The Enigma of Y Chromosome Degeneration: T', a Novel Retrotransposon Is Preferentially Located on the Neey Chromosome of Drosophila Miranda

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The Enigma of Y Chromosome Degeneration: T', a Novel Retrotransposon Is Preferentially Located on the Neey Chromosome of Drosophila Miranda Copyright 0 1997 by the Genetics Society of America The Enigma of Y Chromosome Degeneration: T', a Novel Retrotransposon is Preferentially Located on the NeeY Chromosome of Drosophila miranda Manfred Steinemann and Sigrid Steinemann Institut fur Genetik, Heinrich-Heine-Universitat Dusseldorf; 0-40225 Dusseldorf, Germany Manuscript received July 16, 1996 Accepted for publication October 17, 1996 ABSTRACT We have cloned a novel transposable element from the nepY chromosome of Drosophila miranda. The size of the element, designated asTRAM, is 3.452 bp, including on both sides long terminal direct repeats (LTRs)of 372 bp, respectively. The element is flanked by a 5-bp target site duplication, ATATG. The putative primer binding site (PBS) for minus-strand priming is complementary to 18 nucleotides of the 3"end of tRNATv. Data base screens for DNA sequence identities were negative, apart from the sequence motif of the PBS. The deduced amino acid sequence from the large ORF does not' reveal identities described for other transposons. In situ hybridizations with TRAM subclones show a biased distribution in the genome, with a massive accumulation of TRAM in the neo-Y chromosome, while the former homologue, the XZchromosomeis devoid of TRAMsites. The enriched occurrence of the TRAM element at the evolving neo-Y chromosome of D.miranda adds compelling evidencein favor of the view that Y chromosome degeneration is driven by the accumulation of transposable elements. CHROMOSOME degeneration (MULLER1918, polytene chromosome squashes, the male X chromo- Y 1932) is a process that involves structural changes some in Drosophila can be distinguished by the pres- in chromosome architecture and expansionof genetic ence of an isoform of histone H4 acetylated at lysine 16, inertness along theY chromosome (6CHARLESWORTH H4.Ac16. Staining D. miranda with H4.Ac16 antibodies 1978,1991,1996; LUCCHESI1978,1994; CHARLESWORTH showed that dosage compensation extends across part and CHARLESWORTH1979; BULL1983; RICE 1987,1994; of the X2 (STEINEMANNet al. 1996). The X2 shows a STEINEMANNand STEINEMANN1992). It is generally as- muchbrighter staining over -90% chromosome sumed that the heteromorphic sex chromosome pair length, reflecting thepredominant association of has developed from a pairof homologues. Causes of the H4.Ac16. A terminal region constituting -10% of the evolution of the structurally and functionally different X X2 chromosome is not labeled. This finding fits nicely and Y chromosomes have been the object of specula- with quantitative autoradiographic studies,showing tion sincethe discovery of sex chromosomes.To analyze that RNA synthesis in this region is not upregulated themolecular basis of this evolutionary process we (STROBELet al. 1978). chose a model system, Drosophila miranda. D. miranda Here we describe a novel LTR-retrotransposon cloned belongs to theAmerican representatives of the obscura fromthe neo-Y-chromosomal Lcpl-4 locus. While the group. The separationof D. mirandu from its next rela- neo-Y shows an enrichment of TRAM sites (-50-60), tives D. pseudoobscura and D. persimilis occurred relatively we find the former homologue, the X2 chromosome, recently, about 2 mya ago according to mtDNA restric- to be devoid of sites. Together with the distribution of tion analysis (BARRIOet al. 1992). Due to the fusion of the non-LTR TRIM retrotransposon (STEINEMANNand one of the autosomes to the Y chromosome, a neo-Y STEINEMANN1991) and the ISY3 insertionelements chromosome and a neo-X chromosome, designated as (STEINEMANNand STEINEMANN 1992, 1993),we present X2, were formed (DOBZHANSKY1935; MACKNIGHT 1939; compelling evidence that the first step in Y chromo- STEINEMANN1982). Thusformerly autosomal genes are some degeneration is driven by the accumulation of transmitted in association with the sex chromosomes. transposable elements, especially retrotransposons. We have cloned the larval cuticle protein (Lcp) genes from the X2 and neo-Y chromosome (STEINEMANNand MATERIALS AND METHODS STEINEMANN1990). Analyzing the DNA sequences from Cloning of the TRAM element from theneo-Y chromosome the X2and neo-Y region, we observed amassive accumu- and the homologous region on the X2 chromosome: High lation of DNA insertions on the neo-Y chromosome. In molecularweight DNA from D. miranda was isolatedac- cording to STEINEMANN1982. GenomicEMBL4 lambda librar- Corresponding author; Manfred Steinemann, Institutfur Genetik, ies from partial Sau3A (Boehringer Mannheim) digests were Heinrich HeineUnivenitat Dusseldorf, Univeniatsstr. 