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Genome-wide features of introns are evolutionary decoupled among themselves and from genome size throughout Eukarya

Irma Lozada-Chávez, Peter F. Stadler, Sonja J. Prohaska
doi: https://doi.org/10.1101/283549
Irma Lozada-Chávez
1Department of Computer Science, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
2Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
3Max Planck Institute for Mathematics in the Sciences, Inselstraße 22, D-04103 Leipzig, Germany
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  • For correspondence: ilozada@bioinf.uni-leipzig.de
Peter F. Stadler
1Department of Computer Science, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
2Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
3Max Planck Institute for Mathematics in the Sciences, Inselstraße 22, D-04103 Leipzig, Germany
4Fraunhofer Institut for Cell Therapy and Immunology, Perlickstraße 1, D-04103 Leipzig, Germany
5Department of Theoretical Chemistry, University of Vienna, Währingerstraße 17, A-1090 Wien, Austria
6Santa Fe Institute, 1399 Hyde Park Rd., 87501 Santa Fe NM, USA
7Center for non-coding RNA in Technology and Health
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Sonja J. Prohaska
1Department of Computer Science, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
2Interdisciplinary Center for Bioinformatics, University of Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
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Abstract

The impact of spliceosomal introns on genome and organismal evolution remains puzzling. Here, we investigated the correlative associations among genome-wide features of introns from protein-coding genes (e.g., size, density, genome-content, repeats), genome size and multicellular complexity on 461 eukaryotes. Thus, we formally distinguished simple from complex multicellular organisms (CMOs), and developed the program GenomeContent to systematically estimate genomic traits. We performed robust phylogenetic controlled analyses, by taking into account significant uncertainties in the tree of eukaryotes and variation in genome size estimates. We found that changes in the variation of some intron features (such as size and repeat composition) are only weakly, while other features measuring intron abundance (within and across genes) are not, scaling with changes in genome size at the broadest phylogenetic scale. Accordingly, the strength of these associations fluctuates at the lineage-specific level, and changes in the length and abundance of introns within a genome are found to be largely evolving independently throughout Eukarya. Thereby, our findings are in disagreement with previous estimations claiming a concerted evolution between genome size and introns across eukaryotes. We also observe that intron features vary homogeneously (with low repetitive composition) within fungi, plants and stramenophiles; but they vary dramatically (with higher repetitive composition) within holozoans, chlorophytes, alveolates and amoebozoans. We also found that CMOs and their closest ancestral relatives are characterized by high intron-richness, regardless their genome size. These patterns contrast the narrow distribution of exon features found across eukaryotes. Collectively, our findings unveil spliceosomal introns as a dynamically evolving non-coding DNA class and strongly argue against both, a particular intron feature as key determinant of eukaryotic gene architecture, as well as a major mechanism (adaptive or non-adaptive) behind the evolutionary dynamics of introns over a large phylogenetic scale. We hypothesize that intron-richness is a pre-condition to evolve complex multicellularity.

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Posted March 18, 2018.
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Genome-wide features of introns are evolutionary decoupled among themselves and from genome size throughout Eukarya
Irma Lozada-Chávez, Peter F. Stadler, Sonja J. Prohaska
bioRxiv 283549; doi: https://doi.org/10.1101/283549
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Genome-wide features of introns are evolutionary decoupled among themselves and from genome size throughout Eukarya
Irma Lozada-Chávez, Peter F. Stadler, Sonja J. Prohaska
bioRxiv 283549; doi: https://doi.org/10.1101/283549

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