SINE-derived satellites in scaled reptiles

Mobile DNA (2023) 14:21 Vassetzky et al. Mobile DNA https://doi.org/10.1186/s13100-023-00309-2 Open Access RESEARCH SINE‑derived satellites in scaled reptiles Nikita S. Vassetzky1,2*, Sergei A. Kosushkin2 and Alexey P. Ryskov1 Abstract Background The genomes of many eukaryotes contain DNA repeats in the form of both tandem and interspersed elements with distinct structure, evolutionary histories, and mechanisms of emergence and amplification. Although there is considerable knowledge regarding their diversity, there is little evidence directly linking these two types. Results Different tandem repeats derived from portions of short interspersed elements (SINEs) belonging to different families were identified in 56 genomes of squamate reptiles. All loci of SINE-derived satellites (sSats) were thoroughly analyzed. Snake sSats exhibited high similarity in both structure and copy number, while other taxa may have highly diverse (geckos), rare (Darevskia lizards), or missing sSats (agamid lizards). Similar to most satellites associated with heterochromatin, sSats are likely linked to subtelomeric chromosomal regions. Conclusions Discovered tandem repeats derived from SINEs exhibit satellite-like properties, although they have not amplified to the same degree as typical satellites. The autonomous emergence of distinct sSats from diverse SINE families in numerous squamate species suggests a nonrandom process of satellite genesis originating from repetitive SINEs. Keywords Satellite DNA, Tandem repeats, SINEs, Retrotransposons, Squamata, Reptilia, Evolution Background Eukaryotic genomes contain two primary types of repetitive elements: tandem repeats and transposable (interspersed) elements. These elements are highly diverse, comprising many classes within a genome and differing in structure, genomic organization, and amplification mechanisms. Primarily, tandem repeats are organized in long arrays of relatively short non-coding sequences called satellites. Satellites are typically categorized into two or three classes: micro-, mini- and regular satellites. However, sometimes minisatellites are placed in both the *Correspondence: Nikita S. Vassetzky 1 Institute of Gene Biology of the Russian Academy of Sciences, Moscow 119334, Russia 2 Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow 119991, Russia micro- and satellite categories. We will follow the division into microsatellites (simple repeats) and proper satellites [1]. Satellite DNAs exhibit variations in nucleotide sequence, sequence complexity, repeat unit length, and abundance. However, they do share two essential features: organization into lengthy arrays of tandem headto-tail repeats and association with heterochromatic (telomeric or centromeric) regions [2]. The content of satellite DNA varies from 0.5% to more than 50% in animal genomes [1]. Different genomes may contain satellite families specific to certain species, while others may be shared across numerous taxa. However, most satellite families within a species have unrelated sequences. For example, the human genome contains nine satellite families with the predominant α-satellite comprising over half of total satellite DNA [1]. Structural roles of satellite DNA in chromosome organization, pairing, and segregation have been proposed. Telomeric and centromeric regions stabilize the © The Author(s) 2023. 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The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Vassetzky et al. Mobile DNA (2023) 14:21 chromatin at these sites for effective interactions with DNA-binding proteins, which is crucial for kinetochore formation and chromosomal segregation during mitosis and meiosis. Subtelomeric satellites stabilize chromosomal ends in a sequence-independent manner [1]. A different type of DNA repeats are transposable elements that comprise two classes: retrotransposons and DNA transposons. Retrotransposons utilize RNA-mediated mechanisms and a copy-and-paste process in their amplification, while DNA transposons rely on DNAmediated mechanisms and a cut-and-paste process. Short interspersed elements (SINEs) and long interspersed elements (LINEs) are the most abundant repetitive elements in higher eukaryotes, with SINEs outnumbering LINEs in most vertebrates and plants [3]. SINEs do not encode any proteins and their amplification is dependent on the enzymes of the cell and the partner LINEs. SINEs originate from a limited number of “master” copies, which can vary over time and give rise to numerous subfamilies [4]. SINEs are predominantly found in euchromatin [5]. Certain retrotransposons have distinct evolutionary relationships, such as the 3′-terminal region of a typical SINE originating from its partner LINE. Some SINE families, mostly in mammals, include (TC)n stretches, which resemble microsatellites in both structure and behavior; these structures are hypervariable sites within SINEs [4]. The structure of a SINE typically comprises four distinct regions: a head derived from one of three types of cellular RNAs transcribed by RNA polymerase III (most commonly, tRNA); a body whose origin and function remain largely unknown; a LINE-derived region (LDR) the region necessary for recognition of SINE RNA by the LINE machinery; and a tail composed of a variable-length sequence of simple repeats. This pattern is applicable to three SINE families, Sauria/Squam1 (here referred to as Squam1 to avoid confusion with the Sauria taxonomic name), Squam2, and Squam3, which are relevant to this study [4]. Despite their differing structures and amplification mechanisms, transposable elements and satellites can share similar sequences, suggesting evolutionary relationships. Segments of transposons can be amplified as satellites as reported for LTR retrotransposons, LINEs, SINEs, and DNA transposons. We analyzed a limited number of published SINE-satellite examples and found them inconclusive. Please refer to specific reviews for information about other TE origins o (...truncated)