1, D40225 described in STEINEMANNand STEINEMANN(1990). Using a Dtisseldorf, FR Germany. polymorphic restriction site, overlapping clones with X2 or E-mail: [email protected] neo-Y chromosomal origin were isolated, covering -30 kb Genetics 145 261-266 (February, 1997) 262 Steinemann and Steinemann T terminalrepeat (LTR)-type (XIONGand EICKBUSH TRAM 1990). The 5'- and 3'-LTRs are 372 bp in size (Figure RA P 3). They show identical sequences except forone point H A PXhRX xcx cxh H mutation, an exchange of a C base us. T at position 17. I I I II Ill Ill I I1 I 4 " The internal central region of the TRAM element is + 4"- t- e bordered by sequences that are conserved in retrovi- 4 f" . - - 6 ruses. At the 5' end,a stretch of DNA shows sequence b"----) - - identity to the primer bindingsite (PBS), which is com- FIGURE1.-Restriction map of the TRAM element and se- plementary to 18 nucleotidesof the 3' end of the trypto- quencing strategy. Fragments were subcloned in Ml3mpl8/ 19 and sequenced on both strands. Arrows below the map phan tRNA (tRNA"rP). Indata base screens, we ob- indicate the sequencing strategy.H, HindIII; A, AccI; P, PstI; taineda 100% identity for this TRAM DNA region Xh, XhoI; R, EcoRI; X, XbaI; C, ClaI. (377-399, 23 bp) with Myeloblastosis-associated virus type 2 (accession number L10924), Rous sarcoma virus (RSV, from both locations, respectively (STEINEMANNand STEINE- 378-399, 22 bp; accession number U41731), chicken MANN 1990). For detailed restriction mapping, the regions c-erbB oncogene (378-399, 22 bp; accession number containing the Lcp genes on the X2 and neo-Y chromosome M10066, M13881) and chicken endogenous rav-RAV-0 were subcloned into pUCl8. The DNA was sequenced on both strands from M13mp18/19 subclones by the dideoxy chain avian virus (378-399,22 bp; accession numberJ02015). termination method accordingto the protocol suppliedwith The RTV PBS sequence is complementary to the ac- Sequenase (United States Biochemical). Forthe Xba-Xba frag- ceptorstem of the tRNA"'P (SCHWARTZet al. 1983). ments, we proved the correctorientation by sequencing from Thus, we conclude that TRAM could potentially use flanking sequences over the Xba sites (Figure 1). Standard tRNATrpto prime the replication of its minus strand. DNA techniques were carried out according to SAMBROOK, The 3' end of theinternal domain shows a short FRITSCHand MANIATIS (1989). Computer analysis: The DNA data base screening with polypurine tract (PPT), a characteristic domain in re- BLASTN (ALTSCHUL et ul. 1990) and the Genetics Computer troviruses, which is believed to serve as a primer for the Group SequenceAnalysis Package (DEVEREUXet al. 1984) was replication of the plus DNA strand (VARMUS1983). done using the updated (May 1996) EMBL and GenBank Integration site and codingcapacity of the TRAM nucleotide Sequence Data Library (EMBL, Heidelberg; Gen- Bank, NCBI, Washington). SwissProt data librarywas used for element: The TRAM element has integrated between the screening of the deduced amino acid sequence of the the Lcp3 and Lcp4 locus, 433 bp upstream of the tran- large TRAM ORF. The TRAM sequence is deposited in the scription start of the neo-Y chromosomal Lcp4 (Figure EMBL gene bank, accession number Y08905. 2). The elementhas induced a 5-bp target site duplica- Chromosome in situ hybridizationand D. miranda tion, ATATG (Figure 4). The site of integration of strains: D.miranda flies were cultured on standard Drosoph- ila food at 18". The 111/30 strain is an isoline from single TRAM lies within a sequence showing a palindrome females collected in the wild. D. miranda MPI is a strain of structure. Of interestis the notion that the neighboring unknown origin fromour laboratory. Fragmentsof the TRAM TRIM retrotransposon has integrated in a similar se- element were subcloned into pUCl8. The cloneswere labeled quence structure (STEINEMANNand STEINEMANN 1991). withBiotin-16-dUTP (Boehringer, Mannheim) by the nick In the latter case, the integration was accompanied by translation reaction and hybridized at 58" overnight to alkali an 11-bp deletion, while the integration oc- denatured chromosome squashes (STEINEMANNand STEINE- TRAM MANN 1991). The slides were washed three times in 2X SSC curred without one. In addition to the induced target at 53". Signal detection followed the protocol for immunoper- site duplication, we found two base substitutions at the oxidasestaining supplied with the DETEK I-hrp kit used right hand side of the integration site (Figure 4). (Enzo Diagnostics, New York). The intensity and contrast of The deduced aminoacid sequence of the TRAM ele- the diaminobenzidine (DAB) precipitate were enhanced us- ment reveals one large open reading frame of ing a silver DAB enhancement kit (Amersham). Photomicro- (OW) graphs of the chromosome squasheswere made with an Agfa- 2013 bp (positions 1092-3104) with the first methio- pan 25 film. nine at position 1158. The ORF terminates within the 3'-LTR. Data base screening with the
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