Skip to main content
Log in

Defective I elements introduced intoDrosophila as transgenes can regulate reactivity and prevent I-R hybrid dysgenesis

  • Original Paper
  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Abstract

The I-R hybrid dysgenesis syndrome is characterized by a high level of sterility and I element transposition, occurring in the female offspring of crosses between males of inducer (I) strains, which contain full-length transposable I elements, and females of reactive (R) strains, devoid of functional I elements. The intensity of the syndrome in the dysgenic cross is essentially dependent on the reactivity level of the R females, which is ultimately controlled by still unresolved polygenic chromosomal determinants. In the work reported here, we have introduced a transposition-defective I element with a 2.6 kb deletion within its second open reading frame into a highly reactive R strain, by P-mediated transgenesis. We demonstrate that this defective I element gradually alters the level of reactivity in the three independent transgenic lines that were obtained, over several generations. After > 15 generations, the transgenicDrosophila show strongly reduced reactivity, and finally become refractory to hybrid dysgenesis, without, however, acquiring the inducer phenotype. Induction of a low reactivity level is reversible reactivity again increases upon transgene removal and is maternally inherited, as observed for the control of reactivity in natural R strains. These results demonstrate that defective I elements introduced as single-copy transgenes can act as regulators of reactivity, and suggest that some of the ancestral defective pericentromeric I elements that can be found in all reactive strains could be the molecular determinants of reactivity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abad P, Vaury C, Pelisson A, Chaboissier MC, Busseau I, Bucheton A (1989) A long interspersed repetitive element — the I factor ofDrosophila teissieri — is able to transpose in differentDrosophila species. Proc Natl Acad Sci USA 86:8887–8891

    Google Scholar 

  • Bregliano JC, Kidwell MG (1983) Hybrid dysgenesis determinants. In: Shapiro J (ed) Mobile genetic elements. Academic Press, New York, pp 363–410

    Google Scholar 

  • Bregliano JC, Picard G, Bucheton A, Pelisson A, Lavige JM, L'Heritier P (1980) Hybrid dysgenesis inDrosophila melanogaster. Science 207: 606–611

    Google Scholar 

  • Bucheton A (1973) Contribution à l'étude de la stérilité femelle non mendelienne chezDrosophila melanogaster. Transmission héréditaire des degrés d'efficacité du facteur “réacteur”. C R Acad Sci Paris [D] 276:641–644

    Google Scholar 

  • Bucheton A (1978) Non-mendelian female sterility inDrosophila melanogaster: influence of aging and thermic treatments. Part I. Evidence for a partly inheritable effect of these two factors. Heredity 41:357–369

    Google Scholar 

  • Bucheton A (1979a) Non-mendelian female sterility inDrosophila melanogaster: influence of ageing and thermic treatments. Part II: Action of thermic treatments on the sterility of SF females and on the reactivity of reactive females. Biol Cell 34:43–50

    Google Scholar 

  • Bucheton A (1979b) Non-mendelian female sterility inDrosophila melanogaster: influence of ageing and thermic treatments. Part III. Cumulative effects induced by these factors. Genetics 93:131–142

    Google Scholar 

  • Bucheton A (1990) I transposable elements and I-R hybrid dysgenesis inDrosophila. Trends Genet 6:16–21

    Google Scholar 

  • Bucheton A, Bregliano J-C (1982) The I-R system of hybrid dysgenesis inDrosophila melanogaster: heredity of the reactive condition. Biol Cell 46:123–132

    Google Scholar 

  • Bucheton A, Picard G (1978) Non-mendelian female sterility inDrosophila melanogaster: hereditary transmission of reactivity levels. Heredity 40:207–223

    Google Scholar 

  • Bucheton A, Lavige JM, Picard G, L'Héritier P (1976) Non-mendelian female sterility inDrosophila melanogaster: quantitative variations in the efficiency of inducer and reactive strains. Heredity 36:305–314

    Google Scholar 

  • Bucheton A, Paro R, Sang HM, Pelisson A, Finnegan DJ (1984) The molecular basis of I-R hybrid dysgenesis inDrosophila melanogaster: identification, cloning, and properties of the I factor. Cell 38:153–163

    Google Scholar 

  • Bucheton A, Vaury C, Chaboissier M-C, Abad P, Pélisson A, Simonelig M (1993) I elements and therosophila genome. In: McDonald JF (ed) Transposable elements and evolution. Kluwer Academic Publishers, The Netherlands, pp 173–188

    Google Scholar 

  • Chaboissier M-C, Busseau I, Prosser J, Finnegan DJ, Bucheton A (1990) Identification of a potential RNA intermediate for transposition of the LINE-like element I factor inDrosophila melanogaster. EMBO J 9:3557–3563

    Google Scholar 

  • Crozatier M, Vaury C, Busseau I, Pélisson A, Bucheton A (1988) Structure and genomic organization of I elements involved in I-R hybrid dysgenesis inDrosophila melanogaster. Nucleic Acids Res 16:9199–9213

    Google Scholar 

  • Ephrussi A, Dickinson LK, Lehmann R (1991)oskar organizes the germ plasm and directs localization of the posterior determinantnanos. Cell 66:37–50

