Mobilization of retrotransposons as a cause of chromosomal diversification and rapid speciation: the case for the Antarctic teleost genus Trematomus.

BACKGROUND: The importance of transposable elements (TEs) in the genomic remodeling and chromosomal rearrangements that accompany lineage diversification in vertebrates remains the subject of debate. The major impediment to understanding the roles of TEs in genome evolution is the lack of comparative and integrative analyses on complete taxonomic groups. To help overcome this problem, we have focused on the Antarctic teleost genus Trematomus (Notothenioidei: Nototheniidae), as they experienced rapid speciation accompanied by dramatic chromosomal diversity. Here we apply a multi-strategy approach to determine the role of large-scale TE mobilization in chromosomal diversification within Trematomus species. RESULTS: Despite the extensive chromosomal rearrangements observed in Trematomus species, our measurements revealed strong interspecific genome size conservation. After identifying the DIRS1, Gypsy and Copia retrotransposon superfamilies in genomes of 13 nototheniid species, we evaluated their diversity, abundance (copy numbers) and chromosomal distribution. Four families of DIRS1, nine of Gypsy, and two of Copia were highly conserved in these genomes; DIRS1 being the most represented within Trematomus genomes. Fluorescence in situ hybridization mapping showed preferential accumulation of DIRS1 in centromeric and pericentromeric regions, both in Trematomus and other nototheniid species, but not in outgroups: species of the Sub-Antarctic notothenioid families Bovichtidae and Eleginopsidae, and the non-notothenioid family Percidae. CONCLUSIONS: In contrast to the outgroups, High-Antarctic notothenioid species, including the genus Trematomus, were subjected to strong environmental stresses involving repeated bouts of warming above the freezing point of seawater and cooling to sub-zero temperatures on the Antarctic continental shelf during the past 40 millions of years (My). As a consequence of these repetitive environmental changes, including thermal shocks; a breakdown of epigenetic regulation that normally represses TE activity may have led to sequential waves of TE activation within their genomes. The predominance of DIRS1 in Trematomus species, their transposition mechanism, and their strategic location in "hot spots" of insertion on chromosomes are likely to have facilitated nonhomologous recombination, thereby increasing genomic rearrangements. The resulting centric and tandem fusions and fissions would favor the rapid lineage diversification, characteristic of the nototheniid adaptive radiation.

Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae.

Tnt1 elements are a superfamily of LTR-retrotransposons distributed in the Solanaceae plant family and represent good model systems for studying regulatory and evolutionary controls established between hosts and transposable elements. Tnt1 retrotransposons tightly control their activation, by restricting expression to specific conditions. The Tnt1A element, originally discovered in tobacco, is expressed in response to stress, and its activation by microbial factors is followed by amplification, demonstrating that factors of pathogen origin can generate genetic diversity in plants. The Tnt1A promoter has the potential to be activated by various biotic and abiotic stimuli but a number of these are specifically repressed in tobacco and are revealed only when the LTR promoter is placed in a heterologous context. We propose that a tobacco- and stimulus-specific repression has been established in order to minimize activation in conditions that might generate germinal transposition. In addition to tight transcriptional controls, Tnt1A retrotransposons self-regulate their activity through gradual generation of defective copies that have reduced transcriptional activity. Tnt1 retrotransposons found in various Solanaceae species are characterized by a high level of variability in the LTR sequences involved in transcription, and have evolved by gaining new expression patterns, mostly associated with responses to diverse stress conditions. Tnt1A insertions associated with genic regions are initially favored but seem subsequently counter-selected, while insertions in repetitive DNA are maintained. On the other hand, amplification and loss of insertions may result from more brutal occurrences, as suggested by the large restructuring of Tnt1 populations observed in tobacco compared to each of its parental species. The distribution of Tnt1 elements thus appears as a dynamic flux, with amplification counterbalanced by loss of insertions. Tnt1 insertion polymorphisms are too high to reveal species relationships in the Nicotiana genus, but can be used to evaluate species relationships in the Lycopersicon and Capsicum genera. This also demonstrates that the behavior of Tnt1 retrotransposons differs between host species, most probably in correlation to differences in expression conditions and in the evolutionary and environmental history of each host.

Characterization of natural populations of Drosophila melanogaster with regard to the hobo system: a new hypothesis on the invasion.

