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An Overview of the Introns-First Theory
Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics.
2009 (English)In: Journal of Molecular Evolution, ISSN 0022-2844, E-ISSN 1432-1432, Vol. 69, 527-540 p.Article in journal (Refereed) Published
Abstract [en]

We review the introns-first hypothesis a decade after it was first proposed. It is that exons emerged from

non-coding regions interspersed between RNA genes in an early RNA world, and is a subcomponent of a more general ‘RNA-continuity’ hypothesis. The latter is that some RNA based systems, especially in RNA processing, are ‘relics’ that can be traced back either to the RNA world that preceded both DNA and encoded protein synthesis or to the later ribonucleoprotein (RNP) world (before DNA took over the main coding role). RNA-continuity is based on independent evidence—in particular, the relative inefficiency of RNA catalysis compared with protein catalysis— and leads to a wide range of predictions, ranging from the origin of the ribosome, the spliceosome, small nucleolar RNAs, RNases P and MRP, and mRNA, and it is consistent with the wide involvement of RNA-processing and regulation of RNA in modern eukaryotes. While there may still

be cause to withhold judgement on intron origins, there is strong evidence against introns being uncommon in the last eukaryotic common ancestor (LECA), and expanding only within extant eukaryotic groups—the ‘very-late’ intron invasion model. Similarly, it is clear that there are selective forces on numbers and positions of introns; their existence may not always be neutral. There is still a range of viable alternatives, including introns first, early, and ‘latish’ (i.e. well established in LECA), and regardless of which is ultimately correct, it pays to separate out various questions and to focus on testing the predictions of sub-theories.

Place, publisher, year, edition, pages
2009. Vol. 69, 527-540 p.
Keyword [en]
Introns, RNA world, Eukaryote origins, RNP world, Spliceosome, Introns early
National Category
Biochemistry and Molecular Biology
URN: urn:nbn:se:su:diva-35378DOI: 10.1007/s00239-009-9279-5ISI: 000272574100012OAI: diva2:287199
Available from: 2010-01-18 Created: 2010-01-18 Last updated: 2011-05-02Bibliographically approved
In thesis
1. The deep evolutionary roots of non-coding RNA - a comparative genomics approach
Open this publication in new window or tab >>The deep evolutionary roots of non-coding RNA - a comparative genomics approach
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Non-coding RNAs (ncRNA) are a diverse group of genes that do not encode proteins but function exclusively on the level of RNA and were originally suggested to be remnants of a pre-DNA stage of life known as the RNA world. More recent work, however, has uncovered a rich repertoire of previously unknown families with possible consequences for our understanding of the origin and evolution of the modern RNA infrastructure. The main goal of this thesis was therefore to re-examine the evolutionary history of RNAs and theories regarding the transition from an RNA world in light of recent advances in molecular and computational biology.

Using comparative genomics approaches and sequence data from all domains of life, my work shows that the majority of known RNAs exhibit a highly domain-specific distribution, compatible with an ongoing emergence rather than deep ancestry. Focusing on small nucleolar RNAs (snoRNA), I find that the eukaryote ancestor possessed a complex snoRNA infrastructure, but that intronic snoRNAs are mobile over larger evolutionary time scales. The latter has consequences for predictions made by the Introns-first hypothesis, a framework to explain the emergence of introns in an RNA world and which we revisited in light of advances in our understanding of the evolutionary dynamics of introns.

A more in-depth analysis of ncRNA mobility across vertebrates found intronic copies of both snoRNAs and miRNAs to be more stable than intergenic ones, suggesting that this arrangement may be a consequence of co-expression. Also, snoRNAs are frequently located in highly expressed genes, in line with their role in ribosome biogenesis. Finally, a closer examination of the genomic distribution of two essential ncRNAs, snoRNA U3 and the spliceosomal RNA U1 shows that both are present in numerous copies across vertebrate genomes. Using next-generation sequencing data, I tested whether this is the result of genetic drift or a requirement for having many copies.

Place, publisher, year, edition, pages
Stockholm: Department of Molecular Biology and Functional Genomics, Stockholm University, 2011. 182 p.
non-coding RNA, evolution, comparative genomics, RNA world, introns, snoRNA, miRNA
National Category
Cell and Molecular Biology
Research subject
Molecular Biology
urn:nbn:se:su:diva-56820 (URN)978-91-7447-306-3 (ISBN)
Public defence
2011-06-07, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 14:00 (English)
At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 3: Manuscript. Paper 5: Manuscript.Available from: 2011-05-12 Created: 2011-04-28 Last updated: 2011-05-02Bibliographically approved

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Hoeppner, Marc P.Poole, Anthony M.
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