Transcription of highly repetitive tandemly organized DNA in amphibians and birds: A historical overview and modern concepts

<p>Tandemly organized highly repetitive DNA sequences are crucial structural and functional elements of eukaryotic genomes. Despite extensive evidence, satellite DNA remains an enigmatic part of the eukaryotic genome, with biological role and significance of tandem repeat transcripts remaining rather obscure. Data on tandem repeats transcription in amphibian and avian model organisms is fragmentary despite their genomes being thoroughly characterized. Review systematically covers historical and modern data on transcription of amphibian and avian satellite DNA in somatic cells and during meiosis when chromosomes acquire special lampbrush form. We highlight how transcription of tandemly repetitive DNA sequences is organized in interphase nucleus and on lampbrush chromosomes. We offer LTR-activation hypotheses of widespread satellite DNA transcription initiation during oogenesis. Recent explanations are provided for the significance of high-yield production of non-coding RNA derived from tandemly organized highly repetitive DNA. In many cases the data on the transcription of satellite DNA can be extrapolated from lampbrush chromosomes to interphase chromosomes. Lampbrush chromosomes with applied novel technical approaches such as superresolution imaging, chromosome microdissection followed by high-throughput sequencing, dynamic observation in life-like conditions provide amazing opportunities for investigation mechanisms of the satellite DNA transcription.</p

Additional file 1: Table S1. of Mutual maintenance of di- and triploid Pelophylax esculentus hybrids in R-E systems: results from artificial crossings experiments

List of studied European water frogs from the R-E systems in Eastern Ukraine. (XLSX 18 kb

Interstitial (TTAGGG)_n repeat sites mapping allows to identify parental chromosomes in oocytes of hybrid frogs.

<p>(a-c) FISH mapping of (TTAGGG)_n repeat on metaphase chromosomes of <i>P</i>. <i>lessonae</i> (a, a`), <i>P</i>. <i>ridibundus</i> (b), and diploid <i>P</i>. <i>esculentus</i> (c). One or two interstitial (TTAGGG)<sub>n</sub> repeat sites distinguish parental NOR-bearing chromosomes H (arrows). Asterisks indicate enlarged fragment with two NOR-bearing chromosomes of <i>P</i>. <i>lessonae</i>. Arrows indicate interstitial (TTAGGG)<sub>n</sub> repeat sites. (d1–f1`) Lampbrush chromosomes from oocytes of triploid hybrid frogs with RRL (d1–d6`) and LLR (e1–f1`) genotypes. FISH mapping of (TTAGGG)_n repeat revealed lampbrush chromosome H corresponding to <i>P</i>. <i>ridibundus</i> (d6) or <i>P</i>. <i>lessonae</i> (e1) LBC H. Interstitial (TTAGGG)_n repeat sites are shown by square brackets. Lampbrush chromosomes corresponding to <i>P</i>. <i>ridibundus</i> LBC F (d1,d1`), G (d2,d2`), D (d3,d3`), I (d4,d4`), B (d5,d5`), and <i>P</i>. <i>lessonae</i> LBC B (e2,b2`), F (e3,b3`), L (f1,f1`) are shown. Chromosomes on micrographs (d1–d6`) were taken from the full lampbrush chromosome set represented on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123304#pone.0123304.g001" target="_blank">Fig 1a,a`</a>. Chromosomes on micrographs (e1–e3`) were taken from the from the full lampbrush chromosome set represented on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123304#pone.0123304.g001" target="_blank">Fig 1c,c`</a>. Various marker structures are shown by arrows. Chromosomes were counterstained with DAPI. Corresponding phase-contrast micrographs are shown (d1`,d2`,d3`,d4`,d5`,d6`,e1`,e2`,e3`,f1`). Arrowheads indicate centromeres. Scale bars = 10 μm for all panels except a`, where scale bar = 2 μm.</p

Suggested additional mechanisms of oogenesis in two triploid frogs with RRL genotype and one diploid hybrid frog.

<p>(a) During oogenesis of one triploid frog with RRL genotype neither elimination nor endoreplication occurred to form oocytes with 39 univalents (at the top), endoreplication of all genomes took place to form oocytes with 39 bivalents (in the middle), individual chromosomes from L genome (blue) were lost to form oocytes with aneuploid chromosomal sets (at the bottom). (b) During oogenesis of another triploid frog with RRL genotype elimination of L genome (blue) occurred to form oocytes with 13 bivalents (at the top), premeiotic elimination and endoreplication were absent to form oocytes with 39 univalents (in the middle), endoreplication of all genomes took place to form oocytes with 39 bivalents (at the bottom). (c) During oogenesis of one diploid hybrid frog L genome (blue) was eliminated in all observed oocytes. One round of R genome (orange) endoreplication occurred but bivalents formation was incomplete to form oocytes with both univalents and bivalents (at the top). Two rounds of endoreplication of R genome took place to form oocytes 26 bivalents (in the middle). One round of R genome endoreplication occurred but bivalents could not form that led to formation of oocytes with 26 univalents (at the bottom).</p

Suggested mechanisms of oogenesis typical for triploid hybrid frogs with RRL genotype and diploid hybrid frogs.

<p>(a) During oogenesis of the majority of triploid hybrids with RRL genotype from studied population systems of R-E type, L genome (blue) was eliminated while two remaining R genomes (brown and orange) without endoreplication formed 13 bivalents. (b) In oogenesis of the majority of diploid hybrids with RL genotype from studied population systems of R-E type, L genome (blue) was eliminated and the remaining R genome (orange) was endoreplicated to form 13 bivalents.</p