Structural and Functional Characterization of Ribosomal Protein Gene Introns in Sponges

Abstract

Ribosomal protein genes (RPGs) are a powerful tool for studying intron evolution. They exist in all three domains of life and are much conserved. Accumulating genomic data suggest that RPG introns in many organisms abound with non-protein-coding-RNAs (ncRNAs). These ancient ncRNAs are small nucleolar RNAs (snoRNAs) essential for ribosome assembly. They are also mobile genetic elements and therefore probably important in diversification and enrichment of transcriptomes through various mechanisms such as intron/exon gain/loss. snoRNAs in basal metazoans are poorly characterized. We examined 449 RPG introns, in total, from four demosponges: Amphimedon queenslandica, Suberites domuncula, Suberites ficus and Suberites pagurorum and showed that RPG introns from A. queenslandica share position conservancy and some structural similarity with “higher” metazoans. Moreover, our study indicates that mobile element insertions play an important role in the evolution of their size. In four sponges 51 snoRNAs were identified. The analysis showed discrepancies between the snoRNA pools of orthologous RPG introns between S. domuncula and A. queenslandica. Furthermore, these two sponges show as much conservancy of RPG intron positions between each other as between themselves and human. Sponges from the Suberites genus show consistency in RPG intron position conservation. However, significant differences in some of the orthologous RPG introns of closely related sponges were observed. This indicates that RPG introns are dynamic even on these shorter evolutionary time scales.

Functional and Structural Characterization of FAU Gene/Protein from Marine Sponge Suberites domuncula

“…The most conserved intron position separates the UBQ from RPS30 domain in FAU and varies from 25 to 3339 bp. The average value of sponge RPG intron length is 164 bp [ 29 ], while human RPGs have significantly longer introns, with the average length of 760 bp [ 30 ]. Transposable element insertions play an important role in the evolution of intron size [ 31 ].…”

“…It is known that snoRNAs can change their genomic location within relatively short vertebrate evolutionary time scales [ 35 ]. Since all of examined RPG intron positions were conserved in three Suberites species, it was presumed that on this shorter evolutionary time scale, mobility of snoRNAs is not a significant factor that determines intron dynamics [ 29 ]. However, we found that within the same genus ( Suberites ), SNORA62 can change its genomic location.…”

“…The secondary structure of snoRNA was computed using the RNAfold program of the Vienna RNA Package [ 53 ]. Isolation of small RNAs from sponge was described previously [ 29 ]. In brief, fresh specimens of S. domuncula were cut into pieces, frozen in liquid nitrogen and grounded to a fine powder.…”

Sponges: A Reservoir of Genes Implicated in Human Cancer

“…Many ribosomal protein genes (RPGs) have additional extraribosomal functions, being involved in replication, regulation of cell growth, apoptosis, and cancer development [ 58 ]. RPs have shown to be important tools for studying intron evolution, since the analysis of RPG introns in sponges revealed the same rate of conservancy between two different sponge species compared to the conservancy between sponges and humans [ 59 , 60 ]. Since S30 ribosomal protein is produced from the fusion protein transcribed from the pro-apoptotic regulatory gene FAU, its extraribosomal function may be connected to the regulation of apoptosis [ 57 ].…”