Linking maternal and somatic 5S rRNA types with different sequence-specific non-LTR retrotransposons

Abstract

5S rRNA is a ribosomal core component, transcribed from many gene copies organized in genomic repeats. Some eukaryotic species have two 5S rRNA types defined by their predominant expression in oogenesis or adult tissue. Our next-generation sequencing study on zebrafish egg, embryo, and adult tissue identified maternal-type 5S rRNA that is exclusively accumulated during oogenesis, replaced throughout the embryogenesis by a somatic-type, and thus virtually absent in adult somatic tissue. The maternal-type 5S rDNA contains several thousands of gene copies on chromosome 4 in tandem repeats with small intergenic regions, whereas the somatic-type is present in only 12 gene copies on chromosome 18 with large intergenic regions. The nine-nucleotide variation between the two 5S rRNA types likely affects TFIII binding and riboprotein L5 binding, probably leading to storage of maternal-type rRNA. Remarkably, these sequence differences are located exactly at the sequence-specific target site for genome integration by the 5S rRNA-specific Mutsu retrotransposon family. Thus, we could define maternal-and somatic-type MutsuDr subfamilies. Furthermore, we identified four additional maternal-type and two new somatic-type MutsuDr subfamilies, each with their own target sequence. This target-site specificity, frequently intact maternal-type retrotransposon elements, plus specific presence of Mutsu retrotransposon RNA and piRNA in egg and adult tissue, suggest an involvement of retrotransposons in achieving the differential copy number of the two types of 5S rDNA loci.

Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development

“…This is in line with the observations that somatic rRNAs are first transcribed during gastrulation in amphibian embryogenesis (Brown and Caston 1962;Brown and Littna 1964). Although we and others have found 5S rRNA variation in various organisms (Wegnez et al 1972;Komiya et al 1986;Martins and Wasko 2004;Locati et al 2017), to our knowledge there has never been a report on differentially expressed 5.8S, 18S, and 28S rRNA types in any animal. Taken together, these data suggest that there are maternal-type and somatic-type ribosomes.…”

“…Much like we discovered before with zebrafish 5S rRNA (Locati et al 2017), there is one 5.8S, 18S, and 28S rRNA FIGURE 1. Expression of the maternal-and somatic-type rRNA types in zebrafish development.…”

“…1A, 2B). This is in contrast to the sequence differences between maternaland somatic-type 5S rRNA, which are mainly present in the 5 ′ half (Locati et al 2017). In the LSU, 5.8S rRNA is bound to 28S via three basepaired elements ( Fig.…”

“…Thus this oocyte-variant probably evolved to enable the production of the enormous amount of 5S rRNA in oocytes equivalent to that of hundreds of thousands of somatic cells (Brown 2004). Recently, we reported similar 5S rRNA variants in zebrafish (Locati et al 2017), in which a maternaltype 5S r|RNA (2330 genes on chromosome 4) makes up virtually all oocyte 5S rRNA, which is completely replaced during embryogenesis by the somatic-type (12 genes on chromosome 18). 5S rRNA specificity during development has also been discovered in various other species (Komiya et al 1986;Martins et al 2002;Martins and Wasko 2004;Danzmann et al 2007).…”

“…Intriguingly, the zebrafish maternal-type 45S rDNA locus is located on the long arm of the chromosome 4, where the maternal-type 5S gene cluster is found (Locati et al 2017). This genomic region is also known for its abundance of tRNA genes, scarcity of protein-coding genes, and extensive heterochromatin (≈transcriptional silencing) in somatic cells (Howe et al 2013).…”