Expression patterns of sex-determination genes in single male and female embryos of two Bactrocera fruit fly species during early development

Insect Molecular Biology

Volumn 23, Issue 6, 2014, Pages 754-767

  Morrow, J L ^a   Riegler, M ^a   Frommer, M ^b   Shearman, D C A ^b  

^a WESTERN SYDNEY UNIVERSITY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Bactrocera; Dominant Male Determiner; quantitative reverse transcription PCR; sex determination; single embryo

Indexed keywords

BACTROCERA JARVISI; BACTROCERA TRYONI; TEPHRITIDAE;

MESSENGER RNA;

ANIMAL; ANIMAL EMBRYO; AUSTRALIA; EMBRYOLOGY; FEMALE; GENE EXPRESSION; GENETICS; MALE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SEX DETERMINATION PROCESS; TEPHRITIDAE;

ANIMALS; AUSTRALIA; BASE SEQUENCE; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION; MALE; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA SPLICING; RNA, MESSENGER; SEX DETERMINATION PROCESSES; TEPHRITIDAE;

EID: 84937694083     PISSN: 09621075     EISSN: 13652583     Source Type: Journal    
DOI: 10.1111/imb.12123     Document Type: Article

References (57)

1. Amrein, H., Gorman, M., and, Nöthiger, R., (1988) The sex-determining gene tra-2 of Drosophila encodes a putative RNA binding protein. Cell 55: 1025-1035.
2. An, X., Wilkes, K., Bastian, Y., Morrow, J.L., Frommer, M., and, Raphael, K.A., (2002) The period gene in two species of tephritid fruit fly differentiated by mating behaviour. Insect Mol Biol 11: 419-430.
3. Anderson, D.T., (1962) The embryology of Dacus tryoni (Frogg.) [Diptera, Trypetidae (= Tephritidae)], the Queensland fruit-fly. Development 10: 248-292.
4. Bennett, C.L., and, Frommer, M., (1997) The white gene of the tephritid fruit fly Bactrocera tryoni is characterized by a long untranslated 5′ leader and a 12kb first intron. Insect Mol Biol 6: 343-356.
5. Boggs, R.T., Gregor, P., Idriss, S., Belote, J.M., and, McKeown, M., (1987) Regulation of sexual differentiation in D. melanogaster via alternative splicing of RNA from the transformer gene. Cell 50: 739-747.
6. Bopp, D., Saccone, G., and, Beye, M., (2014) Sex determination in insects: variations on a common theme. Sex Dev 8: 20-28.
7. Bownes, M., (1975) A photographic study of development in the living embryo of Drosophila melanogaster. J Embryol Exp Morphol 33: 789-801.
8. Burghardt, G., Hediger, M., Siegenthaler, C., Moser, M., Dubendorfer, A., and, Bopp, D., (2005) The transformer2 gene in Musca domestica is required for selecting and maintaining the female pathway of development. Dev Genes Evol 215: 165-176.
9. Clough, E., and, Oliver, B., (2012) Genomics of sex determination in Drosophila. Brief Funct Genomics 11: 387-394.
10. Cook, C., (2005) The Role of Cryptochrome in Mating Time Difference in Tephritid Fruit Flies, Bactrocera Tryoni and Bactrocera Neohumeralis. Sydney, University of Sydney.
11. Cruickshank, L., Jessup, A.J., and, Cruickshank, D.J., (2001) Interspecific crosses of Bactrocera tryoni (Froggatt) and Bactrocera jarvisi (Tryon) (Diptera:Tephritidae) in the laboratory. Aust J Entomol 40: 278-280.
12. De Renzis, S., Elemento, O., Tavazoie, S., and, Wieschaus, E.F., (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5: e117.
13. Drew, R.A.I., (1989) The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Mem Queensl Mus 26: 1-521.
14. Erickson, J.W., and, Quintero, J.J., (2007) Indirect effects of ploidy suggest X chromosome dose, not the X: a ratio, signals sex in Drosophila. PLoS Biol 5: e332.
15. Fay, H.A.C., (2012) A highly effective and selective male lure for Bactrocera jarvisi (Tryon)(Diptera: Tephritidae). Aust J Entomol 51: 189-197.
16. Frohman, M.A., Dush, M.K., and, Martin, G.R., (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85: 8998-9002.
