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Like Retrotransposon (Transposable Dement/Interspedflc Hybridization/Zea/Tnpsacum/Waxy Alde) MICHAEL D

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Like Retrotransposon (Transposable Dement/Interspedflc Hybridization/Zea/Tnpsacum/Waxy Alde) MICHAEL D Proc. Nati. Acad. Sci. USA Vol. 91, pp. 11674-11678, November 1994 Evolution Molecular evolution of magellan, a maize Ty3/gypsy- like retrotransposon (transposable dement/interspedflc hybridization/Zea/Tnpsacum/waxy alde) MICHAEL D. PURUGGANAN*t AND SUSAN R. WESSLER*t§ Departments of *Botany and *Genetics, University of Georgia, Athens, GA 30602 Communicated by Wyatt W. Anderson, July 28, 1994 ABSTRACT The magelan transposable element is respon- Understanding the evolutionary biology of retrotrans- sible for a spontaneous 5.7-kb insertion in the maize wx-M posons requires data on the extent and patterns of molecular allele. This element has the sequence and structural charac- variation within element families. In this report, we describe teristics of a Ty3/gypsy-like retrotransposon. The maeln a low-copy-number retrotransposon whose presence within element is present in all Zea species and Tripsacum andersonu; the phylogenetically well-defined genus Zea makes it an It is absent, however, in the genomes of all other Tripsacum excellent subject for the study of retrotransposon evolution. species analyzed. The genetic distances between magellan ele- This Ty3/gypsy-like retrotransposon, which we have named ments suggest that this retrotransposon is evolving faster than magellan, is responsible for a 5.7-kb insertion in a sponta- other Zea nuclear loci. The phylogeny of magelan within Zea neous mutant allele of the maize waxy (wx) locus. The and T. andersonf also reveals a pattern of interspecies trans- magellan element is also found in Tripsacum andersonii but fers, resulting in the movement of mageflan subfmles be- is absent in all other Tripsacum species tested. We find that tween different species genomes. Interspecific hybridization this retrotransposon is evolving faster than other nuclear loci may be a major mechanism by which this retrotransposon and that interspecies transfer of magellan elements appears invades and establishes Itself in new taxa. to have occurred within the genus Zea.l Retrotransposons are a class of transposable elements that MATERIALS AND METHODS encode reverse transcriptase and transpose via an RNA Strains and General Techniques. Strains carrying the wx-M intermediate (1). The elements are widely distributed and allele were obtained from 0. Nelson (University of Wiscon- comprise a significant fraction of eukaryotic genomes. In sin). Seeds and genomic DNA of Zea (from J. Doebley, Drosophila melanogaster, retrotransposons such as copia, University of Minnesota) and Tripsacum (from S. White, gypsy, and 412 are believed to comprise nearly 2% of the University of Georgia) species were obtained as indicated. genome (1) and are responsible for as much as 80%o of Genomic DNA from 14-day-old maize seedlings was isolated spontaneous mutations (2). Retrotransposons have been de- by the method of Shure et al. (12). scribed in 11 plant taxa; most of these elements were dis- Element Isolation and Sequence Analysis. The wx-M inser- covered as restriction fragment length polymorphisms or as tion was previously localized by Southern blot analysis of preexisting insertions within nuclear loci (3, 36). Reverse genomic DNA (13). This insertion was cloned on a 7.8-kb Sal transcriptase sequences have also been isolated by PCR from I fragment following ligation of size-fractionated genomic 68 plant species, including bryophytes, pteridophytes, gym- DNA into the A vector ZAPII (Stratagene) and screening of nosperms, and angiosperms (4, 5). These reverse transcrip- recombinant phage with radioactively labeled wx probes. A tase sequences are presumably associated with yet uniden- 1.4 kb Sst I and a 5.2-kb Kpn I fragment containing the 3' and tified retroelements (5). 5' ends of the insertion, respectively, were subcloned into Although numerous retrotransposons have been isolated pUC119 and the insertion termini were sequenced (14). and characterized, relatively little is known about the mo- Both the 5' magellan termini and reverse transcriptase lecular evolution of these mobile sequences. The mode and sequences were analyzed separately by PCR amplification. tempo of retrotransposon evolution are largely undefined, The magellan 5'-terminal primer sequences are 5'-TGTCAG- and the forces that shape retrotransposon sequence evolution GAGACTGACGCAGC-3' (primer 1) and 5'-GGGTCGT- are poorly understood (4, 5, 37). It has been suggested by TGCGGTCTACTGC-3' (primer 2). The reverse transcrip- several workers that transposable elements evolve differ- tase sequences are 5'-CTAAGCTTTAYCAYCARHTNMG- ently from conventional nuclear loci, since transposons can NAT-3' (primer 3) and 5'-TCGAATTCTGNCCNARNM- move