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Selective forces for the origin of spliceosomes

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Abstract

It has been proposed that eukaryotic spliceosomes evolved from bacterial group II introns via constructive neutral changes. However, a more likely interpretation is that spliceosomes and group II introns share a common undefined RNA ancestor—a proto-spliceosome. Although, the constructive neutral evolution may have probably played some roles in the development of complexity including the evolution of modern spliceosomes, in fact, the origin, losses and the retention of spliceosomes can be explained straight-forwardly mainly by positive and negative selection: (1) proto-spliceosomes evolved in the RNA world as a mechanism to excise functional RNAs from an RNA genome and to join non-coding information (ancestral to exons) possibly designed to be degraded. (2) The complexity of proto-spliceosomes increased with the invention of protein synthesis in the RNP world and they were adopted for (a) the addition of translation signal to RNAs via trans-splicing, and for (b) the exon-shuffling such as to join together exons coding separate protein domains, to translate them as a single unit and thus to facilitate the molecular interaction of protein domains needed to be assembled to functional catalytic complexes. (3) Finally, the spliceosomes were adopted for cis-splicing of (mainly) non-coding information (contemporary introns) to yield translatable mRNAs. (4) Spliceosome-negative organisms (i.e., prokaryotes) have been selected in the DNA–protein world to save a lot of energy. (5) Spliceosome-positive organisms (i.e., eukaryotes) have been selected, because they have been completely spliceosome-dependent.

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Abbreviations

CNE:

Constructive neutral evolution

LECA:

Last eukaryotic common ancestor

LUCA:

Last universal common ancestor

RNP:

Ribonucleoprotein

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Acknowledgments

This work was supported by a grant VEGA 1/0416/09 from the Ministry of Education of the Slovak Republic to J. K., and is the result of the project implementation: “the improvement of centre of excellence for exploitation of informational biomacromolecules in disease prevention and improvement of quality of life,” ITMS 26240120027, supported by the Research and Development Operational Programme funded by the ERDF.

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Authors and Affiliations

  1. Department of Genetics, Faculty of Natural Sciences, Comenius University, Mlynská dolina B-1, 842 15, Bratislava, Slovakia

    Matej Vesteg, Zuzana Šándorová & Juraj Krajčovič

  2. Institute of Cell Biology and Biotechnology, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia

    Matej Vesteg & Juraj Krajčovič

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  1. Matej Vesteg
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  2. Zuzana Šándorová
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  3. Juraj Krajčovič
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Correspondence to Matej Vesteg.

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Vesteg, M., Šándorová, Z. & Krajčovič, J. Selective forces for the origin of spliceosomes. J Mol Evol 74, 226–231 (2012). https://doi.org/10.1007/s00239-012-9494-3

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  • DOI: https://doi.org/10.1007/s00239-012-9494-3

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