Tirant is a new member of the gypsy family of
retrotransposons in Drosophila melanogaster
J. Cañizares, M. Grau, N. Paricio, and M.D. Moltó
Abstract: In this paper, we propose a consensus sequence for a putative complete Tirant retrotransposon. Several
defective copies, as well as relevant sequences available in databases have been analyzed. The putative complete Tirant
element is 8533 bp long, and presents all the structural features of a retroviruslike transposable element of the gypsy
family. It contains three ORFs (open reading frames) that encode putative products resembling the retroviral Gag, Pol,
and Env proteins. Southern blot analyses show that complete and defective Tirant elements are widespread in
Drosophila melanogaster. The different hybridization patterns observed in several natural populations of this species
suggest that Tirant is an active element.
Key words: Drosophila, LTR-retrotransposon, gypsy, retrovirus, envelope protein, phylogeny.
Résumé : Les auteurs proposent ici une séquence consensus qui représente possiblement un rétrotransposon Tirant
complet. Plusieurs copies incomplètes de même que des séquences apparentées présentes dans les banques de données
ont été analysées. La séquence potentiellement complète d’un élément Tirant mesure 8533 pb et présente toutes les
caractéristiques de structure d’un élément transposable de la famille gypsy (type rétrovirus). Elle comprend trois ORF
codant pour des produits putatifs qui ressemblent aux protéines rétrovirales Gag, Pol et Env. Des analyses Southern
montrent que des copies complètes et incomplètes de l’élément Tirant sont très répandues dans le génome du
Drosophila melanogaster. Les divers motifs d’hybridation observés chez plusieurs populations naturelles de cette espèce
pourraient suggérer que l’élément Tirant est actif.
Mots clés : Drosophila, rétrotransposon LTR, gypsy, rétrovirus, protéine de l’enveloppe, phylogénie.
[Traduit par la Rédaction] Cañizares et al. 14
Introduction
Retrotransposons are eukaryotic mobile elements that uti-
lize RNA intermediates and reverse transcription to spread
throughout the genome of their hosts. Some of them are
flanked by long terminal repeats (LTRs) and, depending on
this property, they can be classified as either LTR or non-
LTR retrotransposons (Finnegan 1989).
Numerous families of LTR retrotransposons have been
identified in invertebrates, mainly in Drosophila, where
about 15 independent families are well characterized so far
(Arkhipova et al. 1995a). These elements show strong simi-
larities to vertebrate retroviruses in genetic structure as well
as in replication mechanism, and are classified into three
groups depending on their overall gene organization. The
first group is composed of elements that possess only one
open reading frame (ORF) encoding putative Gag and Pol
proteins, such as copia (Mount and Rubin 1985) and micro-
pia (Lankenau et al. 1988) elements. In the second group,
these proteins are encoded by two slightly overlapping
ORFs, as is the case of 412 (Yuki et al. 1986a), 1731
(Fourcade-Peronnet et al. 1988), and mdg1 (Avedisov et al.
1990). Finally, there is a small group of LTR retrotrans-
posons that are most similar to vertebrate retroviruses, since
they contain a third ORF that corresponds in size, location,
and structure to the retroviral env gene. In addition, they
show the retroviral organization of the functional domains in
the pol gene (Varmus and Brown 1989). So far, these ele-
ments have been only identified in insects, i.e., 17.6 (Saigo
et al. 1984), gypsy (Marlor et al. 1986), 297 (Inouye et al.
1986), and ZAM (Leblanc et al. 1997) in D. melanogaster,
tom in D. ananassae (Tanda et al. 1988), and TED in the
lepidopteran Trichoplusia ni (Friesen and Nissen 1990).
Moreover, it has been shown that the third ORF in the
D. melanogaster gypsy element encodes a fully functional
Env protein (Kim et al. 1994; Song et al. 1994), suggesting
that gypsy is a true infectious retrovirus in invertebrates.
In this work, we describe in detail the molecular structure
of Tirant, a new member of the gypsy family of D. melano-
gaster retrotransposons. It was first identified as a 5.7-kb in-
sertion in the extramacrochaetae (emc) gene, causing the
dominant mutation Achaetous (Ach, Garrell and Modolell
1990). Further analyses confirmed that this insertion is
flanked by two LTRs, and contains moderately repeated
DNA (Moltó et al. 1996). Other mutations associated with
insertions of Tirant in different loci have been recently de-
scribed in D. melanogaster (Thomas et al. 1995; Viggiano et
al. 1997; Wu and Gibson 1998). In order to define the struc-
Genome 43: 9–14 (2000) © 2000 NRC Canada
9
Corresponding Editor: P.B. Moens.
Received March 30, 1999. Accepted July 1, 1999.
J. Cañizares, M. Grau, N. Paricio
1
, and M.D. Moltó.
Departament de Genètica, Facultat de Ciències Biològiques,
Universitat de València, Dr. Moliner, 50; 46100–Burjassot,
Spain.
1
Author to whom all correspondence should be addressed
(e-mail: nuria.paricio@uv.es).