Exploring Non-Coding Mitochondrial DNA Sequences in Bryophyte Molecular Evolution

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Exploring Non-Coding Mitochondrial DNA Sequences in Bryophyte Molecular Evolution Exploring non-coding mitochondrial DNA sequences in bryophyte molecular evolution Dissertation zur Erlangung des Doktorgrades (Dr. rer. nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn vorgelegt von Ute Volkmar aus Halle/Saale Bonn 2010 Angefertigt mit Genehmigung der Mathematisch-Naturwissenschaftlichen Fakultät der Rheinischen Friedrich-Wilhelms-Universität Bonn 1. Gutachter: Prof. Dr. Volker Knoop 2. Gutachter: Prof. Dr. Jan-Peter Frahm Tag der Promotion: 16. April 2010 Erscheinungsjahr: 2010 Contents 1 Summary 1 2 Introduction 2 2.1 Peculiarities of plant mitochondrial genomes . .2 2.2 Mitochondrial genomes in liverworts and mosses . .6 2.3 Genes, introns and spacer regions: different loci for phylogenetic analyses . .7 2.4 Current understanding of moss phylogeny and remaining questions . .8 2.5 Molecular evolution in liverwort chondriomes . 12 3 Results 15 3.1 Novel mitochondrial markers for moss phylogeny . 15 3.1.1 Ute Wahrmund, Theresia Rein, Kai F. Müller, Milena Groth-Malonek and Volker Knoop (2009): Fifty mosses on five trees: comparing phylogenetic information in three types of non-coding mitochondrial DNA and two chloroplast loci. Plant Systematics and Evolution 282 (3): 241-255 . 15 3.1.2 Ute Wahrmund, Dietmar Quandt and Volker Knoop (2010): The phylogeny of mosses – addressing open issues with a new mitochondrial locus: group I intron cobi420. Molecular Phylogenetics and Evolution 54 (2): 417-426 . 31 3.1.3 Ute Wahrmund and Volker Knoop: The lacking roots of mosses: discrepan- cies in chloroplast and mitochondrial data, including the novel intron locus cox1i624. Journal of Molecular Evolution, submitted . 42 3.2 Mitochondrial molecular evolution in liverworts . 68 3.2.1 Ute Wahrmund, Milena Groth-Malonek and Volker Knoop (2008): Tracing plant mitochondrial DNA evolution: Rearrangements of the ancient mitochon- drial gene cluster trnA-trnT-nad7 in liverwort phylogeny. Journal of Molecular Evolution 66: 621-629 . 68 I 3.2.2 Milena Groth-Malonek, Ute Wahrmund, Monika Polsakiewicz and Volker Knoop: Evolution of a pseudogene: Exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and pro- poses a secondary loss of RNA editing in Marchantiidae. Molecular Biology and Evolution 24 (4): 1068-1074 . 80 4 Discussion 93 4.1 The impact of novel mitochondrial markers on moss phylogeny . 93 4.2 New insights into mitochondrial evolution of liverworts: promiscuous spacer regions and long retained pseudogenes . 99 5 Acknowledgements 106 Bibliography 107 II 1 Summary The thesis presented here focussed on the molecular evolution of non-coding mitochondrial DNA in liverworts and mosses. To address remaining questions in moss phylogeny, three mitochondrial gene regions were investi- gated and established as novel molecular markers: the nad5-nad4 intergenic spacer region (Wahrmund et al. 2009) and the two group I introns in the cob gene and cox1 gene (cobi420, Wahrmund et al. 2010 and cox1i624, Volkmar and Knoop subm). Phylogenetic trees based on the single loci and concatenated data sets identified a placement of Catoscopium, Drummondia and Timmiella in the basal Dicranidae, proposed the exclusion of Gigaspermaceae from the Funariidae and a potential sister relationship of the nematodontous moss classes Tetraphidopsida and Polytrichopsida (Wahrmund et al. 2009, 2010). A different resolution of the basal-most moss taxa by chloroplast and mitochondrial markers was ob- served (Volkmar and Knoop subm) and its implications on molecular and morphological evolution in mosses discussed. The hitherto assumed slow evolution of the mitochondrial genome in liverworts was contrasted with the discovery of recombinational activity in the intergenic region of the trnA-trnT-nad7 cluster, an ancient gene arrangement that is also present in algae and mosses. During liverwort evolution, an inversion and at least three independent losses of the trnT and adjacent spacer regions resulted in independent size decreases (Wahrmund et al. 2008). The nad7 gene, part of this gene cluster, is a pseudogene in all jungermanniid and marchantiid liverworts investigated. An ancient gene transfer to the nuclear genome occurred probably in the common ancestor of both classes, more than 350 million years ago (Groth-Malonek et al. 2007b). The exceptionally long retention of the pseudogene indicates an underlying but yet unknown function. In the three haplomitriid liverwort genera Haplomitrium, Apotreubia and Treubia, however, the mitochondrial nad7 gene is intact and functional and experiences an extremely varying degree of C-to-U RNA editing, a modification of mRNAs in plant organelles to reconstitute conserved codon identities. 