Why so Complex? The Intricacy of Genome Structure and Gene Expression, Associated with Angiosperm Mitochondria, May Relate to the Regulation of Embryo Quiescence or Dormancy—Intrinsic Blocks to Early Plant Life

Mitochondria play key roles in cellular-energy metabolism and are vital for plant-life, such as for successful germination and early-seedling establishment. Most mitochondria contain their own genetic system (mtDNA, mitogenome), with an intrinsic protein-synthesis machinery. Although the challenges of maintaining prokaryotic-type structures and functions are common to Eukarya, land plants possess some of the most complex organelle composition of all known organisms. Angiosperms mtDNAs are characteristically the largest and least gene-dense among the eukaryotes. They often contain highly-variable intergenic regions of endogenous or foreign origins and undergo frequent recombination events, which result in different mtDNA configurations, even between closely-related species. The expression of the mitogenome in angiosperms involves extensive mtRNA processing steps, including numerous editing and splicing events. Why do land-plant’s mitochondria have to be so complex? The answer to this remains a matter of speculation. We propose that this complexity may have arisen throughout the terrestrialization of plants, as a means to control embryonic mitochondrial functions —a critical adaptive trait to optimize seed germination. The unique characteristics of plant mtDNA may play pivotal roles in the nuclear-regulation of organellar biogenesis and metabolism, possibly to control embryos quiescence or dormancy, essential determinants for the establishment of viable plantlets that can survive post-germination.

DNA Repair and the Stability of the Plant Mitochondrial Genome

The mitochondrion stands at the center of cell energy metabolism. It contains its own genome, the mtDNA, that is a relic of its prokaryotic symbiotic ancestor. In plants, the mitochondrial genetic information influences important agronomic traits including fertility, plant vigor, chloroplast function, and cross-compatibility. Plant mtDNA has remarkable characteristics: It is much larger than the mtDNA of other eukaryotes and evolves very rapidly in structure. This is because of recombination activities that generate alternative mtDNA configurations, an important reservoir of genetic diversity that promotes rapid mtDNA evolution. On the other hand, the high incidence of ectopic recombination leads to mtDNA instability and the expression of gene chimeras, with potential deleterious effects. In contrast to the structural plasticity of the genome, in most plant species the mtDNA coding sequences evolve very slowly, even if the organization of the genome is highly variable. Repair mechanisms are probably responsible for such low mutation rates, in particular repair by homologous recombination. Herein we review some of the characteristics of plant organellar genomes and of the repair pathways found in plant mitochondria. We further discuss how homologous recombination is involved in the evolution of the plant mtDNA.

Involvement of plastid, mitochondrial and nuclear genomes in plant-to-plant horizontal gene transfer

This review focuses on plant-to-plant horizontal gene transfer (HGT) involving the three DNA-containing cellular compartments. It highlights the great incidence of HGT in the mitochondrial genome (mtDNA) of angiosperms, the increasing number of examples in plant nuclear genomes, and the lack of any convincing evidence for HGT in the well-studied plastid genome of land plants. Most of the foreign mitochondrial genes are non-functional, generally found as pseudogenes in the recipient plant mtDNA that maintains its functional native genes. The few exceptions involve chimeric HGT, in which foreign and native copies recombine leading to a functional and single copy of the gene. Maintenance of foreign genes in plant mitochondria is probably the result of genetic drift, but a possible evolutionary advantage may be conferred through the generation of genetic diversity by gene conversion between native and foreign copies. Conversely, a few cases of nuclear HGT in plants involve functional transfers of novel genes that resulted in adaptive evolution. Direct cell-to-cell contact between plants (e.g. host-parasite relationships or natural grafting) facilitate the exchange of genetic material, in which HGT has been reported for both nuclear and mitochondrial genomes, and in the form of genomic DNA, instead of RNA. A thorough review of the literature indicates that HGT in mitochondrial and nuclear genomes of angiosperms is much more frequent than previously expected and that the evolutionary impact and mechanisms underlying plant-to-plant HGT remain to be uncovered.

Changes in accumulation of heteroplasmic mitochondrial DNA and frequency of recombination via short repeats during plant lifetime in Phaseolus vulgaris.

Recombination via short repeats in plant mitochondrial genomes results in sublimons--DNA molecules with a copy number much lower compared to the main mitochondrial genome. Coexistence of stoichiometrically different mitotypes, called heteroplasmy, plays an important evolutionary role, since sublimons occasionally replace the main genome resulting in a new plant phenotype. It is not clear, how frequency of recombination and sublimon production is regulated and how it is related to changes in the quantity of the main genome and sublimons. We analyzed the accumulation of two recombining main genome sequences and two resulting sublimons in apical meristems, undifferentiated tissues and leaves of different age of Phaseolus vulgaris. Copy numbers of the main genome sequences varied greatly depending on tissue type and organ age while accumulation of sublimons remained much more stable. Although the overall accumulation of plant mtDNA decreased with the leaf age, the quantity of sublimons increased relative to the main genome indicating a higher frequency of recombination via the short 314 bp repeat. Recombination was symmetrical in young developing leaves while in senescent tissues it shifted towards asymmetric events resulting in overrepresentation of one product. We propose that during plant lifetime replication and recombination frequencies change oppositely sustaining heteroplasmic compositions of the genome, which are favorable for inheritance and maintenance of complex plant mtDNA.

The dynamic nature of plant mitochondrial genome organization.

The characteristic features of higher plant mitochondrial genomes: size, structure, recombination activity and evolutionary dynamics, are reviewed with the emphasis on the mitochondrial DNA (mtDNA) of Phaseolus vulgaris. Among all examined eukaryotic organisms, higher plants were found to contain the largest and most complex mitochondrial genomes. The plant mtDNA structure in vivo and mechanisms of evolution are controversial. We present the currently accepted models and how these models correspond to mitochondrial genomes of several common bean lines.