    Google Scholar 

  • Fawcett DH, Lister CK, Kellet E, Finnegan DJ (1986) Transposable elements controlling I-R hybrid dysgenesis inD. melanogaster are similar to mammalian LINES. Cll 47:1007–1015

    Google Scholar 

  • Finnegan DJ (1989) The I factor and I-R hybrid dysgenesis inDrosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington D.C., pp 503–517

    Google Scholar 

  • Hazelrigg T, Levis R, Rubin GM (1984) Transformation ofwhite locus DNA inDrosophila: dosage compensation,zeste interaction, and position effects. Cell 36:469–481

    Google Scholar 

  • Jensen S, Heidmann T (1991) An indicator gene for detection of germline retrotransposition in transgenicdrosophila demonstrates RNA-mediated transposition of the LINE I element. EMBO J 10:1927–1937

    Google Scholar 

  • Jensen S, Cavarec L, Dhellin O, Heidmann T (1994) Retrotransposition of a markedDrosophila LINE-like I element in cells in culture. Nucleic Acids Res 22:1484–1488

    Google Scholar 

  • Karess RE, Rubin GM (1984) Analysis of P transposable element functions inDrosophila. Cell 38:135–146

    Google Scholar 

  • Klemenz R, Weber U, Gehring WJ (1987) Thewhite gene as a marker in a new P element vector for gene transfer inDrosophila. Nucleic Acids Res 15:3947–3959

    Google Scholar 

  • Lachaume P, Pinon H (1993) Germ-line expression of the I factor, a functional LINE from the fruit flyDrosophila melanogaster, is positively regulated by reactivity, a peculiar cellular state. Mol Gen Genet 240:277–295

    Google Scholar 

  • Lavige JM (1986) I-R system of hybrid dysgenesis inDrosophila melanogaster: further data on the arrest of development of the embryos from SF females. Biol Cell 56:207–216

    Google Scholar 

  • Lüning KG (1981) Genetics of inbredDrosophila melanogaster. I. Induction of marker genes and preliminary recombination tests. Hereditas 95:181–188

    Google Scholar 

  • McLean C, Bucheton A, Finnegan D (1993) The 5′ untranslated region of the I factor, a Long Interspersed Nuclear Element-like retrotransposon ofDrosophila melanogaster, contains an internal promoter and sequences that regulate expression. Mol Cell Biol 13:1042–1050

    Google Scholar 

  • Pélisson A, Bregliano JC (1987) Evidence for rapid limitation of the I element copy number in a genome submitted to several generations of I-R hybrid dysgenesis inDrosophila melanogaster. Mol Gen Genet 207:306–313

    Google Scholar 

  • Picard G (1976) Non-Mendelian female sterility inDrosophila melanogaster: hereditary transmission of I factor. Genetics 83:107–123

    Google Scholar 

  • Picard G (1978a) Non-Mendelian female sterility inDrosophila melanogaster: sterility in stocks derived from the genotypically inducer or reactive offspring of SF and RSF females. Biol Cell 31:245–254

    Google Scholar 

  • Picard G (1978b) Non-Mendelian female sterility inDrosophila melanogaster: sterility in the daughter progeny of SF and RSF females. Biol Cell 31:235–244

    Google Scholar 

  • Picard G (1978c) Non-Mendelian female sterility inDrosophila melanogaster: further data on chromosomal contamination. Mol Gen Genet 164:235–247

    Google Scholar 

  • Picard G, L'Héritier P (1971) A maternally inherited factor inducing sterility inD. melanogaster. Drosophila Inf Serv 46:54

    Google Scholar 

  • Picard G, Pelisson A (1979) Non-Mendelian female sterility inDrosophila melanogaster: characterization of the non-inducer chromosomes of inducer strains. Genetics 91:473–489

    Google Scholar 

  • Picard G, Bregliano JC, Bucheton A, Lavige JM, Pelisson A (1978) Non-Mendelian female sterility and hybrid dysgenesis inDrosophila melanogaster. Genet Res Camb 32:275–287

    Google Scholar 

  • Pritchard MA, Dura JM, Pélisson A, Finnegan DJ (1988) A cloned I-factor is fully functional inDrosophila melanogaster. Mol Gen Genet 214:533–540

    Google Scholar 

  • Ronsseray S, Lehmann M, Anxolabéhère D (1991) The maternally inherited regulation of P elements inDrosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome. Genetics 129:501–512

    Google Scholar 

  • Rubin GM, Spradling AC (1982) Genetic transformation ofDrosophila with transposable element vectors. Science 218:348–353

    Google Scholar 

  • Vaury C, Abad P, Pélisson A, Lenoir A, Bucheton A (1990) Molecular characteristics of the heterochromatic I elements from a reactive strain ofDrosophila melanogaster. J Mol Evol 31:424–431

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by D. J. Finnegan

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jensen, S., Cavarec, L., Gassama, MP. et al. Defective I elements introduced intoDrosophila as transgenes can regulate reactivity and prevent I-R hybrid dysgenesis. Molec. Gen. Genet. 248, 381–390 (1995). https://doi.org/10.1007/BF02191637

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02191637

Key words

Navigation