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Home , Long terminal repeat, LTR retrotransposon, P element

Commentary

Long terminal repeat jump between species

Andrew J. Flavell*

Department of Biochemistry, University of Dundee, Medical Sciences Institute͞Wellcome Trust Building Complex, Dow Street, Dundee DD1 5EH, Scotland etrotransposons are an evolutionarily species, but copia is absent from many between these two species. The Rancient class of mobile genetic ele- willistoni strains (6). Jordan et al. (6) have of D. melanogaster, which gained fame as ments that transpose replicatively within cloned and sequenced a fragment of the a vector for germ-line transformation of their host via RNA intermediates. D. willistoni copia. This 1-kilobase frag- that species, has been transferred from the There are three major ment is identical to the most famous and D. willistoni subgroup, probably in this groups, the Ty1-copia group and the gypsy well used copia clone, the white-apricot century (11). The two transfers of mobile group (LTR) retro- copia that was isolated from a spontane- elements have thus been reciprocal. More- transposons and the non-LTR retrotrans- ous insertion of copia into the white locus over, these two transposons are mechanis- posons or LINE elements (ref. 1; Fig. 1). All of D. melanogaster (9, 10). Total sequence tically very distinct from each other; the P three groups are widespread in the eu- conservation of a retrotransposon across element is a classical DNA transposable karyotes, although none of the LTR retro- the 50-million-year gap that separates element that uses a DNA transposition transposon groups have been detected in these two species is simply unbelievable; intermediate. Any mechanism proposed mammals or birds as yet. All LTR retro- thus, either the transposon has jumped to explain both transfers must take these transposons share striking sequence similar- between the two species much more re- observations into account. ities with the of vertebrates, and cently than their common ancestor, or What possible mechanisms are there? at least one LTR retrotransposon of Dro- there was some kind of contamination The evolutionary gap between these two sophila is in fact an infectious (2). artifact in the experiment. Indeed, this species is almost certainly too large for It is universally believed that modern day observation set an alarm bell ringing for even an abortive mating (M. Ashburner, retroviruses, LTR retrotransposons, and me, because this particular copia is also a personal communication); thus, the an- non-LTR retrotransposons share a common clone that most fly labs have in their swer must be that a vector was responsible ancestor, though there is some dispute fridges and freezers. However, the white- for the transfer. The most plausible can-

about which came first (1, 3, 4). apricot copia is also very successful at didate is a parasite with a broad species COMMENTARY Retrotransposons may look a lot like transposing in real flies, and it is reason- range, such as the mite Proctolaelaps re- retroviruses, but they are not by them- able to suppose that it was the one that was galis, which was proposed as a vector for selves infectious. The basic difference be- lucky enough to jump across into D. will- the transfer of the P element (12). This tween a retrotransposon and a retrovirus istoni. The authors were no doubt as wor- hypothesis is attractive, because this mite is the retrotransposon’s lack of an enve- ried as I and have carried out a formidable feeds on Drosophila eggs by punching lope glycoprotein . This crucial dif- series of controls to prove beyond any holes, sucking out the contents, and then ference prohibits the formation of an ex- reasonable doubt that the D. willistoni moving on. P. regalis is a messy eater that tracellular infectious virus particle, leav- does in fact contain integrated does not kill every egg that it attacks, and ing the retrotransposon virus-like particle copia that is virtually identical to the white- it is reasonable to assume that it could marooned inside its host cell (5). LTR apricot copia. The usual negative controls transfer small amounts of the contents of retrotransposons cannot normally transfer are all there to show that the tubes and one egg into another. Such a procedure themselves between adjacent cells; they solutions are clean. Southern analysis could easily induce the transfer of the P certainly cannot move readily from one shows that there is a significant amount of element, and it is very plausible that trans- animal to another, and even more cer- copia present in the D. willistoni genome— fer of the copia virus-like particle would tainly, they cannot transfer horizontally not the tiny amount that would suggest also result in horizontal transfer. from one species into another. In that contamination—and two further rigorous The egg interior is the cytoplasm of a very case, why is there a paper in this issue of PCR controls prove that the D. willistoni large single cell, and the cytoplasm is a PNAS that proves beyond all reasonable DNA samples contain absolutely no con- known intracellular location of the copia doubt that an LTR retrotransposon called taminating copies of two D. melanogaster virus-like particle (13), which contains all of copia has been transferred from one spe- . Lastly, a D. willistoni genomic li- the necessary machinery for introducing a cies of Drosophila, Drosophila willistoni, brary has yielded a copia clone that is new copy of the retrotransposon into the into another, Drosophila melanogaster, identical to the white-apricot copia. genome. Unfortunately, this hypothesis is within the last 200 years (6)? Thus, copia has been transferred be- very difficult to substantiate in the labora- We will address that question a little tween two quite distantly related species tory. Nonetheless, it may well be that many later in the article, but first, let us quickly of Drosophila. These two species have of the possible classes of vector have at one review the evidence that supports the au- shared a host range for only the past 200 time or another managed to ferry trans- thor’s conclusions. The copia element of years. D. willistoni is a New World species posons from one species to another. Such D. melanogaster was among the first LTR and D. melanogaster was an African spe- possible vectors include other kinds of ani- retrotransposons to be discovered (7). It is cies until it began following humans—or, ubiquitous in D. melanogaster, and it has a to be more precise, their rotting fruit— broad distribution in other Drosophila spe- around the world. Moreover, in that time, See companion article on page 12621. cies (8). D. willistoni is a copia-containing another transposon has been transferred *To whom reprint requests should be addressed.

