A chromatin link to caste identity in the carpenter ant Camponotus floridanus

Genome Research

Volumn 23, Issue 3, 2013, Pages 486-496

  Simola, Daniel F ^a,b,c,d,f   Ye, Chaoyang ^a,e   Mutti, Navdeep S ^a,f   Doleza, Kelly ^a,b   Bonasio, Roberto ^c   Liebig, Jürgen ^b   Reinberg, Danny ^c   Berger, Shelley L ^a,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^f DUPONT COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE;

ANT; ARTICLE; BINDING AFFINITY; BINDING SITE; CAMPONOTUS FLORIDANUS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; ENHANCER REGION; GENE CONTROL; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; HISTONE ACETYLATION; HISTONE MODIFICATION; INSECT CASTE; INSECT DEVELOPMENT; LARVA; LARVAL DEVELOPMENT; MUSCLE DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOCIAL BEHAVIOR;

ACETYLATION; ANIMALS; ANTS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; EPIGENESIS, GENETIC; EXPRESSED SEQUENCE TAGS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; GENETIC LOCI; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HISTONES; LARVA; MALE; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE ANALYSIS, DNA; SOCIAL BEHAVIOR;

EID: 84874585430     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.148361.112     Document Type: Article

References (57)

1. Alarcón JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, Barco A. 2004. Chromatin acetylation, memory, and LTP are impaired in CBP+/-mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42: 947-959. (Pubitemid 38798233)
2. Amberg DC, Burke DJ, Strathern JN. 2000. Methods in yeast genetics: A Cold Spring Harbor laboratory course manual, pp. 149-154. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
3. Ament SA, Corona M, Pollock HS, Robinson GE. 2008. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc Natl Acad Sci 105: 4226-4231. (Pubitemid 351754362)
4. Bantignies F, Goodman RH, Smolik SM. 2000. Functional interaction between the coactivator Drosophila CREB-binding protein and ASH1, a member of the trithorax group of chromatin modifiers. Mol Cell Biol 20: 9317-9330. (Pubitemid 32246116)
5. Bejarano F, Busturia A. 2004. Function of the trithorax-like gene during Drosophila development. Dev Biol 268: 327-341. (Pubitemid 38519847)
6. Berger SL. 1999. Gene activation by histone and factor acetyltransferases. Curr Opin Cell Biol 11: 336-341. (Pubitemid 29273804)
7. Berger SL. 2007. The complex language of chromatin regulation during transcription. Nature 447: 407-412. (Pubitemid 46816746)
8. Bonasio R, Zhang G, Ye C, Mutti NS, Fang X, Qin N, Donahue G, Yang P, Li Q, Li C, et al. 2010. Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068-1071.
9. Bonasio R, Li Q, Lian J, Mutti NS, Jin L, Zhao H, Zhang P, Wen P, Xiang H, Ding Y, et al. 2012. Genome-wide and caste-specificDNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr Biol 22: 1755-1764.
10. Borah JC, Mujtaba S, Karakikes I, Zeng L, Muller M, Patel J, Moshkina N, Morohashi K, Zhang W, Gerona-Navaroo G, et al. 2011. A small molecule binding to the coactivator creb-binding protein blocks apoptosis in cardiomyocytes. Chem Biol 18: 531-541.
11. CoronaM, Velarde RA, Remolina S,Moran-Lauter A,Wang Y, Hughes KA, Robinson GE. 2007. Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci 104: 7128-7133. (Pubitemid 47186020)
12. Dupuy F, Sandoz JC, Giurfa M, Josens MR. 2006. Individual olfactory learning in Camponotus ants. Anim Behav 72: 1081-1091. (Pubitemid 44634367)
13. Elango N, Hunt BG, Goodisman MA, Yi SV. 2009. DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc Natl Acad Sci 106: 11206-11211.
14. Evans JD, Wheeler DE. 2001. Gene expression and the evolution of insect polyphenisms. Bioessays 23: 62-68. (Pubitemid 32100502)
15. Ferguson-Smith AC. 2012. Genomic imprinting: The emergence of an epigenetic paradigm. Nat Rev Genet 12: 565-575.
16. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O, Morse EM, Keates T, Hickman TT, Felletar I, et al. 2010. Selective inhibition of BET bromodomains. Nature 468: 1067-1073.
17. Gadau J, Helmkampf M, Nygaard S, Roux J, Simola DF, Smith CR, Suen G, Wurm Y, Smith CD. 2012. The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet 28: 14-21.
18. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
19. Holldobler B, Wilson EO. 1990. The ants. The Belknap Press of Harvard University Press, Cambridge, M.A.
20. Jin Q, Yu LR,Wang L, Zhang Z, Kasper LH, Lee JE,Wang C, Brindle PK, Dent SY, Ge K. 2011. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J 30: 249-262.
21. Kamakura M. 2011. Royalactin induces queen differentiation in honeybees. Nature 473: 478-483.
22. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. 2010. Widespread transcription at neuronal activity-related enhancers. Nature 465: 182-187.
23. Kucharski R, Maleszka J, Foret S, Maleszka R. 2008. Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827-1830. (Pubitemid 351451590)
24. Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SG, Green MR, Goodman RH. 1994. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370: 223-226. (Pubitemid 24236779)
25. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
26. Larschan E, Bishop EP, Kharchenko PV, Core LJ, Lis JT, Park PJ, Kuroda MI. 2011. X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature 471: 115-118.
27. Levenson JM, Sweatt JD. 2005. Epigenetic mechanisms in memory formation. Nat Rev Neurosci 6: 108-118. (Pubitemid 40188945)
28. Lucas C, Sokolowski MB. 2009. Molecular basis for changes in behavioral state in ant social behaviors. Proc Natl Acad Sci 106: 6351-6356.
29. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. 2010. The honey bee epigenomes: Differential methylation of brain DNA in queens and workers. PLoS Biol 8: e1000506.
30. Montooth KL, Marden JH, Clark AG. 2003. Mapping determinants of variation in energy metabolism, respiration and flight in Drosophila. Genetics 165: 623-635. (Pubitemid 37337630)
31. Mutti NS, Dolezal AG, Wolschin F, Mutti JS, Gill KS, Amdam GV. 2011. IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. J Exp Biol 214: 3977-3984.
32. Négre N, Lavrov S, Hennetin J, Bellis M, Cavalli G. 2006. Mapping the distribution of chromatin proteins by ChIP on chip. Methods Enzymol 410: 316-341. (Pubitemid 44287012)
33. Négre N, Brown CD, Ma L, Bristow CA, Miller SW,Wagner U, Kheradpour P, Eaton ML, Loriaux P, Sealfon R, et al. 2011. A cis-regulatory map of the Drosophila genome. Nature 471: 527-531.
34. Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV. 2007. The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5: e62.
35. Nijhout HF. 1999. Control mechanisms of polyphenic development in insects. Bioscience 49: 181-192.
36. Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, Cota P, Wittnam JL, Gogol-Doering A, Opitz L, et al. 2010. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 7: 753-756.
37. Petruk S, Sedkov Y, Smith S, Tillib S, Kraevski V, Nakamura T, Canaani E, Croce CM, Mazo A. 2001. Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene. Science 294: 1331-1334. (Pubitemid 33063097)
38. Poux S, Horard B, Sigrist CJ, Pirrotta V. 2002. The Drosophila Trithorax protein is a coactivator required to prevent reestablishment of Polycomb silencing. Development 129: 2483-2493. (Pubitemid 34863854)
39. Rajakumar R, San Mauro D, Dijkstra MB, Huang MH, Wheeler DE, Hiou-Tim F, Khila A, Cournoyea M, Abouheif E. 2012. Ancestral developmental potential facilitates parallel evolution in ants. Science 335: 79-82.
40. Ringrose L, Paro R. 2007. Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134: 223-232.
41. Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L. 2011. Integrative epigenomicmapping defines four main chromatin states in Arabidopsis. EMBO J 30: 1928-1938.
42. Schones DE, Cui K, Cuddapah S, Roh TY, Barski A, Wang Z, Wei G, Zhao K. 2008. Dynamic regulation of nucleosome positioning in the human genome. Cell 132: 887-898. (Pubitemid 351312809)
43. Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L. 2010. Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25: 275-282.
44. Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV. 2006. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci 103: 962-967. (Pubitemid 43212204)
45. Simola DF, Kim J. 2011. Sniper: Improved SNP discovery by multiply mapping deep sequenced reads. Genome Biol 12: R55.
46. Smith CR, Toth AL, Suarez AV, Robinson GE. 2008. Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9: 735-748.
47. Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB, Zhou YY, Li J, Castellano S, Sbardella G, Issa JP, et al. 2011. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep 12: 238-243.
48. Stearns SC. 1989. The evolutionary significance of phenotypic plasticity. Bioscience 39: 436-445.
49. Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, Diaz MO, Scacheri PC, Harte PJ. 2009. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136: 3131-3141.
50. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
51. Valentine JW, Collins AG, Meyer CP. 1994. Morphological complexity increase in metazoans. Paleobiol 20: 131-142. (Pubitemid 2114088)
52. Waltzer L, Bienz L. 1999. A function of CBP as a transcriptional co-activator during Dpp signalling. EMBO J 18: 1630-1641. (Pubitemid 29127075)
53. West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford University Press, Oxford, New York.
54. Wheeler DE. 1986. Developmental and physiological determinants of caste in social Hymenoptera: Evolutionary implications. Am Nat 128: 13-34.
55. Wheeler DE. 1991. The developmental basis of worker caste polymorphism in ants. Am Nat 138: 1218-1238.
56. Wilson EO. 1953. The origin and evolution of polymorphism in ants. Q Rev Biol 28: 136-156.
57. Zeng PY, Vakoc CR, Chen ZC, Blobel GA, Berger SL. 2006. In vivo dual crosslinking for identification of indirect DNA-associated proteins by chromatin immunoprecipitation. Biotechniques 41: 694-698. (Pubitemid 46534851)