Abstract
The Australian sheep blowfly Lucilia cuprina is a major pest for the Australian and New Zealand sheep industries. With the long-term aim of making a strain of L. cuprina suitable for a genetic control program, we previously developed a tetracycline-repressible female lethal genetic system in Drosophila. A key part of this system is a female-specific promoter from a yolk protein (yp) gene controlling expression of the tetracycline-dependent transactivator (tTA). Here we report the sequence of a 14.2 kb genomic clone from L. cuprina that contains a cluster of three complete yp genes and one partial yp gene. The Lcyp genes are specifically expressed in females that have received a protein meal. A bioinformatic analysis of the promoter of one of the yp genes (LcypA) identified several putative binding sites for DSX, a known regulator of yp gene expression in other Diptera. A transgenic strain of L. cuprina was made that contained the LcypA promoter driving the expression of the Escherichia coli lacZ reporter gene. Transgenic females express high levels of β-galactosidase after a protein meal. Thus the LcypA promoter could be used to obtain female-specific expression of tTA in transgenic L. cuprina.
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References
Bownes M (1994) The regulation of the yolk protein genes, a family of sex differentiation genes in Drosophila melanogaster. Bioessays 16(10):745–752
Burtis KC, Baker BS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56(6):997–1010
Cho S, Wensink PC (1998) Linkage between oligomerization and DNA binding in Drosophila doublesex proteins. Biochemistry 37(32):11301–11308
Concha C, Scott MJ (2009) Sexual development in Lucilia cuprina (Diptera, Calliphoridae) is controlled by the transformer gene. Genetics 182(3):785–798
Concha C, Li F, Scott MJ (2010) Conservation and sex-specific splicing of the doublesex gene in the economically important pest species Lucilia cuprina (Diptera, Calliphoridae). J Genet (in press)
Coschigano KT, Wensink PC (1993) Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev 7(1):42–54
Davidson S (1989) Sheep blowfly control by genetic sabotage. Rural Res 145:19–24
Erdman SE, Chen HJ, Burtis KC (1996) Functional and genetic characterization of the oligomerization and DNA binding properties of the Drosophila doublesex proteins. Genetics 144(4):1639–1652
Fitzsimons HL, Henry RA, Scott MJ (1999) Development of an insulated reporter system to search for cis-acting DNA sequences required for dosage compensation in Drosophila. Genetica 105(3):215–226
Foster GG (1991) Simulation of genetic control. Homozygous-viable pericentric inversions in field-female killing systems. Theor Appl Genet 82:368–378
Foster GG, Vogt WG, Woodburn TL (1985) Genetic analysis of field trials of sex-linked translocation strains for genetic control of the Australian sheep blowfly Lucilia cuprina (Wiedemann). Aust J Biol Sci 38:275–293
Foster GG, Vogt WG, Woodburn TL, Smith PH (1988) Computer simulation of genetic control. Comparison of sterile males and field-female killing systems. Theor Appl Genet 76:870–879
Heath AC, Bishop DM (2006) Flystrike in New Zealand: an overview based on a 16-year study, following the introduction and dispersal of the Australian sheep blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae). Vet Parasitol 137(3–4):333–344
Hediger M, Burghardt G, Siegenthaler C, Buser N, Hilfiker-Kleiner D, Dubendorfer A, Bopp D (2004) Sex determination in Drosophila melanogaster and Musca domestica converges at the level of the terminal regulator doublesex. Dev Genes Evol 214(1):29–42
Heinrich JC, Scott MJ (2000) A repressible female-specific lethal genetic system for making transgenic insect strains suitable for a sterile-release program. Proc Natl Acad Sci USA 97(15):8229–8232
Heinrich JC, Li X, Henry RA, Haack N, Stringfellow L, Heath AC, Scott MJ (2002) Germ-line transformation of the Australian sheep blowfly Lucilia cuprina. Insect Mol Biol 11(1):1–10
Hens K, Lemey P, Macours N, Francis C, Huybrechts R (2004) Cyclorraphan yolk proteins and lepidopteran minor yolk proteins originate from two unrelated lipase families. Insect Mol Biol 13(6):615–623
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(5007):833–836
Hultmark D, Klemenz R, Gehring WJ (1986) Translational and transcriptional control elements in the untranslated leader of the heat-shock gene hsp22. Cell 44(3):429–438
Krafsur ES (1998) Sterile insect technique for suppressing and eradicating insect population: 55 years and counting. J Agric Entomol 15(4):303–317
Martinez A, Bownes M (1994) The sequence and expression pattern of the Calliphora erythrocephala yolk protein a and b genes. J Mol Evol 38(4):336–351
McInnis DO, Tam S, Grace C, Miyashita D (1994) Population suppression and sterility induced by variable sex ratio, sterile insect releases of Ceratitis capitata (diptera: Tephritidae) in Hawaii. Ann Entomol Soc Am 87:231–240
Pane A, Salvemini M, Delli Bovi P, Polito C, Saccone G (2002) The transformer gene in Ceratitis capitata provides a genetic basis for selecting and remembering the sexual fate. Development 129(15):3715–3725
Perkins HD, Howells AJ (1992) Genomic sequences with homology to the P element of Drosophila melanogaster occur in the blowfly Lucilia cuprina. Proc Natl Acad Sci USA 89(22):10753–10757
Rina M, Savakis C (1991) A cluster of vitellogenin genes in the mediterranean fruit fly Ceratitis capitata: Sequence and structural conservation in dipteran yolk proteins and their genes. Genetics 127(4):769–780
Robinson AS (2002) Genetic sexing strains in medfly, Ceratitis capitata, sterile insect technique programmes. Genetica 116(1):5–13
Thomas DD, Donnelly CA, Wood RJ, Alphey LS (2000) Insect population control using a dominant, repressible, lethal genetic system. Science 287(5462):2474–2476
Tortiglione C, Bownes M (1997) Conservation and divergence in the control of yolk protein genes in dipteran insects. Dev Genes Evol 207:264–281
Wardhaugh KG, Morton R, Bedo D, Horton BJ, Mahon RJ (2007) Estimating the incidence of fly myiases in Australian sheep flocks: Development of a weather-driven regression model. Med Vet Entomol 21(2):153–167
Webber LG (1958) Nutrition and reproduction in the Australian sheep blowfly Lucilia cuprina. Aust J Zool 6(2):139–144
White NM, Bownes M (1997) Cloning and characterization of three Musca domestica yolk protein genes. Insect Mol Biol 6(4):329–341
Acknowledgments
We thank Phil Batterham for the gift of a L. cuprina genomic DNA phage library and Fred Gould for comments on the manuscript. This research benefited significantly from discussion at regular research co-ordination meetings of the FAO/IAEA co-ordinated research project on “Molecular technologies to improve the effectiveness of the sterile insect technique”. Our research was supported by funding from Massey University and Meat and Wool New Zealand.
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Scott, M.J., Atapattu, A., Schiemann, A.H. et al. Organisation and expression of a cluster of yolk protein genes in the Australian sheep blowfly, Lucilia cuprina . Genetica 139, 63–70 (2011). https://doi.org/10.1007/s10709-010-9492-6
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DOI: https://doi.org/10.1007/s10709-010-9492-6