division of labor in the honey bee (Apis mellifera): the role of tyramine beta-hydroxylase. The Journal of experimental biology. 2006;209(Pt 14):2774-84. Epub 2006/07/01. doi: 10.1242/jeb.02296 PMID: 16809468.
54. Mutti NS, Wang Y, Kaftanoglu O, Amdam GV. Honey bee PTEN-description, developmental knockdown, and tissue-specific expression of splice-variants correlated with alternative social phenotypes. PloS one. 2011;6(7):e22195. Epub 2011/07/23. doi: 10.1371/journal.pone.0022195 PMID: 21779392; PubMed Central PMCID: PMC3136494.
55. Mello TR, Aleixo AC, Pinheiro DG, Nunes FM, Bitondi MM, Hartfelder K, et al. Developmental regulation of ecdysone receptor (EcR) and EcR-controlled gene expression during pharate-adult development of honeybees (Apis mellifera). Frontiers in genetics. 2014;5:445. Epub 2015/01/08. doi: 10.3389/fgene. 2014.00445 PMID: 25566327; PubMed Central PMCID: PMC4273664.
56. Velarde RA, Robinson GE, Fahrbach SE. Coordinated responses to developmental hormones in the Kenyon cells of the adult worker honey bee brain (Apis mellifera L.). J Insect Physiol. 2009;55(1):59-69. Epub 2008/11/18. doi: 10.1016/j.jinsphys.2008.10.006 PMID: 19013465.
57. Bozic J, Woodring J. Variation in JH synthesis rate in mature honeybees and its possible role in reprogramming of hypopharyngeal gland function. Pflugers Archiv: European journal of physiology. 2000;439(3 Suppl):R163-4. Epub 2000/02/01. PMID: 10653178.
58. Pinto LZ, Hartfelder K, Bitondi MM, Simoes ZL. Ecdysteroid titers in pupae of highly social bees relate to distinct modes of caste development. J Insect Physiol. 2002;48(8):783-90. Epub 2003/05/29. PMID: 12770056.
59. Soares MP, Elias-Neto M, Simoes ZL, Bitondi MM. A cuticle protein gene in the honeybee: expression during development and in relation to the ecdysteroid titer. Insect biochemistry and molecular biology. 2007;37(12):1272-82. Epub 2007/10/31. doi: 10.1016/j.ibmb.2007.07.014 PMID: 17967346.
60. Robinson GE, Vargo EL. Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioral pacemaker. Archives of insect biochemistry and physiology. 1997;35(4):559-83. Epub 1997/01/01. doi: 10.1002/(SICI) 1520-6327 (1997) 35:4<559::AID-ARCH13>3.0. CO;2-9 PMID: 9210289.
61. Hartfelder K. Insect juvenile hormone: from "status quo" to high society. Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas/Sociedade Brasileira de Biofisica [et al]. 2000;33(2):157-77. Epub 2000/02/05. PMID: 10657056.
62. Jianke Li MF, Zhaohui Zhang, Yinghong Pan. Identification of the proteome complement of hypopharyngeal glands from two strains of honeybees (Apis mellifera). Apidologie. 2008;39:199-214. doi: 10. 1051/apido:2007059
63. Burtis KC, Thummel CS, Jones CW, Karim FD, Hogness DS. The Drosophila 74EF early puff contains E74, a complex ecdysone-inducible gene that encodes two ets-related proteins. Cell. 1990;61(1):85-99. Epub 1990/04/06. PMID: 2107982.
64. Sun G, Zhu J, Li C, Tu Z, Raikhel AS. Two isoforms of the early E74 gene, an Ets transcription factor homologue, are implicated in the ecdysteroid hierarchy governing vitellogenesis of the mosquito, Aedes aegypti. Molecular and cellular endocrinology. 2002;190(1-2):147-57. Epub 2002/05/09. PMID: 11997188.
65. Sekimoto T, Iwami M, Sakurai S. 20-Hydroxyecdysone regulation of two isoforms of the Ets transcription factor E74 gene in programmed cell death in the silkworm anterior silk gland. Insect molecular biology. 2007;16(5):581-90. Epub 2007/09/27. doi: 10.1111/j.1365-2583.2007.00751.x PMID: 17894557.
66. Danforth BN, Ji S. Elongation factor-1 alpha occurs as two copies in bees: implications for phylogenetic analysis of EF-1 alpha sequences in insects. Molecular biology and evolution. 1998;15(3):225-35. Epub 1998/03/21. PMID: 9501490.
67. Ben-Shahar Y, Leung HT, Pak WL, Sokolowski MB, Robinson GE. cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. The Journal of experimental biology. 2003;206(Pt 14):2507-15. Epub 2003/06/11. PMID: 12796464.