17. Gabrieli, P., Falaguerra, A., Siciliano, P., Gomulski, L.M., Scolari, F., Zacharopoulou, A., et al. (2010) Sex and the single embryo: early development in the Mediterranean fruit fly, Ceratitis capitata. BMC Dev Biol 10: 12.
18. Hancock, D.L., Hamacek, E.L., Lloyd, A.C., and, Elson-Harris, M.M., (2000) The Distribution and Host Plants of Fruit Flies (Diptera: Tephritidae) in Australia. Department of Primary Industries, Brisbane, Qld.
19. Hempel, L.U., and, Oliver, B., (2007) Sex-specific DoublesexM expression in subsets of Drosophila somatic gonad cells. BMC Dev Biol 7: 113.
20. Hendrichs, J., Franz, G., and, Rendon, P., (1995) Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. J Appl Entomol 119: 371-377.
21. Hilfiker-Kleiner, D., Dübendorfer, A., Hilfiker, A., and, Nöthiger, R., (1993) Developmental analysis of two sex-determining genes, M and F, in the housefly, Musca domestica. Genetics 134: 1187-1194.
22. Krosch, M.N., Schutze, M.K., Armstrong, K.F., Graham, G.C., Yeates, D.K., and, Clarke, A.R., (2012) A molecular phylogeny for the Tribe Dacini (Diptera: Tephritidae): systematic and biogeographic implications. Mol Phylogenet Evol 64: 513-523.
23. Lagos, D., Ruiz, M.F., Sanchez, L., and, Komitopoulou, K., (2005) Isolation and characterization of the Bactrocera oleae genes orthologous to the sex determining Sex-lethal and doublesex genes of Drosophila melanogaster. Gene 348: 111-121.
24. Lagos, D., Koukidou, M., Savakis, C., and, Komitopoulou, K., (2007) The transformer gene in Bactrocera oleae: the genetic switch that determines its sex fate. Insect Mol Biol 16: 221-230.
25. Liang, H.-L., Nien, C.-Y., Liu, H.-Y., Metzstein, M.M., Kirov, N., and, Rushlow, C., (2008) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456: 400-403.
26. -ΔΔ CT method. Methods 25: 402-408.
27. Mattox, W., Palmer, M.J., and, Baker, B.S., (1990) Alternative splicing of the sex determination gene transformer-2 is sex-specific in the germ line but not in the soma. Genes Dev 4: 789-805.
28. McKeown, M., Belote, J.M., and, Baker, B.S., (1987) A molecular analysis of transformer, a gene in Drosophila melanogaster that controls female sexual differentiation. Cell 48: 489-499.
29. Meats, A., Holmes, H.M., and, Kelly, G.L., (2004) Laboratory adaptation of Bactrocera tryoni (Diptera: Tephritidae) decreases mating age and increases protein consumption and number of eggs produced per milligram of protein. Bull Entomol Res 94: 517-524.
30. Meise, M., Hilfiker-Kleiner, D., Dubendorfer, A., Brunner, C., Nothiger, R., and, Bopp, D., (1998) Sex-lethal, the master sex-determining gene in Drosophila, is not sex-specifically regulated in Musca domestica. Development 125: 1487-1494.
31. Miyatake, T., (1998) Genetic changes of life history and behavioral traits during mass-rearing in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Res Popul Ecol 40: 301-310.
32. Morrow, J., Scott, L., Congdon, B., Yeates, D., Frommer, M., and, Sved, J., (2000) Close genetic similarity between two sympatric species of tephritid fruit fly reproductively isolated by mating time. Evolution 54: 899-910.
33. Morrow, J.L., Frommer, M., Shearman, D.C.A., and, Riegler, M., (2014) Tropical tephritid fruit fly community with high incidence of shared Wolbachia strains as platform for horizontal transmission of symbionts. Environ Microbiol Epub ahead of print. doi: 10.1111/1462-2920.12382.
34. Pane, A., Salvemini, M., Delli Bovi, P., Polito, C., and, Saccone, G., (2002) The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129: 3715-3725.
35. Penalva, L.O., and, Sanchez, L., (2003) RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev 67: 343-359.
36. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
