The dice of fate: The csd gene and how its allelic composition regulates sexual development in the honey bee, Apis mellifera

BioEssays

Volumn 26, Issue 10, 2004, Pages 1131-1139

  Beye, Martin ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; COMPLEMENTARY SEX DETERMINER GENE; GENE; GENETIC ANALYSIS; GENETIC CODE; GENOME ANALYSIS; HAPLOIDY; HETEROZYGOSITY; HOMOZYGOSITY; HONEYBEE; MOLECULAR CLONING; MOLECULAR MODEL; NONHUMAN; PHYLOGENY; REGULATORY MECHANISM; REVIEW; SEX DETERMINATION; SEXUAL DEVELOPMENT; SPECIES DIFFERENTIATION;

ALLELES; ANIMALS; BEES; FEMALE; GENES, INSECT; MALE; MODELS, BIOLOGICAL; PHYLOGENY; SEX DETERMINATION (GENETICS); SEX DIFFERENTIATION;

ANIMALIA; APIS; APIS MELLIFERA; APOIDEA; DIPTERA; FORMICIDAE; HEXAPODA; HYMENOPTERA; SYMPHYTA; VESPIDAE;

EID: 7044261973     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20098     Document Type: Review

References (56)

1. Cline TW, Meyer BJ. 1996. Vive la Difference: Males vs females in flies vs worms. Annu Rev Genet 30:637-702.
2. Goodfellow PN, Lovell-Badge R. 1993. Sry and sex determination in mammals. Annu Rev Genet 27:71-92.
3. Whiting PW. 1943. Multiple alleles in complementary sex determination of Habrobracon. Genetics 28:365-382.
4. Beye M, Moritz RFA, Epplen C. 1994. Sex linkage in the honeybee Apis mellifera detected by multilocus DNA fingerprinting. Naturwissenschaften 81:460-462.
5. Beye M, Crozier RH, Crozier YC, Moritz RFA. 1996. Mapping the sex locus of the honeybee (Apis mellifera). Naturwissenschaften 83: 424-426.
6. Hunt GJ, Page RE. 1994. Linkage analysis of sex determination in the honey bee (Apis mellifera). Mol Gen Genet 244:512-518.
7. Hunt GJ, Page RE Jr. 1995. Linkage map of the honey bee, Apis mellifera, based on RAPD markers. Genetics 139:1371-1382.
8. Beye M, Hunt GJ, Page RE, Fondrk MK, Grohmann L, et al. 1999. Unusually high recombination rate detected in the sex locus region of the honey bee (Apis mellifera). Genetics 153:1701-1708.
9. Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW. 2003. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419-429.
10. Page RE Jr., Gadau J, Beye M. 2002. The emergence of hymenopteran genetics. Genetics 160:375-379.
11. Dzierzon J. 1845. Gutachten über die von Herrn Direktor Stöhr im ersten und zweiten Kapitel des General-Gutachtens aufgestellten Fragen. Eichstädter Bienenzeitung 1:109-113; 119-121.
12. Siebold CTh. 1856. Die Drohneneier sind nicht befruchtet. Bienenzeitung 12:181-184.
13. Nachtsheim H. 1916. Zytologische Studien über die Geschlechtsbestimmung bei der Honigbiene (Apis mellifera). Arch Zellforsch 11:169-241.
14. Mable BK, Otto SP. 1998. The evolution of life cycles with haploid and diploid phases. Bioessays 20:453-462.
15. Crozier RH, Pamilo P. 1996. Evolution of social insect colonies. Oxford: Oxford University Press.
16. Bull JJ. 1983. Evolution of Sex Determining Mechanisms. Menlo Park, Calif.: Benjamin/Cummings Publishing Company.
17. McClung CE. 1902. The accessory chromosome-sex determinant? Biol Bull Mar Biol Lab, Woods Hole 3:43-84.
18. Wilson EB. 1905. The chromosomes in relation to determination of sex in insects. Science 22:500-502.
19. Bridges CB. 1916. Non-disjunction as proof of the chromosome theory of heredity. Genetics 1:1-52.
20. Bridges CB. 1925. Sex in relation to genes and chromosomes. Am Nat 59:134.
21. Whiting PW. 1933. Selective fertilization and sex determination in Hymenoptera. Science 78:537-538.
22. Adams J, Rothman ED, Kerr WE, Paulino ZL. 1977. Estimation of the number of sex alleles and queen maitings from diploid male frequencies in a population of Apis mellifera. Genetics 86:583-596.
23. Cook JM. 1993. Sex determination in the hymenoptera: A review of models and evidence. Heredity 71:421-435.
24. Dobson SL, Tanouye MA. 1998. Evidence for a genomic imprinting sex determination mechanism in Nasonia vitripennis (Hymenoptera; Chalcidoidea). Genetics 149:233-242.
25. Poirié M, Périquet G, Beukeboom LW. 1992. The hymenopteran way of determining sex. Semin Dev Biol 3:357-361.
26. Schutt C, Nothiger R. 2000. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127:667-677.
27. Hasselmann M, Fondrk MK, Page RE, Beye M. 2001. Fine scale mapping in the sex locus region of the honey bee (Apis mellifera). Insect Mol Biol 10:605-608.
