The spread of the first introns in proto-eukaryotic paralogs

Abstract

Spliceosomal introns are a unique feature of eukaryotic genes. Previous studies have established that many introns were present in the protein-coding genes of the last eukaryotic common ancestor (LECA). Intron positions shared between genes that duplicated before LECA could in principle provide insight into the emergence of the first introns. In this study we use ancestral intron position reconstructions in two large sets of duplicated families to systematically identify these ancient paralogous intron positions. We found that 20–35% of introns inferred to have been present in LECA were shared between paralogs. These shared introns, which likely preceded ancient duplications, were wide spread across different functions, with the notable exception of nuclear transport. Since we observed a clear signal of pervasive intron loss prior to LECA, it is likely that substantially more introns were shared at the time of duplication than we can detect in LECA. The large extent of shared introns indicates an early origin of introns during eukaryogenesis and suggests an early origin of a nuclear structure, before most of the other complex eukaryotic features were established.

Integrating Phylogenetics With Intron Positions Illuminates the Origin of the Complex Spliceosome

“…In a previous study, we investigated the spread of introns in proto-eukaryotic paralogs ( Vosseberg et al 2022 ). Intron positions that are shared between genes that duplicated during eukaryogenesis are likely shared because they were present in the gene before it duplicated.…”

“…Subsequent expansions resulted from the numerous gene duplications that we observed. These duplications enabled us to assess the extent of intron positions that were shared between paralogs and likely predated the duplication event ( Vosseberg et al 2022 ). Our ancestral intron position reconstructions support the presence of introns in almost half of the proteins before their recruitment into the spliceosome.…”

“…In sharp contrast to a probably intron-rich LECA ( Csuros et al 2011 ; Vosseberg et al 2022 ) with a complex spliceosome, prokaryotic genes lack spliceosomal introns, which must have emerged at some time during eukaryogenesis. Spliceosomal introns and the key spliceosomal protein PRPF8 are thought to derive from self-splicing group II introns in prokaryotic genomes.…”

“…This is based on similarities in the splicing reaction, function, and structure of the RNAs involved, as well as the homology inferred between the spliceosomal protein PRPF8 and the single protein encoded by group II introns, the intron-encoded protein (IEP) ( Zimmerly and Semper 2015 ). Recent work has suggested that the emergence of intragenic introns might have been an early event during eukaryogenesis ( Vosseberg et al 2022 ). The evolutionary histories of a few gene families in the spliceosome have been described ( Anantharaman et al 2002 ; Veretnik et al 2009 ; Califice et al 2012 ) and they suggest that gene duplications played a pivotal role in the emergence of the complex spliceosome.…”

Analysis on the interactions between the first introns and other introns in mitochondrial ribosomal protein genes

“…The first introns have gained increasing attentions in recent years because of their unique features that are located in close proximity to the transcription, and the distinct deposition of epigenetic marks and nucleosome density on the first intronic DNA sequence ( Fu et al, 2022 ; Singh et al, 2022 ; Spijker et al, 2022 ; Vosseberg et al, 2022 ), and it is realized that the first introns play a key role in several mechanisms regulating gene expression. We determined that the matching features between the first introns and the corresponding reverse complementary sequences of other introns must provide many useful information.…”