Satellite DNA-Like Elements Associated With Genes Within Euchromatin of the Beetle Tribolium castaneum

Abstract

In the red flour beetle Tribolium castaneum the major TCAST satellite DNA accounts for 35% of the genome and encompasses the pericentromeric regions of all chromosomes. Because of the presence of transcriptional regulatory elements and transcriptional activity in these sequences, TCAST satellite DNAs also have been proposed to be modulators of gene expression within euchromatin. Here, we analyze the distribution of TCAST homologous repeats in T. castaneum euchromatin and study their association with genes as well as their potential gene regulatory role. We identified 68 arrays composed of TCAST-like elements distributed on all chromosomes. Based on sequence characteristics the arrays were composed of two types of TCAST-like elements. The first type consists of TCAST satellite-like elements in the form of partial monomers or tandemly arranged monomers, up to tetramers, whereas the second type consists of TCAST-like elements embedded with a complex unit that resembles a DNA transposon. TCAST-like elements were also found in the 5′ untranslated region (UTR) of the CR1-3_TCa retrotransposon, and therefore retrotransposition may have contributed to their dispersion throughout the genome. No significant difference in the homogenization of dispersed TCAST-like elements was found either at the level of local arrays or chromosomes nor among different chromosomes. Of 68 TCAST-like elements, 29 were located within introns, with the remaining elements flanked by genes within a 262 to 404,270 nt range. TCAST-like elements are statistically overrepresented near genes with immunoglobulin-like domains attesting to their nonrandom distribution and a possible gene regulatory role.

Structural and functional liaisons between transposable elements and satellite DNAs

“…However, a reverse could be also possible by capturing already existing tandem repeats by a TE (Kejnovsky et al 2006;Macas et al 2009). In favor of this assumption is the presence of 1.2 monomer of highly abundant centromeric satDNA of the beetle Tribolium castaneum in the 5′-UTR of a retrotransposon dispersed throughout the genome (Brajković et al 2012).…”

“…Such mechanism could represent an alternative pathway that explains the presence of satDNA monomers in TEs, as well as in other genome segments. Transposition potential of satDNA monomer(s) alone is evident from examples where they were found inserted into diverse non-homologous repetitive or non-repetitive sequences including in the vicinity of genes (for example, DiBartolomeis et al 1992;Plohl et al 2010;Kuhn et al 2012;Brajković et al 2012;Meštrović et al 2013).…”

“…Based on comparison with the Crassostrea gigas orthologues genes that lack inserted repetitive elements, authors conclude that insertions might induce divergences in gene functioning and also contribute to accumulation of differences between species (Kourtidis et al 2006a). Copies of TCAST satDNA of the beetle T. castaneum were found embedded in a transposon-like structure with long TIRs and are statistically overrepresented in the relative vicinity of nine immunoglobulin-like genes (Brajković et al 2012). Another example of putative functionality is indicated for the MITE miDNA4 of the frog Xenopus which incorporates one or several satDNA motifs, also found as independent units outside of this element (Scalvenzi and Pollet 2014).…”

Adjacent sequences disclose potential for intra-genomic dispersal of satellite DNA repeats and suggest a complex network with transposable elements

“…However, observed exceptions to this rule can be either because junctions were recently formed or because monomers are not homogenized by unequal crossover at all, for example, if arrays are too short and/or isolated from the rest [19, 26, 27], or are supposed to evolve under constraints [20, 21]. In any case, considering the available data, satDNA sequence ends mostly form well-defined junctions, irrespective of whether they are between different satDNAs [26–29], satDNAs and TEs [22, 30], or satDNAs and other sequences [20, 31]. …”

First evidence of DNA methylation in insectTribolium castaneum

“…In addition, it could result in the activation and spreading of repetitive elements within euchromatin and their insertion near genes. 41 Certain insertions of repetitive elements could alter gene expression and enhance adaptation under stress conditions. 42,43 Preservation of satellite DNA methylation in all developmental stages of T. castaneum indicates the importance of this epigenetic modification for the maintenance of low transcription levels and a silent heterochromatin state.…”