Abstract
During the evolution of the Y chromosome of Drosophila hydei, retrotransposons became incorporated into the lampbrush loop pairs formed by several of the male fertility genes on this chromosome. Although insertions of retrotransposons are involved in many spontaneous mutations, they do not affect the functions of these genes. We have sequenced gypsy elements that are expressed as constituents of male fertility gene Q in the lampbrush loop pair Nooses. We find that these gypsy elements are all truncated and specifically lost those sequences that may interfere with the continuity of lampbrush loop transcription. Only defective coding regions are found within the loop. Gypsy is not transcribed in loops of many other Drosophila species harboring the family. These results suggest that any contribution of gypsy to the function of male fertility gene Q does not depend on a conserved DNA sequence.
Similar content being viewed by others
References
Alberola TM, de Frutos R (1993) Gypsy homologous sequences in Drosophila subobscura (gypsyDS). J Mol Evol 36:127–135
Amersham (1984) M13 cloning and sequencing handbook
Arkhipova IR, Mazo AM, Cherkassova VA, Gorelova TV, Schuppe NG, Ilyin YV (1986) The steps of reverse transcription of Drosophila mobile dispersed genetic elements and U3-R-U5 structure of their LTRs. Cell 44:555–563
Arkhipova IR, Ilyin YV (1991) Properties of promoter regions of mdg1 Drosophila retrotransposon indicate that it belongs to a specific class of promoters. EMBO J 10:1169–1177
Bingham PM, Zachar Z (1989) Retrotransposons and the FB transposon from Drosophila melanogaster. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington DC, pp 485–502
Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Annu Rev Microbiol 43:403–434
Bonaccorsi S, Gatti M, Pisano C, Lohe A (1990) Transcription of a satellite DNA on two Y chromosome loops of Drosophila melanogaster. Chromosoma 99:260–266
Bonaccorsi S, and Lohe A (1991) Fine mapping of satellite DNA sequences along the Y chromosome of Drosophila melanogaster: relationships between satellite DNA sequences and fertility factors. Genetics 129:177–189
Bridges CB (1916) Non-disjunction as proof of the chromosome theory of heredity. Genetics 1:1–52, 107–163
Charlesworth B (1978) Model for evolution of Y chromosomes and dosage compensation. Proc Natl Acad Sci USA 75:5618–5622
Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033
Charlesworth B, Langley CH (1991) Population genetics of transposable elements in Drosophila. In: Selander RK, Clark AG, Whittam TS (eds) Evolution at the molecular level. Sinauer Associates, Sunderland, pp 150–176
Corces VG, Geyer PK (1991) Interactions of retrotransposons with the host genome: the case of the gypsy element of Drosophila. Trends Genet 7:86–90
Daniels SB, Peterson KR, Strausbaugh LD, Kidwell MG, Chovnick A (1990a) Evidence for horizontal transmission of the P element between Drosophila species. Genetics 124:339–355
Daniels SB, Chovnick A, Boussy IA (1990b) Distribution of hobo transposable elements in the genus Drosophila. Mol Biol Evol 7:589–606
Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acid Res 12:387–395
Endow SA, Atwood KC (1988) Magnification: gene amplification by an inducible system of sister chromatid exchange. Trends Genet 4:348–351
Finnegan DJ (1990) Transposable elements. Dros Inf Serv 68:371–382
Gatti M, Pimpinelli S (1992) Functional elements in Drosophila melanogaster heterochromatin. Annu Rev Genet 26:239–275
Gepner J, Hays T (1993) A fertility region on the Y chromosome of Drosophila melanogaster encodes the structural gene for a dynein microtubule motor. Proc Natl Acad Sci USA 90:11132–11136
Geyer PK, Green MM, Corces VG (1988) Mutant gene phenotypes mediated by a Drosophila melanogaster retrotransposon require sequences homologous to mammalian enhancers. Proc Natl Acad Sci USA 85:8593–8597