28. Beye M, Poch A, Burgtorf C, Moritz RFA, Lehrach H. 1998. A gridded genomic library of the honeybee (Apis mellifera): A reference library system for basic and comparative genetic studies of a Hymenopteran Genome. Genomics 49:317-320.
29. Hastings ML, Krainer AR. 2001. Pre-mRNA splicing in the new millennium. Curr Opin Cell Biol 13:302-309.
30. Graveley BR. 2000. Sorting out the complexity of SR protein functions. RNA 6:1197-1211.
31. Beye M, Hartel S, Hagen A, Hasselmann M, Omholt SW. 2002. Specific developmental gene silencing in the honey bee using a homeobox motif. Insect Mol Biol 11:527-532.
32. Tacke R, Manley JL. 1999. Determinants of SR protein specificity. Curr Opin Cell Biol 11:358-362.
33. Dauwalder B, Mattox W. 1998. Analysis of the functional specificity of RS domains in vivo. EMBO J 17:6049-6060.
34. Kay BK, Williamson MP, Sudol M. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14:231-241.
35. Sudol M, Sliwa K, Russo T. 2001. Functions of WW domains in the nucleus. FEBS Lett 490:190-195.
36. Wang HY, Lin W, Dyck JA, Yeakley JM, Songyang Z, et al. 1998. SRPK2: a differentially expressed SR protein-specific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J Cell Biol 140:737-750.
37. Yeakley JM, Tronchere H, Olesen J, Dyck JA, Wang HY, et al. 1999. Phosphorylation regulates in vivo interaction and molecular targeting of serine/arginine-rich pre-mRNA splicing factors. J Cell Biol 145:447-455.
38. Kamper J, Reichmann M, Romeis T, Bolker M, Kahmann R. 1995. Multiallelic recognition: nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81:73-83.
39. Black DL. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72:291-336.
40. Hoshijima K, Inoue K, Higuchi I, Sakamoto H, Shimura Y. 1991. Control of doublesex alternative splicing by transformer and transformer-2 in Drosophila. Science 252:833-836.
41. Tian M, Maniatis T. 1993. A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell 74:105-114.
42. Wang J, Xiao SH, Manley JL. 1998. Genetic analysis of the SR protein ASF/SF2: interchangeability of RS domains and negative control of splicing. Genes Dev 12:2222-2233.
43. Dubendorfer A, Hediger M, Burghardt G, Bopp D. 2002. Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int J Dev Biol 46:75-79.
44. Hediger M, Burghardt G, Siegenthaler C, Buser N, Hilfiker-Kleiner D, et al. 2004. Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214:29-42.
45. Pane A, Salvemini M, Bovi PD, Polito C, Saccone G. 2002. The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129:3715-3725.
46. Hilfiker-Kleiner D, Dubendorfer A, Hilfiker A, Nothiger R. 1993. Developmental analysis of two sex-determining genes, M and F, in the housefly, Musca domestica. Genetics 134:1187-1194.
47. Willhoeft U, Franz G. 1996. Identification of the sex-determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics 144:737-745.
48. Ohbayashi F, Suzuki MG, Mita K, Okano K, Shimada T. 2001. A homologue of the Drosophila doublesex gene is transcribed into sex-specific mRNA isoforms in the silkworm, Bombyx mori. Mol Genet Metab 128:145-158.
49. Wilkins AS. 1995. Moving up the hierarchy: A hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17:71-77.
50. Marin I, Baker BS. 1998. The evolutionary dynamics of sex determination. Science 281:1990-1994.
51. Saccone G, Peluso I, Artiaco D, Giordano E, Bopp D, et al. 1998. The Ceratitis capitata homologue of the Drosophila sex-determining gene Sex-lethal is structurally conserved, but not sex-specifically regulated. Development 125:1495-1500.
52. Meise M, Hilfiker-Kleiner D, Dübendorfer A, Brunner C, Nöthiger R, et al. 1998. Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125:1487-1494.
53. Garrett-Engele CM, Siegal ML, Manoli DS, Williams BC, Li H, et al. 2002. intersex, a gene required for female sexual development in Drosophila, is expressed in both sexes and functions together with doublesex to regulate terminal differentiation. Development 129:4661-4675.
54. Christiansen A, Keisman E, Ahmad S, Baker B. 2002. Sex comes in from the cold: the integration of sex and pattern. Trends Genet 18:510.
55. Hasselmann M, Beye M. 2004. Signatures of selection among sex-determining alleles of the honey bee. Proc Natl Acad Sci USA 101:4888-4893.
56. http://www.rug.nl/biologie/onderzoek/onderzoekGroepen/ evolutionaryGenetics/evogen/