Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes--though this be madness, yet there's method in't

Abstract

Mitochondrial heteroplasmy is defined as the coexistence of divergent mitochondrial genotypes in a cell. The ratio of the alternative genomes may be variable, but in plants, the usually prevalent main genome is accompanied by sublimons--substoichiometric mitochondrial DNA (mtDNA) molecules. Plant mitochondrial heteroplasmy was originally viewed as being associated with pathological mutations or was found in non-natural plant populations. Currently, it is considered to be a common situation in plants. Recent years have changed the previous view on the role of homologous recombination, small-scale mutations, and paternal leakage of mtDNA in the generation of heteroplasmy. Newly developed sensitive techniques have allowed the precise estimation of mtDNA stoichiometry. Mechanisms of maintenance and transmission of heteroplasmic genomes, including DNA recombination and replication, as well as mitochondrial fusion and fission, have been studied. This review describes the high level of plant mitochondrial genome complication--the 'madness' resulting from the heteroplasmic state and explains the method hidden in this madness. Heteroplasmy is described as the evolutionary strategy of uniparentally inherited plant mitochondrial genomes which do not undergo sexual recombination. In order to compensate for this deficiency, alternative types of mtDNA are substoichiometrically accumulated as a reservoir of genetic variability and may undergo accelerated evolution. Occasionally, sublimons are selected and amplified in the process called substoichiometric shifting, to take over the role of the main genome. Alternative mitochondrial genomes may recombine, yielding new mtDNA variants, or segregate during plant growth resulting in plants with mosaic phenotypes. Two opposite roles of mitochondrial heteroplasmy with respect to acceleration or counteracting of mutation accumulation are also discussed. Finally, nuclear control of heteroplasmy and substoichiometric shifting is described.

Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes

“…The AC frequency for short repeats in Viscum mtDNA is markedly higher than in the nine other angiosperm mtDNAs for which AC frequency has been measured by high-depth genome sequencing and also is higher than in angiosperms in which nongenome-scale approaches have been used (59). Not even a single AC was detected for the vast number (>300,000 and >70,000) of short-repeat pairs (30-100 bp in length) present in the mitogenomes of S. conica (11.3 Mb) and cucumber (1.7 Mb), respectively (9, 60).…”

“…In angiosperm mitochondria, low-abundance substoichiometric DNA molecules (termed "sublimons") are often present, arising via recombination between short repeats (57)(58)(59). Most pairs of repeats in Viscum mtDNA are short; of those ≥30 bp in size, 97% (305 of 315) are ≤100 bp in length, and 86% of these are <50 bp in length.…”

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

“…Unlike the small (15-18 kb) and homogenous mitochondrial genomes of animals, plant mitochondrial genomes are large (hundreds of kb or more) and complicated, with dramatic variations in structure, size, and organization [2]. Studies have shown that in the angiosperm mitochondrial genomes, frequent DNA recombination may result in genomic rearrangements, yielding multiple types of recombinant structures that may vary dramatically in copy number (substoichiometric shifting (SSS)); the recombinant structures may contain new open reading frames (ORFs) and some of them can cause cytoplasmic male sterility (CMS) [3][4][5]. CMS is a widespread phenomenon observed in more than 150 flowering plant species [6] and often associated with unusual ORFs present in the mitochondrial genomes [5].…”

Transformation of the mitochondrial genome

“…When these repeated sequences are in direct orientation, they allow the genome to be subdivided into a collection of molecules, each containing only a portion of the genetic information. These molecules of plant mitochondrial DNA can vary in copy number over time, a process called substoichiometric shifting (Small et al, 1987;Janska et al, 1998;Abdelnoor et al, 2003) that leads to heteroplasmic complexity (Woloszynska, 2010). Silencing of genes that control such shifting, such as the DNA mismatch repair protein MSH1 that is homologous to mutator protein MutS in Escherichia coli (Abdelnoor et al, 2003), might be a good approach to solve the problem of plant transformation.…”