Geyer PK, Corces VG (1992) DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev 6:1865–1873
Goldstein LSB, Hardy RW, Lindsley DL (1982) Structural genes on the Y chromosome of Drosophila melanogaster. Proc Natl Acad Sci USA 79:7405–7409
Green MM (1988) Mobile DNA elements and spontaneous gene mutation. In: Lambert ME, McDonald JF, Weinstein IB (eds) Eukaryotic transposable elements as mutagenic agents. Banbury report 30. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 41–50
Grimaldi DA (1990) A phylogenetic, revised classification of genera in the Drosophilidae (Diptera). Bull Am Mus Nat Hist 197:1–139
Grond CJ, Siegmund I, Hennig W (1983) Visualization of a lampbrush loop-forming fertility gene in Drosophila hydei. Chromosoma 88:50–56
Hackstein JHP (1987) Spermatogenesis in Drosophila. In: Hennig W (ed) Spermatogenesis, genetic aspects. Results and problems in cell differentiation, vol 15. Springer, Berlin, pp 61–116
Hackstein JHP, Leoncini O, Beck H, Peelen G, Hennig W (1982) Genetic fine structure of the Y chromosome of Drosophila hydei. Genetics 101:257–277
Hackstein JHP, Glätzer KH, Hulsebos TJM (1991) Genetic and cytogenetic analysis of the “Th-Ps” region of the Y chromosome of Drosophila hydei: evidence for dual functions of the lampbrush loop-forming fertility genes? Mol Gen Genet 227:293–305
Hardy RW, Tokuyasu KT, Lindsley DL (1981) Analysis of spermotogenesis in Drosophila melanogaster bearing deletions for Y-chromosome fertility genes. Chromosoma 83:593–617
Hareven D, Zuckerman M, Lifschytz E (1986) Origin and evolution of the transcribed repeated sequences on the Y chromosome lampbrush loops of Drosophila hydei. Proc Natl Acad Sci USA 83:125–129
Hennig W (1985) Y chromosome function and spermatogenesis in Drosophila hydei. Adv Genet 23:179–234
Hennig W (1990) The Y chromosome of Drosophila. In: Adolph KW (ed) Chromosomes: eukaryotic, prokaryotic and viral. CRC Press, Boca Raton, Florida, pp 213–238
Hennig W (1993) Conventional protein coding genes in the Drosophila Y chromosome: is the puzzle of the fertility gene function solved? Proc Natl Acad Sci USA 90:10904–10906
Hennig W, Huijser P, Vogt P, Jäckle H, Edström J-E (1983) Molecular cloning of microdissected lampbrush loop DNA sequences of Drosophila hydei. EMBO J 2:1741–1746
Hennig W, Brand RC, Hackstein J, Hochstenbach R, Kremer H, Lankenau D-H, Lankenau S, Miedema K, Pötgens A (1989) Y chromosomal fertility genes of Drosophila: a new type of eukaryotic genes. Genome 31:561–571
Hess O, Meyer GF (1968) Genetic activities of the Y chromosome in Drosophila during spermatogenesis. Adv Genet 14:171–228
Hochstenbach R (1994) Anatomy of a lampbrush loop-forming male fertility gene on the Y chromosome of Drosophila hydei. Ph.D. thesis, Department of Molecular and Developmental Genetics, Catholic University of Nijmegen, The Netherlands
Hochstenbach R, Pötgens A, Meijer H, Dijkhof R, Knops M, Schouren K, Hennig W (1993a) Partial reconstruction of the lampbrush loop pair Nooses on the Y chromosome of Drosophila hydei. Chromosoma 102:526–545
Hochstenbach R, Wilbrink M, Suijkerbuijk R, Hennig W (1993b) Localization of the lampbrush loop pair Nooses on the Y chromosome of Drosophila hydei by fluorescence in situ hybridization. Chromosoma 102:546–552
Hochstenbach R, Knops M, Hennig W (1994) Discrimination of related transcribed and non-transcribed repetitive DNA sequences from the Y chromosomes of Drosophila hydei and Drosophila eohydei. Mol Gen Genet 234:54–62
Huijser P, Hennig W (1987) Ribosomal DNA-related sequences in a Y chromosomal lampbrush loop of Drosophila hydei. Mol Gen Genet 206:441–451
Huijser P, Kirchhoff C, Lankenau D-H, Hennig W (1988) Retrotransposon-like sequences are expressed in Y chromosomal lampbrush loops of Drosophila hydei. J Mol Biol 203:689–697
