Characterization of repeat arrays in ultra‐long nanopore reads reveals frequent origin of satellite DNA from retrotransposon‐derived tandem repeats

Vondrak, Tihana; Robledillo, Laura Ávila; Novák, Petr; Koblížková, Andrea; Neumann, Pavel; Macas, Jiří

doi:10.1111/tpj.14546

Cited by 79 publications

(101 citation statements)

References 64 publications

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“…Thirteen satellite DNA families whose genome abundance differ ~10–1000 times have been recorded in the pea centromeres [ 7 ], confirming that tandem organization is favorable, while abundance of a tandem repeat could be less determinative criteria for centromeric assortment. In addition to satellites, retroelements can be equally important or even dominant centromere components [ 43 ], and contribution of retrotransposons to functional centromeres have been documented in different animal, plant and fungal lineages [ 43 – 47 ]. In T .…”

Section: Discussionmentioning

confidence: 99%

CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum

et al. 2020

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Centromeres are chromosomal domains essential for kinetochore assembly and correct chromosome segregation. Inconsistent in their underlying DNA sequences, centromeres are defined epigenetically by the presence of the centromere-specific histone H3 variant CenH3. Most of the analyzed eukaryotes have monocentric chromosomes in which CenH3 proteins deposit into a single, primary constriction visible at metaphase chromosomes. Contrary to monocentrics, evolutionary sporadic holocentric chromosomes lack a primary constriction and have kinetochore activity distributed along the entire chromosome length. In this work, we identified cCENH3 protein, the centromeric H3 histone of the coleopteran model beetle Tribolium castaneum . By ChIP-seq analysis we disclosed that cCENH3 chromatin assembles upon a repertoire of repetitive DNAs. cCENH3 in situ mapping revealed unusually elongated T . castaneum centromeres that comprise approximately 40% of the chromosome length. Being the longest insect regional centromeres evidenced so far, T . castaneum centromeres are characterized by metapolycentric structure composed of several individual cCENH3-containing domains. We suggest that the model beetle T . castaneum with its metapolycentromeres could represent an excellent model for further studies of non-canonical centromeres in insects.

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Section: Discussionmentioning

confidence: 99%

CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum

et al. 2020

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“…The presence of long tandem arrays in currently available sequence assemblies is limited by the assemblies being based on short-read DNA sequencing approaches, which can tend to pile up tandem repeats. As assemblies based on the newer long-read sequencing techniques such as those of Oxford Nanopore or Pacific Biosciences [32,33] appear, the problem of under-representation of repeat numbers in tandem arrays should decrease. Table 1.…”

Section: Introductionmentioning

confidence: 99%

Long Tandem Arrays of Cassandra Retroelements and Their Role in Genome Dynamics in Plants

Kalendar

Raskina

Belyayev

et al. 2020

IJMS

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Retrotransposable elements are widely distributed and diverse in eukaryotes. Their copy number increases through reverse-transcription-mediated propagation, while they can be lost through recombinational processes, generating genomic rearrangements. We previously identified extensive structurally uniform retrotransposon groups in which no member contains the gag, pol, or env internal domains. Because of the lack of protein-coding capacity, these groups are non-autonomous in replication, even if transcriptionally active. The Cassandra element belongs to the non-autonomous group called terminal-repeat retrotransposons in miniature (TRIM). It carries 5S RNA sequences with conserved RNA polymerase (pol) III promoters and terminators in its long terminal repeats (LTRs). Here, we identified multiple extended tandem arrays of Cassandra retrotransposons within different plant species, including ferns. At least 12 copies of repeated LTRs (as the tandem unit) and internal domain (as a spacer), giving a pattern that resembles the cellular 5S rRNA genes, were identified. A cytogenetic analysis revealed the specific chromosomal pattern of the Cassandra retrotransposon with prominent clustering at and around 5S rDNA loci. The secondary structure of the Cassandra retroelement RNA is predicted to form super-loops, in which the two LTRs are complementary to each other and can initiate local recombination, leading to the tandem arrays of Cassandra elements. The array structures are conserved for Cassandra retroelements of different species. We speculate that recombination events similar to those of 5S rRNA genes may explain the wide variation in Cassandra copy number. Likewise, the organization of 5S rRNA gene sequences is very variable in flowering plants; part of what is taken for 5S gene copy variation may be variation in Cassandra number. The role of the Cassandra 5S sequences remains to be established.

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“…Novel satDNAs can arise from the amplification of unique sequences through replication slippage [19,20], unequal exchange, rolling circle replication [4,[21][22][23], or even from transposable elements (TEs) [24][25][26]. However, much of the species-level differences in satDNA arises through movement and divergence of ancestral satellites inherited through common decent [27].…”

Section: Introductionmentioning

confidence: 99%

Dynamic evolution of euchromatic satellites on the X chromosome inDrosophila melanogasterand thesimulansclade

Sproul

Khost

Eickbush

et al. 2019

Preprint

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ABSTRACTSatellite DNAs (satDNAs) are among the most dynamically evolving components of eukaryotic genomes and play important roles in genome regulation, genome evolution, and speciation. Despite their abundance and functional impact, we know little about the evolutionary dynamics and molecular mechanisms that shape satDNA distributions in genomes. Here we use high-quality genome assemblies to study evolutionary dynamics of two complex satDNAs, Rsp-like and 1.688 gm/cm3, in Drosophila melanogaster and its three nearest relatives in the simulans clade. We show that large blocks of these repeats are highly dynamic in the heterochromatin, where their genomic location varies across species. We discovered that small blocks of satDNA that are abundant in X chromosome euchromatin are similarly dynamic, with repeats changing in abundance, location, and composition among species. We detail the proliferation of a rare satellite (Rsp-like) across the X chromosome in D. simulans and D. mauritiana. Rsp-like spreads by inserting into existing clusters of the older, more abundant 1.688 satellite, in events that were likely facilitated by microhomology-mediated repair pathways. We show that Rsp-like is abundant on extrachromosomal circular DNA in D. simulans, which may have contributed to its dynamic evolution. Intralocus satDNA expansions via unequal exchange and the movement of higher-order repeats also contribute to the fluidity of the repeat landscape. We find evidence that euchromatic satDNA repeats experience cycles of proliferation and diversification somewhat analogous to bursts of transposable element proliferation. Our study lays a foundation for mechanistic studies of satDNA proliferation and the functional and evolutionary consequences of satDNA movement.

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Characterization of repeat arrays in ultra‐long nanopore reads reveals frequent origin of satellite DNA from retrotransposon‐derived tandem repeats

Cited by 79 publications

References 64 publications

CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum

CenH3 distribution reveals extended centromeres in the model beetle Tribolium castaneum

Long Tandem Arrays of Cassandra Retroelements and Their Role in Genome Dynamics in Plants

Dynamic evolution of euchromatic satellites on the X chromosome inDrosophila melanogasterand thesimulansclade

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