Mitochondrial Genome Evolution in the Plant Lineage

Abstract

Land plants feature particularly complicated mitochondrial genomes. Plant mitochondrial DNAs may be more than 100 times larger than those of animals and are structurally much more complex due to frequent ongoing recombination. The significant increase of plant mitochondrial genome sizes results from a combination of several factors: more genes are encoded, many of these carry introns and, most importantly, the plant mitochondrial genome has a propensity to accept foreign DNA sequences from the chloroplast, the nucleus, or even from other mitochondrial genomes via horizontal gene transfer. Similarly, plant mitochondria are also more complex on the transcriptome level where processes such as frequent RNA editing or trans-splicing of disrupted introns contribute to RNA maturation. The evolution of these peculiar features is discussed in the framework of our modern understanding of plant phylogeny to which mitochondrial genome data have contributed significantly.

Glossary

Chondrome:

Understood as the mitochondrial genome (similar to the term “plastome” for the chloroplast genome). Sometimes mixed up with the term chondriome, now more widely used to circumscribe all mitochondria in a cell (see Chap. 2).

Clade:

See monophyletic.

Cytoplasmic male sterility (CMS):

The economically most important phenotypic trait connected to plant mitochondrial DNA mutations. The corresponding mitochondrial dysfunctions are revealed as male infertility resulting from nonfunctional pollen grains.

Endosymbiotic gene transfer (EGT):

The functional relocation of genes from the organelle endosymbiont genomes into the host cell nucleus as a corollary of the endosymbiont hypothesis. Functional gene transfer may proceed through mature RNA and reverse transcription. Clearly though, such functional gene transfer is accompanied by DNA-based copying mechanisms which lead to insertion of small and large DNA fragments of mitochondrial (numt) and plastid (nupt) origin in the nuclear genome.

Group I and group II introns:

Introns that are commonly observed in organelle genomes of plants and fungi, characterized by highly characteristic RNA secondary structures. For details see Box 1.1.

Heteroplasmy:

The existence of different organelle genomes within a single individual, a single cell or even a single organelle (given that organelle DNAs are generally present in multiple copies).

Horizontal gene transfer (HGT):

The process of DNA sequence migration across species borders. For details see Box 1.3.

Lateral gene transfer (LGT):

A term that is frequently used synonymously to >Horizontal gene transfer.

Monophyletic:

Literally, of “one stem,” a group of organisms (a clade) encompassing all descendants which trace back to a single (usually extinct) ancestor. Indentifying monophyletic clades through shared derived characters (>synapomorphies) is the goal of cladistics as introduced by Willi Hennig (1950) into modern phylogenetics.

Promiscuous DNA:

Mostly nonfunctional DNA fragments copied from one genome to another in the eukaryotic cell. Plant mitochondria are particularly prone to accumulation of DNA sequences from the chloroplast or the nuclear genome. Foreign DNA derived from the chloroplast or the nuclear genome is frequently inserted in to the mtDNA of vascular plants.

RNA editing:

Modification of nucleotide sequences on transcript level, in plant organelles in the form of cytidine-uridine exchanges. For details see Box 1.2.

Synapomorphy:

Any shared, derived (i.e., newly acquired) state of a morphologic, biochemical, developmental, or any other character in a group of organisms helping to identify them as a >monophyletic clade. Examples are the water-conducting tissues and the dominating diploid sporophyte generation for the vascular plant (tracheophyte) clade.

Trans-splicing:

The maturation of a RNA molecule through splicing of separate, independent precursor-transcripts encoded by separate, distant genomic loci. In plant organelles, gene arrangements requiring trans-splicing have arisen through recombinational activity disrupting ancestral group II or group I intron continuities.