Tracing Plant Mitochondrial DNA Evolution: Rearrangements of the Ancient Mitochondrial Gene Cluster trnA-trnT-nad7 in Liverwort Phylogeny

Abstract

Whereas frequent recombination characterizes flowering plant mitochondrial genomes, some mitochondrial gene arrangements may, in contrast, be conserved between streptophyte algae and early land plant clades (bryophytes). Here we explore the evolutionary fate of the mitochondrial gene arrangement trnA-trnT-nad7, which is conserved among the alga Chara, the moss Physcomitrella, and the liverwort Marchantia, although trnT is inverted in orientation in the latter. Surprisingly, we now find that the Chara-type gene arrangement is generally conserved in mosses, but that trnT is lacking between trnA and nad7 in all simple-thalloid and leafy (jungermanniid) liverworts. The ancient gene continuity trnA-trnT-nad7 is, however, conserved in Blasia, representing the sister lineage to all other complex-thalloid (marchantiid) liverworts. The recombinogenic insertion of short sequence stretches, including nad5 and rps7 pseudogene fragments copied from elsewhere in the liverwort mtDNA, likely mediated a subsequent inversion of trnT and flanking sequences in a basal grade of marchantiid liverworts, which was then followed by an independent secondary loss of trnT in derived marchantiid taxa later in evolution. In contrast to the previously observed extreme degree of coding sequence conservation and the assumed absence of active recombination in Marchantia mtDNA, this now reveals a surprisingly dynamic evolution of marchantiid liverwort mitochondrial genomes.

The Mitochondrial Genome of the Lycophyte Huperzia squarrosa: The Most Archaic Form in Vascular Plants

“…Three recent studies reported pseudogene pieces in intergenic spacers [18], [38], [39]. One of them performed a systematic survey of pseudogene pieces in all seven sequenced bryophyte mitochondrial genomes and found that the three liverworts had a few dozens of such fragments in the spacers, whereas the two hornworts had only a few pieces and the two mosses had none [18].…”

Organellar genomes of the four-toothed moss, Tetraphis pellucida

“…However, while this appears to have been a very early and defining event in the evolution of both hornworts and liverworts, it is a derived condition in mosses and conceivably even unique to Tetraphis (as it may be unique to Huperzia within the tracheophytes). Wahrmund et al [45] showed that the entire trnA-trnT-nad7 gene cluster has been subject to extensive recombination during the evolutionary history of liverworts. However, it is striking that a BLASTn search for the region of 122 bp adjacent to the rpl2 gene in T. pellucida matches only the same region in H. squarrosa , suggesting the possibility of a shared mechanism for the independent loss of nad7 in Tetraphis and Huperzia .…”

20,000 species and five key markers: The status of molecular bryophyte phylogenetics

“…Later phylogenetic studies addressing relationships within the bryophyte grade favoured the more variable non-coding regions, such as introns (see above) and lately spacers, both in the nad cluster (see above) and the trnA-trnT-nad7 region (e.g. Groth-Malonek et al 2007;Wahrmund et al 2008Wahrmund et al , 2009Wahrmund et al , 2010; see also Knoop 2010). Recently, two additional mitochondrial group I introns, cox1i624 and cobi420, were established as promising markers in bryophyte phylogenetics (Wahrmund et al 2010;Volkmar & Knoop 2010).…”