Vertical inheritance and bursts of transposition have shaped the evolution of the BS non-LTR retrotransposon in Drosophila

Granzotto, Adriana; Lopes, Fabrício Ramon; Vieira, Cristina; Carareto, Claudia M. A.

doi:10.1007/s00438-011-0629-9

Cited by 12 publications

(17 citation statements)

References 61 publications

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“…Interestingly, BS appears to be transpositionally active in D. melanogaster but inactive in D. simulans [73]. One interpretation is that BS was active in the common ancestor and regulated by Hmr and Lhr .…”

Section: Discussionmentioning

confidence: 99%

The Hmr and Lhr Hybrid Incompatibility Genes Suppress a Broad Range of Heterochromatic Repeats

et al. 2014

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Hybrid incompatibilities (HIs) cause reproductive isolation between species and thus contribute to speciation. Several HI genes encode adaptively evolving proteins that localize to or interact with heterochromatin, suggesting that HIs may result from co-evolution with rapidly evolving heterochromatic DNA. Little is known, however, about the intraspecific function of these HI genes, the specific sequences they interact with, or the evolutionary forces that drive their divergence. The genes Hmr and Lhr genetically interact to cause hybrid lethality between Drosophila melanogaster and D. simulans, yet mutations in both genes are viable. Here, we report that Hmr and Lhr encode proteins that form a heterochromatic complex with Heterochromatin Protein 1 (HP1a). Using RNA-Seq analyses we discovered that Hmr and Lhr are required to repress transcripts from satellite DNAs and many families of transposable elements (TEs). By comparing Hmr and Lhr function between D. melanogaster and D. simulans we identify several satellite DNAs and TEs that are differentially regulated between the species. Hmr and Lhr mutations also cause massive overexpression of telomeric TEs and significant telomere lengthening. Hmr and Lhr therefore regulate three types of heterochromatic sequences that are responsible for the significant differences in genome size and structure between D. melanogaster and D. simulans and have high potential to cause genetic conflicts with host fitness. We further find that many TEs are overexpressed in hybrids but that those specifically mis-expressed in lethal hybrids do not closely correlate with Hmr function. Our results therefore argue that adaptive divergence of heterochromatin proteins in response to repetitive DNAs is an important underlying force driving the evolution of hybrid incompatibility genes, but that hybrid lethality likely results from novel epistatic genetic interactions that are distinct to the hybrid background.

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Section: Discussionmentioning

confidence: 99%

The Hmr and Lhr Hybrid Incompatibility Genes Suppress a Broad Range of Heterochromatic Repeats

et al. 2014

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“…Non-LTR retrotransposons are common elements in Drosophila genomes and are often described as vertically inherited in this group of species (Malik et al 1999; Granzotto et al 2011). I- like element sequences have been found in many species, and their distribution correlates with the phylogenetic relationships between species (Bucheton et al 1992), which indicates that they are old components of Drosophila genomes.…”

Section: Discussionmentioning

confidence: 99%

Specific Activation of an I-Like Element in Drosophila Interspecific Hybrids

Carnelossi¹,

Lerat²,

Henri³

et al. 2014

Genome Biology and Evolution

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The non-long terminal repeat (LTR) retrotransposon I, which belongs to the I superfamily of non-LTR retrotransposons, is well known in Drosophila because it transposes at a high frequency in the female germline cells in I–R hybrid dysgenic crosses of Drosophila melanogaster. Here, we report the occurrence and the upregulation of an I-like element in the hybrids of two sister species belonging to the repleta group of the genus Drosophila, D. mojavensis, and D. arizonae. These two species display variable degrees of pre- and postzygotic isolation, depending on the geographic origin of the strains. We took advantage of these features to explore the transposable element (TE) dynamics in interspecific crosses. We fully characterized the copies of this TE family in the D. mojavensis genome and identified at least one complete copy. We showed that this element is transcriptionally active in the ovaries and testes of both species and in their hybrids. Moreover, we showed that this element is upregulated in hybrid males, which could be associated with the male-sterile phenotype.

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“…As MITEs are generally <600 bp, size and sequence homogeneity (Feschotte et al . 2002), their copy numbers were calculated based on the following criteria: 1) All fragments showed more than 80% identity and coverage to their consensus sequences and 2) fragments were considered to be a single insertion when they were separated by less than 200 bp (Granzotto et al 2011). Meanwhile, there were two subfamilies of MITEs identified in lizard ( ConanN1_AC and ConanN2_AC ) and the length of ConanN1_AC was about 150 bp longer than that of ConanN2_AC .…”

Section: Methodsmentioning

confidence: 99%

Recurrent Horizontal Transfers of Chapaev Transposons in Diverse Invertebrate and Vertebrate Animals

Zhang

Feschotte

Han

et al. 2014

Genome Biology and Evolution

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Horizontal transfer (HT) of a transposable element (TE) into a new genome is regarded as an important force to drive genome variation and biological innovation. In addition, HT also plays an important role in the persistence of TEs in eukaryotic genomes. Here, we provide the first documented example for the repeated HT of three families of Chapaev transposons in a wide range of animal species, including mammals, reptiles, jawed fishes, lampreys, insects, and in an insect bracovirus. Multiple alignments of the Chapaev transposons identified in these species revealed extremely high levels of nucleotide sequence identity (79–99%), which are inconsistent with vertical evolution given the deep divergence time separating these host species. Rather, the discontinuous distribution amongst species and lack of purifying selection acting on these transposons strongly suggest that they were independently and horizontally transferred into these species lineages. The detection of Chapaev transposons in an insect bracovirus indicated that these viruses might act as a possible vector for the horizontal spread of Chapaev transposons. One of the Chapaev families was also shared by lampreys and some of their common hosts (such as sturgeon and paddlefish), which suggested that parasite–host interaction might facilitate HTs.

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Vertical inheritance and bursts of transposition have shaped the evolution of the BS non-LTR retrotransposon in Drosophila

Cited by 12 publications

References 61 publications

The Hmr and Lhr Hybrid Incompatibility Genes Suppress a Broad Range of Heterochromatic Repeats

The Hmr and Lhr Hybrid Incompatibility Genes Suppress a Broad Range of Heterochromatic Repeats

Specific Activation of an I-Like Element in Drosophila Interspecific Hybrids

Recurrent Horizontal Transfers of Chapaev Transposons in Diverse Invertebrate and Vertebrate Animals

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