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MBE Advance Access originally published online on February 5, 2007
Molecular Biology and Evolution 2007 24(4):1068-1074; doi:10.1093/molbev/msm026
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Evolution of a Pseudogene: Exclusive Survival of a Functional Mitochondrial nad7 Gene Supports Haplomitrium as the Earliest Liverwort Lineage and Proposes a Secondary Loss of RNA Editing in Marchantiidae

Milena Groth-Malonek, Ute Wahrmund, Monika Polsakiewicz and Volker Knoop

Institut für Zelluläre und Molekulare Botanik, Abteilung Molekulare Evolution, Kirschallee 1, D-53115 Bonn, Germany

E-mail: volker.knoop{at}uni-bonn.de.

Accepted for publication January 31, 2007.

Gene transfer from the mitochondrion into the nucleus is a corollary of the endosymbiont hypothesis. The frequent and independent transfer of genes for mitochondrial ribosomal proteins is well documented with many examples in angiosperms, whereas transfer of genes for components of the respiratory chain is a rarity. A notable exception is the nad7 gene, encoding subunit 7 of complex I, in the liverwort Marchantia polymorpha, which resides as a full-length, intron-carrying and transcribed, but nonspliced pseudogene in the chondriome, whereas its functional counterpart is nuclear encoded. To elucidate the patterns of pseudogene degeneration, we have investigated the mitochondrial nad7 locus in 12 other liverworts of broad phylogenetic distribution. We find that the mitochondrial nad7 gene is nonfunctional in 11 of them. However, the modes of pseudogene degeneration vary: whereas point mutations, accompanied by single-nucleotide indels, predominantly introduce stop codons into the reading frame in marchantiid liverworts, larger indels introduce frameshifts in the simple thalloid and leafy jungermanniid taxa. Most notably, however, the mitochondrial nad7 reading frame appears to be intact in the isolated liverwort genus Haplomitrium. Its functional expression is shown by cDNA analysis identifying typical RNA-editing events to reconstitute conserved codon identities and also confirming functional splicing of the 2 liverwort-specific group II introns. We interpret our results 1) to indicate the presence of a functional mitochondrial nad7 gene in the earliest land plants and strongly supporting a basal placement of Haplomitrium among the liverworts, 2) to indicate different modes of pseudogene degeneration and chondriome evolution in the later branching liverwort clades, 3) to suggest a surprisingly long maintenance of a nonfunctional gene in the presumed oldest group of land plants, and 4) to support the model of a secondary loss of RNA-editing activity in marchantiid liverworts.

Key Words: livercorts • mitochondrial DNA • pseudogene evolution • RNA editing • phylogeny


Charles Delwiche, Associate Editor


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M. Rudinger, M. Polsakiewicz, and V. Knoop
Organellar RNA Editing and Plant-Specific Extensions of Pentatricopeptide Repeat Proteins in Jungermanniid but not in Marchantiid Liverworts
Mol. Biol. Evol., July 1, 2008; 25(7): 1405 - 1414.
[Abstract] [Full Text] [PDF]



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