Until now, with regard to the hobo system of hybrid dysgenesis, natural populations of Drosophila melanogaster have been investigated using only two criteria: at the molecular level, the presence or absence of XhoI fragments 2.6 kb long or smaller; and/or at the genetic level, the ability to induce gonadal dysgenesis sterility in crosses A (females of an E reference strain crossed with males under test) and A* (females under test crossed with males of an H reference strain). Recently, analyses of laboratory strains using these criteria as well as the mobilization of two reporter genes, the male recombination and the number of 'TPE' repeats in the S region, revealed a lack of correlation between the different dysgenic parameters themselves, and also between these parameters and the molecular characteristics of the strains. Thirteen current strains derived from world populations were therefore investigated with regard to all these dysgenic traits, to determine discriminating criteria providing a robust method of classifying natural populations and deducing the dynamics of hobo elements in these populations. We show, as in laboratory strains, a lack of correlation between the parameters studied. Therefore, the significance of each of them as well as the nature of hobo hybrid dysgenesis are discussed, to propose an analysis method of the hobo system applicable to natural populations. According to the geographical distribution of hobo activities in world populations and to the variable polymorphism of the number of 'TPE' repeats, we propose a new scenario for the invasion of D. melanogaster by hobo elements.

A scenario for the hobo transposable element invasion, deduced from the structure of natural populations of Drosophila melanogaster using tandem TPE repeats.

Temporal surveys of hobo transposable elements in natural populations reveal a historical pattern suggesting a recent world-wide invasion of D. melanogaster by these transposons, perhaps following a recent horizontal transfer. To clarify the dynamics of hobo elements in natural populations, and thus to provide further data for our understanding of the hobo invasion, TPE tandem repeats, observed in the polymorphic S region of the element, were used as molecular markers. The number of TPE repeats was studied in 101 current populations from around the world, and in 63 strains collected in the past. This revealed a geographical distribution which seems to have been stable since the beginning of the 1960s. This distribution is compatible with a number of hypotheses for the dynamics of hobo elements. We propose a scenario based on an invasion in two stages: first, a complete invasion by elements with three TPE repeats, followed by the beginning of a new invasion involving hobo elements with five or seven repeats.

Characterization of permissivity for hobo-mediated gonadal dysgenesis in Drosophila melanogaster.

The hobo transposon is responsible for one of the three hybrid dysgenic systems that have been described in Drosophila melanogaster. Most studies on the hobo dysgenic system have been carried out using the PM system as a reference. However, these two systems differ significantly. In particular, several studies have failed to find any correlation between the molecular structures of hobo elements, the instability of the transposon and the incidence of gonadal dysgenic (GD) sterility. On the other hand, no study of the ability of females to permit hobo activity in their progeny when they are crossed with males harboring active hobo elements (permissivity) has yet been reported. In order to investigate the parameters involved in hobo permissivity, four E strains were studied with regard to the molecular nature of their hobo sequences and the GD sterility induced by a controlled source of hobo transposase. We show that hobo permissivity varies both within and between E strains. Moreover, permissivity decreases with age in E females. Our results are discussed with respect to similar phenomena that have been described in relation to the reactivity of the IR dysgenic system.

The mobility of the tobacco Tnt1 retrotransposon correlates with its transcriptional activation by fungal factors.

We have analyzed the stress-induced amplification of the tobacco Tnt1 element, one of the rare active plant retrotransposons. Tnt1 mobility was monitored using the retrotransposon-anchored SSAP strategy that allows the screening of multiple insertion sites of high copy number elements. We have screened for Tnt1 insertion polymorphisms in plants regenerated from mesophyll leaf cells, either via explant culture or via protoplast isolation. The second procedure includes an overnight exposure to fungal extracts known to induce high levels of Tnt1 transcription. Newly transposed Tnt1 copies were detected in nearly 25% of the plants regenerated via protoplast isolation, and in less than 3% of the plants derived from explant culture. These results show that Tnt1 transcription is followed by transposition, and that fungal extracts efficiently activate Tnt1 mobility. Transcription appears to be the key step to controlling Tnt1 amplification, as newly transposed Tnt1 copies show high sequence similarities to the subpopulations of transcribed Tnt1 elements. Our results provide direct evidence that factors of microbial origin are able to induce retrotransposon amplification in plants, and strengthen the hypothesis that stress modulation of transposable elements might play a role in generating host genetic plasticity in response to environmental stresses.