within genomes and contribute to genetic variation DYTYNAC-3' (primer 4). Primers 3 and 4 were designed to (6-10). Evolutionary rates between retrotransposon se- recognize conserved coding regions in Ty3/gypsy-like ele- quences may also differ significantly from the evolutionary ments (15). PCR conditions were as described (13); annealing rates of other nuclear genes (10). Several plant species, for temperatures as low as 520C were used in screening for the example, are known to harbor highly divergent reverse presence of magellan long terminal repeat (LTR) sequences. transcriptase sequences within their genomes (5, 6); the PCR amplification of magellan 5'-terminal sequences was heterogeneity of these sequences is attributed in part to the conducted with genomic DNAs from Zea mays ssp. mays, Z. high mutation rates associated with retrotransposition (5). mays ssp. mexicana, Z. mays ssp. parviglumis, Z. mays ssp. There is also evidence that retrotransposons may possess the huehuetenangensis, Z. luxurians, Z. diploperennis, Tripsac- ability to move horizontally across reproductive barriers that isolate species (5, 6, 11). Abbreviation: LTR, long terminal repeat. tPresent address: Department of Biology, 0116, University of Cal- ifornia at San Diego, La Jolla, CA 92093. The publication costs of this article were defrayed in part by page charge §To whom reprint requests should be addressed. payment. This article must therefore be hereby marked "advertisement" IThe sequences reported in this paper have been deposited in the in accordance with 18 U.S.C. §1734 solely to indicate this fact. GenBank data base (accession nos. U03916-U03968). 11674 Downloaded by guest on September 25, 2021 Evolution: Purugganan and Wessler Proc. Natl. Acad. Sci. USA 91 (1994) 11675 um andersonii, T. dactyloides, T. australe, T. peruvianum, A and T. cundinamarce as templates. The reverse transcriptase sequence was amplified from clones. PCR- Ty3 wx-M-containing Magellan CQQSUDRPQPLSPGQQMOR -GaSWTI amplified DNAs were cloned in pCRII by the TA cloning del COOVUAmHUG QPLPV RLUDXIIGVPLSUMsI procedure (Invitrogen) and sequenced by either the dideoxy sequencing method (Sequenase; United States Biochemical) Ty3 OOSS 000 *O@0 0 * *@ 0*0 or the automated sequencing facility of the University of Magellan Georgia Molecular Genetics Instrumentation Facility. del UVIV~mKSI'IPIH!!T8#Lh1LYK3IIRLTGIPTTIVTD Phylogenetic Analyses. magellan sequences were aligned contiguously beginning at nucleotide 30 of the 5' LTR, and Ty3 gaps were added by visual inspection to maximize similarity. Magellan D R D~~ 1 del ~~ RDIMR * * 000 *0S 0 Phylogenetic trees were inferred under maximum parsimony *. *-- *S 0 e*eA0000 *---00**es 0 * 0 *- 0* by using the heuristic search algorithm of the PAUP 3.0 program (16). magellan subfamilies were determined by B 00 OS 00 0 0 00 0 500 5 inferring within-species element phylogenies and identifying ry3 monophyletic element groups. These subfamilies contain a*gellan del RL-DIP MRTRGYZLVWIWVLfU NIPYID magellan copies that share at least 97% sequence similarity. * OOOS 0 05 00 000000 0 0 00 0 magellan copies whose sequence were closest to the element consensus for a subfamily were chosen as representatives for try3 I the groups; representative members from each subfamily Magellan UIWFSDIVLIYS-RQKSVNVLWXDDLIYSSKKHLVERQZLYmm3uBmQL8KcVWam Ifigcrno del KIPXV DYVRTYSRMMIMRX RI IQ were then used in all-ZealTripsacum analysis. The PHYLIP * *@ * *@00 ** *-0 * *00* @ 3.3 package (17) was utilized in computing pairwise Kimura two-parameter DNA distances (18) under a transition/ FIG. 2. Alignment of the integrase (A) and reverse transcriptase transversion ratio of2. Both sequence and distance data were (B) domains of magellan, yeast Ty3, and Lilium del retrotrans- also used for tree building under the DNAPARS and neighbor- posons. Dashes indicate gaps. Amino acid residues which are identical between magellan and the adjacent sequences are indicated joining PHYLIP algorithms. by dots. Ty3 and del sequences are from refs. 15 and 20. RESULTS mageflan Sequences Within the Genera Zea and Tripsacum. The presence of magellan within the genera Zea and Structure of the Retrotransposon Insertion in wx-M. The Tripsacum was assayed in a PCR survey using primers that wx-M allele was previously shown to contain a 5.7-kb inser- recognize the magellan 5' LTR and an internal magellan tion in a Sal I fragment that spans exons 1-9 of the 14 exons sequence (Fig. 3A). These primers were located ""590 bp of the maize wx gene (19). The wx-M insertion was isolated apart. A fragment of approximately this size was detected and found to be located within wx exon 3 just 2 bp down- following PCR amplification of genomic DNA from Zea stream of the intron 2/exon 3 splice junction. The insertion and T. has some of the structural features of a retrotransposon (see species andersonii. However, no PCR
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