On the evolutionary origin of the plant mitochondrion and its genome

Abstract

Higher plants occupy very different positions in the mitochondrial and nuclear lineages of global phylogenetic trees based on conserved regions of small subunit (SSU) and large subunit (LSU) rRNA sequences. In the nuclear subtree, plants branch off late, at a position reflecting a massive radiation of the major multicellular (and some unicellular) groups; in the mitochondrial subtree, in contrast, plants branch off early, near the point of connection between the mitochondrial and eubacterial lineages. Moreover, in the nuclear lineage, plants branch together with the unicellular green alga Chlamydomonas reinhardtii, whereas in the mitochondrial lineage (in both SSU and LSU trees), metaphytes and chlorophyte branch separately. Statistical evaluation indicates that the anomalous branching position of higher plants in the mitochondrial lineage is not a treeing artifact attributable to the relatively rapid rate of sequence divergence of non-plant mitochondrial rRNA sequences. In considering alternative biological explanations for these results, we are led to propose that the rRNA genes in plant mitochondria may be of more recent evolutionary origin than the rRNA genes in other mitochondria. This proposal has implications for monophyletic vs. polyphyletic scenarios of mitochondrial origin and is consistent with other evidence indicating that plant mtDNA is an evolutionary mosaic.