Satellite DNA Modulates Gene Expression in the Beetle Tribolium castaneum after Heat Stress

Abstract

Non-coding repetitive DNAs have been proposed to perform a gene regulatory role, however for tandemly repeated satellite DNA no such role was defined until now. Here we provide the first evidence for a role of satellite DNA in the modulation of gene expression under specific environmental conditions. The major satellite DNA TCAST1 in the beetle Tribolium castaneum is preferentially located within pericentromeric heterochromatin but is also dispersed as single repeats or short arrays in the vicinity of protein-coding genes within euchromatin. Our results show enhanced suppression of activity of TCAST1-associated genes and slower recovery of their activity after long-term heat stress relative to the same genes without associated TCAST1 satellite DNA elements. The level of gene suppression is not influenced by the distance of TCAST1 elements from the associated genes up to 40 kb from the genes’ transcription start sites, but it does depend on the copy number of TCAST1 repeats within an element, being stronger for the higher number of copies. The enhanced gene suppression correlates with the enrichment of the repressive histone marks H3K9me2/3 at dispersed TCAST1 elements and their flanking regions as well as with increased expression of TCAST1 satellite DNA. The results reveal transient, RNAi based heterochromatin formation at dispersed TCAST1 repeats and their proximal regions as a mechanism responsible for enhanced silencing of TCAST1-associated genes. Differences in the pattern of distribution of TCAST1 elements contribute to gene expression diversity among T. castaneum strains after long-term heat stress and might have an impact on adaptation to different environmental conditions.

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

“…Low sequence variability of satDNA monomers has also been observed when their short segments are located in the proximity of genes. It was hypothesized that low sequence variability can in this case be a consequence of possible roles in gene regulation and/or chromatin structure [20, 21, 52]. …”

“…Analysis of sequence variability performed on the 1.688 satDNA of Drosophila [20] and on satDNAs of the beetle Tribolium castaneum [19] showed that satDNA copies located in euchromatic chromosomal domains evolve under similar rules as their counterparts in heterochromatic compartments. A heat-stress induced regulatory mechanism of transient genome-wide heterochromatinization has been recently proposed in T. castaneum as a possible functional role of isolated euchromatic satDNA copies [21]. …”

“…SatDNA monomers at array ends often show enhanced level of decay, a phenomenon considered to be a consequence of the lack of sequence homogenization of terminal repeats by unequal crossover [22–25]. 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].…”

Diversity and distribution of alpha satellite DNA in the genome of an Old World monkey: Cercopithecus solatus

“…In almost all eukaryotes, the DNA underlying centromeres is made of large tracts of nearly identical tandem DNA repeats, known as satellite DNA [1–3]. The remarkable variation of satellite DNAs between species has been an enigma ever since their discovery and different important roles have been ascribed to these sequences, from the imperative centromeric function in mitosis and meiosis to regulatory functions [4, 5]. …”

CpSAT-1, a transcribed satellite sequence from the codling moth, Cydia pomonella

“…Finally, satDNA can influence gene expression, such as TCAST1 in the beetle Tribolium castaneum, which has been shown to suppress the expression of various proteincoding genes after heat shock (Feliciello et al 2015). SatDNAs performing a structural or functional role may contain various functional motifs, such as binding sites for centromeric proteins (e.g.…”