1 2 Introduction 2.1 Peculiarities of plant mitochondrial genomes Despite being derived from the same α-proteobacterial-like ancestor, there are many differences be- tween animal and plant mitochondrial genomes – manifested in many aspects such as (i) complexities of the DNA molecules, (ii) sizes, (iii) numbers and orders of genes encoded, (iv) intron presences and their conservation, (v) affinity for interorganellar gene transfer and uptake of foreign DNA and (vi) the ability for and extent of RNA editing. Regarding these traits, animal mitochondrial DNA is a small and compact molecule (with appr. 16 kb) and typically contains 37 intronless genes (13 genes for proteins necessary in the respiratory chain, 22 tRNAs and two rRNAs). Rarely, introns have been found in mitochondrial genes of enigmatic taxa representing basal lineages of the metazoa phylogeny e.g. the placozoon Trichoplax adherens (Burger et al. 2009), the bilaterian Nephtys spec. (Valles et al. 2008), some cnidaria like Metridium senile (Beagley et al. 1998) and few porifera like Tetilla spec. (Rot et al. 2006). In animals, the highly conserved gene order with only small spacer regions is in stark contrast to the high substitution rate found in the coding sequences. In plants (Fig. 1.1), in contrast, exactly the opposite is found: In mitochondrial genomes of strik- ingly varying sizes (appr. 58 to more than 4000 kb) flexible gene order and gene content are closely linked with highly conserved coding sequences. There are only few examples of gene arrangements that are conserved across different land plant clades and these are usually found in early land plants (see below). In maize (Zea mays) it was shown that the gene order can vary greatly even between two cytotypes due to homologous recombination and the formation of smaller subcircles (Fauron et al. 1995). Such ‘multipartite’ structures are now generally recognized as a feature of angiosperm mito- chondrial genomes (Sugiyama et al. 2005). Likewise ‘early’ tracheophytes such as the quillwort Isoetes engelmannii feature mtDNA reflecting frequent genomic rearrangements (Grewe et al. 2009). It is how- ever not associated with a large genome size, as Isoetes engelmannii owns the smallest yet sequenced mitochondrial genome (appr. 58 kb). The publication of several completely sequenced mitochondrial (mt) genomes has weakened the generalization that the evolution of land plants (Fig. 1.1) is accompanied by the enlargement of mi- 2 Introduction tochondrial DNA. Best examples are the moss Physcomitrella patens (105 kb, Terasawa et al. 2007) and the lycophyte Isoetes engelmannii (58 kb, Grewe et al. 2009) whose mt genomes are considerably smaller than that of the liverwort Marchantia polymorpha (187 kb, Oda et al. 1992), a member of the earliest land plant group. In addition, the mt genome of the gymnosperm Cycas taitungensis (415 kb, Chaw et al. 2008) is larger than that of the angiosperm Arabidopsis thaliana (Unseld et al. 1997). Even within closely related species and genera, the mt genome size can differ enormously as shown in Cu- cumis melo (muskmelon, appr. 1600 kb) and Cucumis sativus (cucumber, appr. 1000 kb, Ward et al. 1981). The largest plant mt genome known so far does not belong to a member of the quite derived Cucurbitaceae (angiosperms, eurosids I) but rather to the basal-most angiosperm Amborella trichopoda (appr. 4000 kb, J. Palmer, pers. comm.). angiosperms gymnosperms tracheophytes = Gnetopsida vascular plants monilophytes lycophytes embryophytes hornworts = land plants mosses marchantiid liverworts bryophytes jungermanniid liverworts haplomitriid liverworts charophyte algae Figure 2.1: Overview of land plant evolution, rooted with charophyte algae as sister clade to all land plants, after Qiu et al. (2006) An increase in genome size in general is not caused by a higher number of genes or more introns encoded. It is mainly the consequence of larger spacer regions and in part due to the uptake of ‘for- eign’ DNA. Looking at one of only few spacer regions that are conserved between the three bryophyte divisions, the nad5-nad4 spacer (Groth-Malonek et al. 2007a), its size enlarges to more than 3 kb in hornworts before the gene continuity is disrupted in the early tracheophytes. In addition, the size of introns can increase. Mitochondrial introns (like the ones in the chloroplast genome) can be distin- guished by their three-dimensional structure into group I and group II introns. The folding into loop and pairing regions allows close proximity of the two exons and facilitates splicing. The extension of introns usually occurs in loop 5 and 8 of group I introns and in domain IV of group II introns and can even result in breaking of genes into parts due to an interrupted transcription. Then, trans-splicing of
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