Jarrell KA, Meselson M (199l) Drosophila retrotransposon promoter includes an essential sequence at the initiation site and requires a downstream promoter for full activity Proc Natl Acad Sci USA 88:102–104
Kuff EL, Lueders KK (l988) The intracisternal A-particle gene family: structure and functional aspects. Adv Cancer Res 51:183–276
Lankenau D-H (1990) Molecular structure and evolution of a retrotransposon family in Drosophila. Ph.D. thesis, Department of Molecular and Developmental Genetics, Catholic University of Nijmegen, The Netherlands
Lankenau D-H, Huijser P, Jansen E, Miedema K, Hennig W (1988) Micropia: a retrotransposon of Drosophila combining structural features of DNA viruses, retroviruses and non-viral transposable elements. J Mol Biol 204:233–246
Lankenau D-H, Huijser P, Jansen E, Miedema K, Hennig W (1990) DNA sequence comparison of micropia transposable elements from Drosophila hydei and Drosophila melanogaster. Chromosoma 99:111–117
Lankenau S, Corces VG, Lankenau D-H (1994) The Drosophila micropia retrotransposon encodes a testis-specific antisense-RNA complementary to reverse transcriptase. Mol Cell Biol, 14: 1764–1775
Leoncini O (1977) Temperatursensitive Mutanten im Y Chromosom von Drosphila hydei. Chromosoma 63:329–357
Lifschytz E (1987) The developmental program of spermiogenesis in Drosophila: a genetic analysis. Int Rev Cytol 109:211–258
Lifschytz E, Hareven D, Azriel A, Brodsly H (1983) DNA clones and RNA transcripts of four lampbrush loops from the Y chromosome of Drosophila hydei. Cell 32:191–199
Lifschytz E, Hareven D (1985) Molecular evidence for partial inactivation of Y loops in T(X;Y)56 males from D. hydei. Mol Gen Genet 199:46–52
Lobe AR, Brutlag DL (1987) Identical satellite DNA sequences in sibling species of Drosophila. J Mol Biol 194:161–170
de Loos F, Dijkhof R, Grond CJ, Hennig W (1984) Lampbrush chromosome loop-specificity of transcript morphology in spermatocyte nuclei of Drosophila hydei. EMBO J 3:2845–2849
Marlor RL, Parkhurst SM, Corces VG (1986) The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 6:1129–1134
Martin G, Wiernasz D, Schedl P (1983) Evolution of Drosophila repetitive-dispersed DNA. J Mol Evol 19:203–213
Mazo AM, Mizrokhi LJ, Karavanov AA, Sedkov YA, Krichevskaja AA, Ilyin YV (1989) Suppression in Drosophila: su(Hw) and su(f) gene products interact with a region of gypsy (mdg4) regulating its transcriptional activity. EMBO J 8:903–911
Meyerowitz EM, Hogness DS (1982) Molecular organization of a Drosophila puff site that responds to ecdysone. Cell 28:165–176
Mizrokhi LJ, Mazo AM (1990) Evidence for horizontal transmission of the mobile element jockey between distant Drosophila species. Proc Natl Acad Sci USA 87:9216–9220
Mizrokhi LJ, Mazo AM (1991) Cloning and analysis of the mobile element gypsy from D. virilis. Nucleic Acids Res 19:913–916
Morgan TH (1914) No crossing-over in the male of Drosophila of genes in the second and third pairs of chromosomes. Biol Bull 26:195–204
Muller HJ (1918) Genetic variability, twin hybrids and constant hybrids, in a case of balanced lethal factors. Genetics 3:422–449
Ohno S (1967) Sex chromosomes and sex linked genes. Springer-Verlag, Berlin
Papenbrock T (1991) Molekulare Analyse der Riesentranskripte aus den Y chromosomalen Lampenbürstenschleifen von Drosophila hydei. Ph.D. thesis, Institut für Genetik, Heinrich Heine Universität, Düsseldorf, Germany
Parkhurst SM, Corces VG (1986) Interactions among the gypsy transposable element and the yellow and the suppressor of Hairy-wing loci in Drosophila melanogaster. Mol Cell Biol 6:47–53
Parkhurst SM, Harrison DA, Remington MP, Spana C, Kelley RL, Coyne RS, Corces VG (1988) The Drosophila su(Hw) gene, which controls the phenotypic effect of the gypsy transposable element, encodes a putative DNA-binding protein. Genes Dev 2:1205–1215
