Comparisons Among Two Fertile and Three Male-Sterile Mitochondrial Genomes of Maize

Abstract

We have sequenced five distinct mitochondrial genomes in maize: two fertile cytotypes (NA and the previously reported NB) and three cytoplasmic-male-sterile cytotypes (CMS-C, CMS-S, and CMS-T). Their genome sizes range from 535,825 bp in CMS-T to 739,719 bp in CMS-C. Large duplications (0.5-120 kb) account for most of the size increases. Plastid DNA accounts for 2.3-4.6% of each mitochondrial genome. The genomes share a minimum set of 51 genes for 33 conserved proteins, three ribosomal RNAs, and 15 transfer RNAs. Numbers of duplicate genes and plastid-derived tRNAs vary among cytotypes. A high level of sequence conservation exists both within and outside of genes (1.65-7.04 substitutions/10 kb in pairwise comparisons). However, sequence losses and gains are common: integrated plastid and plasmid sequences, as well as noncoding ''native'' mitochondrial sequences, can be lost with no phenotypic consequence. The organization of the different maize mitochondrial genomes varies dramatically; even between the two fertile cytotypes, there are 16 rearrangements. Comparing the finished shotgun sequences of multiple mitochondrial genomes from the same species suggests which genes and open reading frames are potentially functional, including which chimeric ORFs are candidate genes for cytoplasmic male sterility. This method identified the known CMS-associated ORFs in CMS-S and CMS-T, but not in CMS-C.

The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

“…Angiosperm mitochondrial genomes harbor tremendous variation in genome size (22,23,34,35). Previous examples of variation within and between species have often been attributed to large sequence duplications (27) or the insertions of large quantities of foreign DNA (23,36,37). In contrast, a fundamentally different mechanism seems to be at play in S. noctiflora, with the presence or absence of entire chromosomes explaining the size variation between genomes within this species (Fig.…”

“…This variation at the level of entire chromosomes is in striking contrast to the overall pattern of structural conservation in the set of shared chromosomes. The lack of inversions and rearrangements is highly unusual for angiosperm mitochondrial genomes, which are often structurally dynamic even within species (27)(28)(29)(30). This difference is likely caused by a reduced rate of intragenomic recombination between small repeats in S. noctiflora mtDNA (22).…”

“…As in this study, the identification of multichromosomal structures in angiosperms has been based almost exclusively on mapping/ sequencing (21-23), but, in some other cases, sequence data have been supplemented with electrophoretic separation of chromosomes and electron microscopy-based observations (11,12,14,15,17,18,20,45,46). To date, the only direct characterization of chromosomal structure in an angiosperm multichromosomal mitochondrial genome was performed in Silene vulgaris (26)(27)(28)(29)(30). In this case, a Southern blot analysis of the smallest (∼5 kb) mitochondrial chromosome confirmed the existence of the predicted circular molecules but found that most of the DNA was present in multimeric forms that varied in susceptibility to exonuclease digestion, indicating diversity in molecular size and structure.…”

“…Angiosperm mitochondrial genomes are characterized by a number of unusual properties, including their large and variable sizes (ranging from ∼200 kb to over 10 Mb), low gene densities, extensive posttranscriptional modifications, and propensity to capture foreign DNA sequences (24,25). They generally exhibit very low rates of nucleotide substitution, but their structures are highly dynamic, varying extensively among and even within species as a result of frequent rearrangements and gain/loss of intergenic sequences (26)(27)(28)(29)(30). In most angiosperm mitochondria, there is also a high frequency of recombination between large repeated sequences within the genome, interconverting between a suite of alternative conformations that coexist within an individual (31).…”

Cell-to-cell movement of mitochondria in plants

“…Still, the rearranged region integrated into the chimeric mitochondrial genomes by homologous recombination preserving either the CMS or fertile mtDNA structure. Thus, nonhomologous end joining, the driving force behind mtDNA rearrangement during evolution, is not involved in the formation of mosaic mtDNAs (31,32). The rearranged mitochondrial genomes were stable for at least three seed generations.…”