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Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa?

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Abstract

Phylum Euglenozoa comprises three groups of eukaryotic microbes (kinetoplastids, diplonemids, and euglenids), the mitochondrial (mt) genomes of which exhibit radically different modes of organization and expression. Gene fragmentation is a striking feature of both euglenid and diplonemid mtDNAs. To rationalize the emergence of these highly divergent mtDNA types and the existence of insertion/deletion RNA editing (in kinetoplastids) and trans-splicing (in diplonemids), we propose that in the mitochondrion of the common evolutionary ancestor of Euglenozoa, small expressed gene fragments promoted a rampant neutral evolutionary pathway. Interactions between small antisense transcripts of these gene fragments and full-length transcripts, assisted by RNA-processing enzymes, permitted the emergence of RNA editing and/or trans-splicing activities, allowing the system to tolerate indel mutations and further gene fragmentation, respectively, and leading to accumulation of additional mutations. In this way, dramatically different mitochondrial genome structures and RNA-processing machineries were able to evolve. The paradigm of constructive neutral evolution acting on the widely different mitochondrial genetic systems in Euglenozoa posits the accretion of initially neutral molecular interactions by genetic drift, leading inevitably to the observed ‘irremediable complexity’.

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Authors and Affiliations

  1. Biology Centre, Institute of Parasitology, Czech Academy of Sciences, and Faculty of Sciences, University of South Bohemia, 37005, České Budĕjovice, Czech Republic

    Pavel Flegontov & Julius Lukeš

  2. Centre for Comparative Genomics and Evolutionary Bioinformatics, and Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, B3H 4R2, Canada

    Michael W. Gray

  3. Robert-Cedergren Center in Bioinformatics and Genomics, and Department of Biochemistry, Université de Montréal, Montreal, QC, H3C 3J7, Canada

    Gertraud Burger

Authors
  1. Pavel Flegontov
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  2. Michael W. Gray
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  3. Gertraud Burger
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  4. Julius Lukeš
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Correspondence to Julius Lukeš.

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Communicated by H. Jacobs.

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Flegontov, P., Gray, M.W., Burger, G. et al. Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa?. Curr Genet 57, 225–232 (2011). https://doi.org/10.1007/s00294-011-0340-8

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  • DOI: https://doi.org/10.1007/s00294-011-0340-8

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