A Long-Term Conserved Satellite DNA That Remains Unexpanded in Several Genomes of Characiformes Fish Is Actively Transcribed.

Rodrigo Milan Calegari,Rodrigo Zeni Dos Santos,Silvana Melo,Duílio Mazzoni Zerbinato De Andrade Silva,Fausto Foresti,Francisco J Ruiz-Ruano,Ricardo Utsunomia,Fábio Porto-Foresti,Claudio Oliveira,Marcela Uliano-Silva

doi:10.1093/gbe/evab002

Abstract

Eukaryotic genomes contain large amounts of repetitive DNA sequences, such as tandemly repeated satellite DNAs (satDNAs). These sequences are highly dynamic and tend to be genus- or species-specific due to their particular evolutionary pathways, although there are few unusual cases of conserved satDNAs over long periods of time. Here, we used multiple approaches to reveal that an satDNA named CharSat01-52 originated in the last common ancestor of Characoidei fish, a superfamily within the Characiformes order, ∼140–78 Ma, whereas its nucleotide composition has remained considerably conserved in several taxa. We show that 14 distantly related species within Characoidei share the presence of this satDNA, which is highly amplified and clustered in subtelomeric regions in a single species (Characidium gomesi), while remained organized as small clusters in all the other species. Defying predictions of the molecular drive of satellite evolution, CharSat01-52 shows similar values of intra- and interspecific divergence. Although we did not provide evidence for a specific functional role of CharSat01-52, its transcriptional activity was demonstrated in different species. In addition, we identified short tandem arrays of CharSat01-52 embedded within single-molecule real-time long reads of Astyanax paranae (536 bp–3.1 kb) and A. mexicanus (501 bp–3.9 kb). Such arrays consisted of head-to-tail repeats and could be found interspersed with other sequences, inverted sequences, or neighbored by other satellites. Our results provide a detailed characterization of an old and conserved satDNA, challenging general predictions of satDNA evolution.

Highlights

Satellite DNAs are noncoding tandemly repeated sequences that constitute large portions of eukaryotic genomes, with head-to-tail arrays reaching up to hundreds of thousands of nucleotides (Lopez-Flores and Garrido-Ramos 2012; Plohl et al 2012)
To delimit the occurrence of CharSat01-52, we searched for this satellite DNAs (satDNAs) in the genomes of several fish species by using multiple approaches
CharSat01-52 exhibits the main features of an authentic tandem repeat in almost all the sampled Characoidea species, as evidenced by the ladder-like pattern of PCR amplification and the tandem-repeated structure of RepeatExplorer contigs (Novak et al 2013)

Summary

Introduction

Satellite DNAs (satDNAs) are noncoding tandemly repeated sequences that constitute large portions of eukaryotic genomes, with head-to-tail arrays reaching up to hundreds of thousands of nucleotides (Lopez-Flores and Garrido-Ramos 2012; Plohl et al 2012) These sequences are preferably found on the heterochromatin of pericentromeric and subtelomeric regions, their occurrence in euchromatic areas has been reported (Plohl et al 2012; Garrido-Ramos 2015; Ruiz-Ruano et al 2016; Silva et al 2017). In the context of concerted evolution and the general absence of functional selective constraints, satDNA sequences are frequently reported as being species or genus specific, with few examples of satellite repeats being conserved over a long period of time (e.g., more than 50 Myr) (Plohl et al 2012; Lorite et al 2017; Halbach et al 2020)

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Results

Conclusion