PNAS ͉ October 26, 1999 ͉ vol. 96 ͉ no. 22 ͉ 12211–12212 Downloaded by guest on September 30, 2021 Why is the horizontal transfer of retro- 28 and 29). The situation is even worse, transposons among multicellular eu- because every transposon must compete for karyotes particularly significant? All of the genomic space against the other mobile retroelements (genetic elements that use elements in the host. Finally, natural selec- reverse and RNA intermedi- tion against the accumulation of transpo- ates in their propagation) transpose replica- son-induced deleterious is con- tively, which leads to high levels of accumu- stantly eliminating all but the fittest individ- lation of these elements in many classes of uals. Drosophila may be a particularly organism. This phenomenon is particularly antagonistic environment for transposons, noticeable in mammals, birds, amphibians, because it has a small genome in which any and plants, where huge numbers of ancient transposition has a reasonable chance of relics of retrotransposons, retrovirus copies, knocking out a gene. This antagonistic en- and SINE elements accumulate, sometimes vironment is probably why Drosophila has to the point where they take up large frac- relatively few retrotransposons in euchro- tions of the total genome (20–22). In addi- matic regions (areas of open tion, it is commonly seen that the introduc- where most of the genes reside), but many of tion of a transposon into a new host genome stimulates the transposition of the mobile these transposons are apparently capable of Fig. 1. The simplest common structures of LINE ele- element many-fold (23–25). Finally, trans- transposition (Wei Li and A.F., unpublished ments (non-LTR retrotransposons), the two groups of position of retroelements results in gene observations). One of the biggest mysteries LTR retrotransposons and retrovirus . copia is for me is how so many different types of a Ty1-copia group LTR retrotransposon. Structural do- , causing a variety of genetic dis- mains: gag, core particle components; en, endonucle- eases, for example, in humans (26). There- transposons manage to coexist in such a ase; rt, ; LTR, long terminal repeat; difficult environment. There are at least 23 int, ; env, envelope glycoprotein. fore, it is very important to understand the extent to which horizontal transfer of retro- different LTR retrotransposons and retro- elements has occurred in the past histories viruses in the genome of D. melanogaster ͞͞ ͞ mal parasites, such as wasps (14) and nem- of higher , the effects that this alone (see http: fly.ebi.ac.uk:7081 trans- ͞ ͞ atode worms, or microorganisms like fungi transfer has had on the genomes of those posons lk melanogaster-transposon.html). or bacteria (14) or viruses themselves (15). organisms, and the mechanisms of the trans- Maybe horizontal transfer is useful for the All that the vector would need is a broad fers. mobile element, not so much to allow host range and the ability to gain access to Jordan et al. (6) favor the view that hor- these mobile elements to escape their the germ cells somehow. izontal transfer is a strategy for transposons antagonistic host environment, but to give Evidence is accumulating slowly and to escape an ‘‘arms race’’ between the nat- them time to mull over a few good ideas steadily that many classes of transposable ural tendency of the transposons to trans- for resisting that environment and per- element have been transferred horizontally pose and the evolution of host-mediated haps give the host time to forget how to between species. One of the most primitive mechanisms for repressing transposition (6, deal with them. Perhaps we should follow mobile elements, the group I , has 27). It is surely true that ‘‘bailing out’’ of an the lead of those who model host– probably invaded the mitochondrial ge- increasingly antagonistic ecological niche pathogen interactions (30) to come up nome of plants from fungi many times (16). could lead to an overall amplification in the with hypotheses for how horizontal trans- Other DNA transposons, in particular the number of transposons in existence. How- mission affects the evolution of retroele- ͞ mariner Tc1 superfamily seem to have been ever, this situation does nothing for the poor ments and their host genomes. particularly aggressive in their spread across wee transposons that are left behind, and, in the animal kingdom (17). LINE elements that donor species, the rules stay the same: I thank Margaret Kidwell for many helpful may have been transferred between snakes namely, multiply by transposition; perish by suggestions with this manuscript, Michael Ash- and mammals (18) and SINE elements random mutation; or, if you are extremely burner for his useful opinions concerning the ( of small RNA genes that are fortunate, become useful for the host (as has sexual practices of fruit flies, and Amar Kumar propagated via RNA intermediates) have been the case for the LINE elements that for information on the variety of LTR retro- probably moved between fish species (19). preserve the of Drosophila; refs. transposons in D. melanogaster.

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