Abstract
In the flour beetle, Tribolium castaneum (peri)centromeric heterochromatin is mainly composed of a major satellite DNA TCAST1 interspersed with minor satellites. With the exception of heterochromatin, clustered satellite repeats are found dispersed within euchromatin. In order to uncover a possible satellite DNA function within the beetle genome, we analysed the expression of the major TCAST1 and a minor TCAST2 satellite during the development and upon heat stress. The results reveal that TCAST1 transcription was strongly induced at specific embryonic stages and upon heat stress, while TCAST2 transcription is stable during both processes. TCAST1 transcripts are processed preferentially into piRNAs during embryogenesis and into siRNAs during later development, contrary to TCAST2 transcripts, which are processed exclusively into piRNAs. In addition, increased TCAST1 expression upon heat stress is accompanied by the enrichment of the silent histone mark H3K9me3 on the major satellite, while the H3K9me3 level at TCAST2 remains unchanged. The transcription of the two satellites is proposed to be affected by the chromatin state: heterochromatin and euchromatin, which are assumed to be the prevalent sources of TCAST1 and TCAST2 transcripts, respectively. In addition, distinct regulation of the expression might be related to diverse roles that major and minor satellite RNAs play during the development and stress response.
Highlights
RNAs are involved in chromatin modification by directing the installation of the heterochromatin mark H3K9me3 at their homologous genomic targets, which leads to transcriptional silencing [1,2]. small interfering RNAs (siRNAs) are 21–22 nt long and are derived from repetitive sequences, in particular from satellite DNAs, and their role in heterochromatin establishment has been demonstrated in the yeast Schizosaccharomyces pombe, plants and insects [3,4,5]
PiRNAs, which are ~26–30 nt long, mostly derive from transposon sequences and their major role is to repress transposon activity at both the transcriptional and translational level [6]. piRNAs are expressed in the animal germ line with the primary aim of protecting genome integrity, but they are present in the somatic tissues of many arthropods [7]. siRNAs and piRNAs differ in their biogenesis, while siRNA is derived from long double stranded transcripts processed by the endonuclease Dicer [8], piRNAs are derived from long single-stranded precursors, which are processed by a unique set of proteins [9,10]
On the antisense DNA strand, the abundant piRNAs and siRNAs map to a region between 180–240 bp during embryogenesis, while in adults, abundant TCAST1 siRNAs are derived from the position 180–220 bp and this profile is not changed upon heat stress (Figure 3)
Summary
RNAs (piRNAs) are involved in chromatin modification by directing the installation of the heterochromatin mark H3K9me at their homologous genomic targets, which leads to transcriptional silencing [1,2]. siRNAs are 21–22 nt long and are derived from repetitive sequences, in particular from satellite DNAs, and their role in heterochromatin establishment has been demonstrated in the yeast Schizosaccharomyces pombe, plants and insects [3,4,5]. TCAST1 transcription is strongly induced by heat stress (HS) and is accompanied by an increase in repressive histone marks H3K9me2/3 at TCAST1 repeats, resulting in the transient suppression of TCAST1-associated gene expression [23]. It is not known whether other T. castaneum satellites exhibit features similar to TCAST1 with respect to a burst of transcripts during embryogenesis and upon HS, followed by their processing into small RNAs, and if their transcripts can affect the H3K9me level at homologous satellite repeats upon HS. Our findings reveal a distinct regulation of expression of different satellite DNAs during the development and upon environmental stress and we discuss the diverse roles that their transcripts might play during these processes, regarding heterochromatin establishment and maintenance, as well as the modulation of nearby genes expression
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