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MBE Advance Access originally published online on September 8, 2004
Molecular Biology and Evolution 2005 22(1):117-125; doi:10.1093/molbev/msh259
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Molecular Biology and Evolution vol. 22 no. 1 © Society for Molecular Biology and Evolution 2005; all rights reserved.

Research Article

Ancestors of Trans-Splicing Mitochondrial Introns Support Serial Sister Group Relationships of Hornworts and Mosses with Vascular Plants

Milena Groth-Malonek*, Dagmar Pruchner{dagger}, Felix Grewe* and Volker Knoop*

* Institut für Zelluläre und Molekulare Botanik, Abt. Molekulare Evolution, Universität Bonn, Bonn, Germany; {dagger} Abt. Molekulare Botanik, Universität Ulm, Ulm, Germany

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

Some group II introns in the organelle genomes of plants and algae are disrupted and require trans-splicing of the affected exons from independent transcripts. A peculiar mitochondrial nad5 gene structure is universally conserved in flowering plants where two trans-splicing introns frame a tiny exon of only 22 nucleotides, and two additional conventional group II introns interrupt the nad5 reading frame at other sites. These four introns are absent in the liverwort Marchantia polymorpha, which carries a group I intron at an unrelated site in nad5. To determine how intron gains and losses have sculptured mitochondrial gene structures in early land-plant evolution, we have investigated the full nad5 gene structures in the three bryophyte classes and the fern Asplenium nidus. We find the single Marchantia group I intron nad5i753 present as the only intervening sequence in both closely (Corsinia and Monoclea) and distantly related (Noteroclada, Bazzania, and Haplomitrium) liverwort genera. In a taxonomically wide spectrum of mosses (Sphagnum, Encalypta, Timmia, Ulota, and Rhacocarpus); however, we additionally identify the angiosperm-type group II introns nad5i230 and nad5i1455. The latter is a cis-arranged homolog to one of the two angiosperm trans-splicing introns, notably the first of its kind in mosses. In the hornwort Anthoceros, the "moss and liverwort–type" group I intron nad5i753 is absent, and, besides nad5i230 and nad5i1455, intron nad5i1477 is present as the second ancestral group II intron which has evolved into a trans-splicing arrangement in angiosperms. The influence of highly frequent RNA editing, most notably in the genera Haplomitrium, Anthoceros, and Asplenium, on phylogenetic tree construction is investigated and discussed. Taken together, the data (1) support a sister group relationship of liverworts as a whole to all other embryophytes, (2) indicate loss of a group I and serial entries of group II introns in the nad5 gene during early evolution of the nonliverwort lineage, and (3) propose a placement of hornworts as sister group to tracheophytes.

Key Words: Bryophytes • evolution • phylogeny • group I and group II introns • RNA editing


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