37. Rothwell, W.F., and, Sullivan, W., (2000) Fluorescent analysis of Drosophila embryos. In Drosophila Protocols (, Sullivan, W., Ashburner, M., and, Hawley, R.S., eds), pp. 141-157. Cold Spring Harbor Laboratory Press, Cold Spring Harbour, NY.
38. Ruiz, M.F., Milano, A., Salvemini, M., Eirin-Lopez, J.M., Perondini, A.L.P., Selivon, D., et al. (2007) The gene Transformer of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. PLoS ONE 2: e1239.
39. Saccone, G., Peluso, I., Artiaco, D., Giordano, E., Bopp, D., and, Polito, L.C., (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.
40. Saccone, G., Pane, A., and, Polito, L.C., (2002) Sex determination in flies, fruitflies and butterflies. Genetica 116: 15-23.
41. Saccone, G., Salvemini, M., Pane, A., and, Polito, L.C., (2008) Masculinization of XX Drosophila transgenic flies expressing the Ceratitis capitata DoublesexM isoform. Int J Dev Biol 52: 1051-1057.
42. Salvemini, M., Robertson, M., Aronson, B., Atkinson, P., Polito, L.C., and, Saccone, G., (2009) Ceratitis capitata transformer-2 gene is required to establish and maintain the autoregulation of Cctra, the master gene for female sex determination. Int J Dev Biol 53: 109-120.
43. Salz, H.K., (2011) Sex determination in insects: a binary decision based on alternative splicing. Curr Opin Genet Dev 21: 395-400.
44. Sarno, F., Ruiz, M.F., Eirín-Lápez, J.M., Perondini, A.L., Selivon, D., and, Sànchez, L., (2010) The gene transformer-2 of Anastrepha fruit flies (Diptera, Tephritidae) and its evolution in insects. BMC Evol Biol 10: 140.
45. Schetelig, M.F., Milano, A., Saccone, G., and, Handler, A.M., (2012) Male only progeny in Anastrepha suspensa by RNAi-induced sex reversion of chromosomal females. Insect Biochem Mol Biol 42: 51-57.
46. Schutt, C., and, Nothiger, R., (2000) Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127: 667-677.
47. Shearman, D.C.A., (2002) The evolution of sex determination systems in dipteran insects other than Drosophila. Genetica 116: 25-43.
48. Shearman, D.C.A., and, Frommer, M., (1998) The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol Biol 7: 355-366.
49. Shearman, D.C.A., Frommer, M., Morrow, J.L., Raphael, K.A., and, Gilchrist, A.S., (2010) Interspecific hybridization as a source of novel genetic markers for the sterile insect technique in Bactrocera tryoni (Diptera: Tephritidae). J Econ Entomol 103: 1071-1079.
50. Siera, S.G., and, Cline, T.W., (2008) Sexual back talk with evolutionary implications: stimulation of the Drosophila sex-determination gene sex-lethal by its target transformer. Genetics 180: 1963-1981.
51. Sievert, V., Kuhn, S., Paululat, A., and, Traut, W., (2000) Sequence conservation and expression of the Sex-lethal homologue in the fly Megaselia scalaris. Genome 43: 382-390.
52. Souza, H.M.L., Matioli, S.R., and, Souza, W.N., (1988) The adaptation process of Ceratitis capitata to the laboratory analysis of life-history traits. Entomol Exp Appl 49: 195-201.
53. Tian, M., and, Maniatis, T., (1993) A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell 74: 105-114.
54. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034-research0034.11.
55. Willhoeft, U., and, Franz, G., (1996a) Comparison of the mitotic karyotypes of Ceratitis capitata, Ceratitis rosa, and Trirhithrum coffeae (Diptera: Tephritidae) by C-banding and FISH. Genome 39: 884-889.
56. Willhoeft, U., and, Franz, G., (1996b) Identification of the sex-determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics 144: 737-745.
57. Zabalou, S., Apostolaki, A., Livadaras, I., Franz, G., Robinson, A.S., Savakis, C., et al. (2009) Incompatible insect technique: incompatible males from a Ceratitis capitata genetic sexing strain. Entomol Exp Appl 132: 232-240.