Pearson WR, Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:244–2448
Rice WR (1987) Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116:161–167
Roseman RR, Pirrotta V, Geyer PK (1993) The su(Hw) protein insulates expression of the Drosophila melanogaster white gene from chromosomal position effects. EMBO J 12:435–442
Saigo K, Kugimiya W, Matsuo Y, Inouye S, Yoshioka K, Yuki S (1984) Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature 312:659–661
Sandmeyer SB, Hansen LJ, Chalker DL (1990) Integration specificity of retrotransposons and retroviruses. Annu Rev Genet 24:491–518
Smith PA, Corces VG (1992) The suppressor of Hairy-wing binding region is required for gypsy mutagenesis. Mol Gen Genet 233:65–70
Spana C, Harrison DA, Corces VG (1988) The Drosophila melanogaster suppressor of Hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes Dev 2:1414–1423
Stacey SN, Lansman RA, Brock HW, Grigliatti TA (1986) Distribution and conservation of mobile elements in the genus Drosophila. Mol Biol Evol 3:522–534
Steinemann M, Steinemann S (1991) Preferential Y chromosomal localization of TRIM, a novel transposable element of Drosophila miranda, obscura group. Chromosoma 101:169–179
Steinemann M, Steinemann S (1992) Degenerating Y chromosome of Drosophila miranda: a trap for retrotransposons. Proc Natl Acad Sci USA 89:7591–7595
Steinemann M, Steinemann S, Lottspeich F (1993) How Y chromosomes become genetically inert. Proc Natl Acad Sci USA 90:5737–5741
Trapitz P, Wlaschek M, Bunëmann H (1988) Structure and function of Y chromosomal DNA: II. Analysis of lampbrush loop associated transcripts in nuclei of primary spermatocytes of Drosophila hydei by in situ hybridization using asymmetric RNA probes of four different families of repetitive DNA. Chromosoma 96:159–170
Trapitz P, Glätzer KH, Bünemann H (1992) Towards a physical map of the fertility genes on the heterochromatic Y chromosome of D. hydei: families of repetitive sequences transcribed on the lampbrush loops ‘Nooses’ and ‘Threads’ are organized in extended clusters of several hundred kilobases. Mol Gen Genet 235:221–234
Vogt P, Hennig W, Siegmund I (1982) Identification of cloned Y chromosomal DNA sequences from a lampbrush loop of Drosophila hydei. Proc Natl Acad Sci U S A 79:5132–5136
Vogt P, Hennig W (1983) Y chromosomal DNA of Drosophila hydei. J Mol Biol 167:37–56
Vogt P, Hennig W, ten Hacken D, Verbost P (1986) Evolution of Y chromosomal lampbrush loop DNA sequences of Drosophila. Chromosoma 94:367–376
Vogt P, Hennig W (1986b) Molecular structure of the lampbrush loops nooses of the Y chromosome of Drosophila hydei: I. The Y chromosome-specific repetitive DNA sequence family ayl is dispersed in the loop DNA. Chromosoma 94:449–458
Vogt P, Hennig W (1986b) Molecular structure of the lampbrush loops nooses of the Y chromosome of Drosophila hydei: II. DNA sequences with homologies to multiple genomic locations are major constituents of the loop. Chromosoma 94:459–467
Wasserman M (1982) Evolution of the repleta group. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology of Drosophila, vol 3b. Academic Press, London, pp 61–139
Wlaschek M, Awgulewitsch A, Bunemann H (1988) Structure and function of Y chromosomal DNA: I. Sequence organization and localization of four different families of repetitive DNA on the Y chromosome of Drosophila hydei. Chromosoma 96:145–158
Author information
Authors and Affiliations
Additional information
Correspondence to: W. Hennig
Rights and permissions
About this article
Cite this article
Hochstenbach, R., Harhangi, H., Schouren, K. et al. Degenerating gypsy retrotransposons in a male fertility gene on the Y chromosome of Drosophila hydei . J Mol Evol 39, 452–465 (1994). https://doi.org/10.1007/BF00173414
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00173414