Cassandraretrotransposons carry independently transcribed 5S RNA

Abstract

We report a group of TRIMs (terminal-repeat retrotransposons in miniature), which are small nonautonomous retrotransposons. These elements, named Cassandra, universally carry conserved 5S RNA sequences and associated RNA polymerase (pol) III promoters and terminators in their long terminal repeats (LTRs). They were found in all vascular plants investigated. Uniquely for LTR retrotransposons, Cassandra produces noncapped, polyadenylated transcripts from the 5S pol III promoter. Capped, read-through transcripts containing Cassandra sequences can also be detected in RNA and in EST databases. The predicted Cassandra RNA 5S secondary structures resemble those for cellular 5S rRNA, with high information content specifically in the pol III promoter region. Genic integration sites are common for Cassandra, an unusual feature for abundant retrotransposons. The 5S in each LTR produces a tandem 5S arrangement with an inter-5S spacing resembling that of cellular 5S. The distribution of 5S genes is very variable in flowering plants and may be partially explained by Cassandra activity. Cassandra thus appears both to have adapted a ubiquitous cellular gene for ribosomal RNA for use as a promoter and to parasitize an as-yet-unidentified group of retrotransposons for the proteins needed in its lifecycle.pol III ͉ genome evolution ͉ transcription ͉ transposable element R etrotransposons, excepting SINEs (short interspersed nuclear elements) and LINEs (long interspersed nuclear elements), resemble retroviruses in their structure and intracellular life cycle. They are ubiquitous in the genomes of plants, animals, and fungi and account for Ͼ50% of large plant genomes (1, 2). Their life cycle comprises transcription of genomic copies, translation of their encoded proteins, packaging of the transcripts into virus-like particles, reverse transcription, and targeting of the cDNA copy to the nucleus for integration into the genome (3, 4). The transcriptional signals for RNA polymerase II (pol II) are found in the long terminal repeats (LTRs) at either end of the element, flanking the priming sites for reverse transcription and the coding domain specifying the proteins needed for replication and integration [supporting information (SI) Fig. S1].In addition to the classical retrotransposons, several well conserved nonautonomous groups have been discovered that lack all or part of their coding capacity (5). The BARE2 elements cannot express the capsid protein GAG (6), and Morgane lacks most of its coding capacity (7). The TRIM (terminal repeat retrotransposon in miniature) and LARD (large retrotransposon derivative) elements (Fig. S1) entirely lack reading frames for retrotransposon proteins (8-12). The TRIM elements are composed of 100-to 250-bp LTRs, priming sites for reverse transcriptase, and a small intervening segment. Evidence for past mobility suggests that they are activated by transcomplementation (10). These have been found in at least 13 species from four plant families (9, 10).Here, we describe a group of TRIM elements, which w...

Systematic analysis and evolution of 5S ribosomal DNA in metazoans

“…Finally, our work supports the conclusions of various recent reports (Rooney and Ward, 2005;Kalendar et al, 2008;Vierna et al, 2009;Freire et al, 2010;Perina et al, 2011;Vierna et al, 2011;Vizoso et al, 2011), in which it was shown that the evolutionary patterns of 5S rDNA in animals are complex and cannot be explained only in the light of concerted evolution. Birth-and-death processes, selection, homogenizing mechanisms typically involved in concerted evolution Figure 7 Evolutionary-conserved linkages of 5S rRNA and mir-562.…”

“…They appear to be the result of stochastic processes within genomes with no effect on fitness, even though this has not been demonstrated (see Drouin and Moniz de Sá (1995) for a review). Interestingly, 5S rDNA repeats can show different organization modes in the same species (Little and Braaten, 1989), and their transposition could be frequent within genomes, as reported by Drouin and Moniz de Sá (1995); Kalendar et al (2008); Cohen et al (2010).…”

The linked units of 5S rDNA and U1 snDNA of razor shells (Mollusca: Bivalvia: Pharidae)

“…Drouin and Moniz de Sá (1995) hypothesised that a 5S rDNA transposition could be produced at the DNA level mediated by extrachromosomal circular DNA or by an RNA intermediate. Interestingly, recent surveys have given support to both hypothesis (Kalendar et al, 2008;Cohen et al, 2010). Similarily, Rooney and Ward, (2005) hypothesised that 5S rDNA was capable of multiplying and integrating into other areas of the genome through a process the same as, or similar to, retroposition, in filamentous fungi.…”

Two reported cytotypes of the emergent orchid model species Erycina pusilla are two different species

“…The divergent number and physical location of the 5S rDNA genes could be caused not only by chromosome rearrangement, including inversions, duplications, deletions and translocations (Hanson et al 1996;Thomas et al 1996;Raskina et al 2008;Wang et al 2013), but also by transposon-mediated transposition events (Raskina et al 2004;Altinkut et al 2006;Datson and Murray 2006). Several cases of 5S rDNAderived sequences being found within transposable elements have been reported (Kapitonov and Jurka 2003;Kalendar et al 2008). By contrast, loss of rDNA loci during evolution has occurred in Brassicaceae and Rosaceae (Mishima et al 2002;Hasterok et al 2006;Liu and Davis 2011).…”