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 United States of America

Volumn 108, Issue 37, 2011, Pages 15282-15287

  Jarosch, Antje ^a   Stolle, Eckart ^a   Crewe, Robin M ^b   Moritz, Robin F A ^a,b  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Caste determination; Cuticular protein 2 family; Gene expression

Indexed keywords

NUCLEOTIDE; RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GEMINI; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; DROSOPHILA; EXON; GENE DELETION; HONEYBEE; INTRON; KNOCKOUT GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FUNCTION; PARASITE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN BINDING; RNA INTERFERENCE; SEQUENCE HOMOLOGY; SEXUAL BEHAVIOR; WORKER (INSECT);

ALTERNATIVE SPLICING; ANIMALS; BEES; EXONS; FEMALE; GENE KNOCKDOWN TECHNIQUES; HIERARCHY, SOCIAL; INSECT PROTEINS; INTRONS; MODELS, GENETIC; PROTEIN ISOFORMS; REPRODUCTION; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; SEXUAL BEHAVIOR, ANIMAL; TRANSCRIPTION FACTORS;

APIS MELLIFERA; HEXAPODA;

EID: 80053081882     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1109343108     Document Type: Article

References (41)

1. Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7: 1-16.
2. Winston ML, Slessor KN (1998) Honeybee primer pheromones and colony organization: Gaps in our knowledge. Apidologie (Celle) 29:81-95. (Pubitemid 28163088)
3. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial hymenoptera. Am Nat 132:217-234.
4. Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247-254.
5. Sakagami SF (1958) The false-queen: Fourth adjustive response in dequeened honeybee colonies. Behaviour 13:280-296.
6. Onions GW (1912) South African "fertile-worker bees". S Afr Agric J 1:720-728.
7. Anderson RH (1963) The laying worker in the cape honey-bee Apis mellifera capensis. J Apic Res 2:85-92.
8. Neumann P, Hepburn HR, Radloff SE (2000) Modes of worker reproduction, reproductive dominance and brood cell construction in queenless honeybee (Apis mellifera l.) colonies. Apidologie (Celle) 31:479-486. (Pubitemid 30624738)
9. Crewe RM, Velthuis HHW (1980) False queens: A consequence of mandibular gland signals in worker honeybees. Naturwissenschaften 67:467-469.
10. Wossler TC (2002) Pheromone mimicry by Apis mellifera capensis social parasites leads to reproductive anarchy in host Apis mellifera scutellata colonies. Apidologie (Celle) 33:139-163.
11. Simon UE, Moritz RFA, Crewe RM (2001) The ontogenetic pattern of mandibular gland components in queenless worker bees (Apis mellifera capensis Esch.). J Insect Physiol 47:735-738. (Pubitemid 32489062)
12. Dietemann V, Neumann P, Härtel S, Pirk CWW, Crewe RM (2007) Pheromonal dominance and the selection of a socially parasitic honeybee worker lineage (Apis mellifera capensis Esch.). J Evol Biol 20:997-1007. (Pubitemid 46663122)
13. Malka O, Shnieor S, Hefetz A, Katzav-Gozansky T (2007) Reversible royalty in worker honeybees (Apis mellifera) under the queen influence. Behav Ecol Sociobiol 61: 465-473. (Pubitemid 44953019)
14. Greeff JM (1996) Effects of thelytokous worker reproduction on kin-selection and conflict in the cape honeybee, Apis mellifera capensis. Philos T Roy Soc B 351: 617-625.
15. Lattorff HMG, Moritz RFA, Fuchs S (2005) A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity 94: 533-537. (Pubitemid 40641176)
16. Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3:292-295.
17. Judice CC, et al. (2006) Gene expression profiles underlying alternative caste phenotypes in a highly eusocial bee, Melipona quadrifasciata. Insect Mol Biol 15:33-44.
18. Hoskins RA, et al. (2007) Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 316:1625-1628. (Pubitemid 46982037)
19. Giot L, et al. (2003) A protein interaction map of Drosophila melanogaster. Science 302:1727-1736. (Pubitemid 37505730)
20. Verma S, Ruttner F (1983) Cytological analysis of the thelytokous parthenogenesis in the cape honeybee (Apis mellifera capensis Escholtz). Apidology 14:41-57.
21. Kang HC, et al. (2005) Erythroid cell-specific alpha-globin gene regulation by the CP2 transcription factor family. Mol Cell Biol 25:6005-6020. (Pubitemid 40946554)
22. López AJ (1995) Developmental role of transcription factor isoforms generated by alternative splicing. Dev Biol 172:396-411.
23. Evans JD, Wheeler DE (2001) Expression profiles during honeybee caste determination. Genome Biol 2, 10.1186/gb-2000-2-1-research0001.
24. Grozinger CM, Fan Y, Hoover SER, Winston ML (2007) Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Mol Ecol 16:4837-4848. (Pubitemid 350135217)
25. 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)
26. Elango N, Hunt BG, Goodisman MAD, Yi SV (2009) DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc Natl Acad Sci USA 106:11206-11211.
27. Kamakura M (2011) Royalactin induces queen differentiation in honeybees. Nature 473:478-483.
28. Yoon JB, Li G, Roeder RG (1994) Characterization of a family of related cellular transcription factors which can modulate human immunodeficiency virus type 1 transcription in vitro. Mol Cell Biol 14:1776-1785. (Pubitemid 24074572)
29. Attardi LD, Tjian R (1993) Drosophila tissue-specific transcription factor NTF-1 contains a novel isoleucine-rich activation motif. Genes Dev 7(7B):1341-1353. (Pubitemid 23210883)
30. Pagani F, Stuani C, Zuccato E, Kornblihtt AR, Baralle FE (2003) Promoter architecture modulates CFTR exon 9 skipping. J Biol Chem 278:1511-1517. (Pubitemid 36801378)
31. Cramer P, Pesce CG, Baralle FE, Kornblihtt AR (1997) Functional association between promoter structure and transcript alternative splicing. Proc Natl Acad Sci USA 94: 11456-11460. (Pubitemid 27451020)
32. Lenasi T, Peterlin BM, Dovc P (2006) Distal regulation of alternative splicing by splicing enhancer in equine β-casein intron 1. RNA 12:498-507. (Pubitemid 43290876)
33. Hastings ML, Wilson CM, Munroe SH (2001) A purine-rich intronic element enhances alternative splicing of thyroid hormone receptor mRNA. RNA 7:859-874. (Pubitemid 32552873)
34. McCarthy EM, Phillips, JA, III (1998) Characterization of an intron splice enhancer that regulates alternative splicing of human GH pre-mRNA. Hum Mol Genet 7:1491-1496. (Pubitemid 28429931)
35. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406-3415.
36. Buratti E, Baralle FE (2004) Influence of RNA secondary structure on the pre-mRNA splicing process. Mol Cell Biol 24:10505-10514. (Pubitemid 39603113)
37. Hess G (1942) On the influence of the fertility of queenless and vitamin E on the ovaries of worker bees (Translated from German). Beih Schweiz Bienen Ztg 1:33-110.
38. Consortium HGS; Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949.
39. Scotto-Lavino E, Du G, Frohman MA (2006) 39 end cDNA amplification using classic RACE. Nat Protoc 1:2742-2745.
40. Scotto-Lavino E, Du G, Frohman MA (2006) 59 end cDNA amplification using classic RACE. Nat Protoc 1:2555-2562.
41. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.