Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility

Abstract

Summary In angiosperms, mitochondrial‐encoded genes can cause cytoplasmic male sterility (CMS), resulting in the coexistence of female and hermaphroditic individuals (gynodioecy). We compared four complete mitochondrial genomes from the gynodioecious species Silene vulgaris and found unprecedented amounts of intraspecific diversity for plant mitochondrial DNA (mtDNA). Remarkably, only about half of overall sequence content is shared between any pair of genomes. The four mtDNAs range in size from 361 to 429 kb and differ in gene complement, with rpl5 and rps13 being intact in some genomes but absent or pseudogenized in others. The genomes exhibit essentially no conservation of synteny and are highly repetitive, with evidence of reciprocal recombination occurring even across short repeats (< 250 bp). Some mitochondrial genes exhibit atypically high degrees of nucleotide polymorphism, while others are invariant. The genomes also contain a variable number of small autonomously mapping chromosomes, which have only recently been identified in angiosperm mtDNA. Southern blot analysis of one of these chromosomes indicated a complex in vivo structure consisting of both monomeric circles and multimeric forms. We conclude that S. vulgaris harbors an unusually large degree of variation in mtDNA sequence and structure and discuss the extent to which this variation might be related to CMS.

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

“…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).…”

“…To validate the variation in chromosome abundance that was inferred from sequence coverage data, we performed absolute qPCR measurements of the two BRP chromosomes (30,60) with the most highly divergent read depths (Table S4). Three markers were assayed on each chromosome.…”

“…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).…”

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

“…As in Viscum, repeat length correlates with AC frequency in Mimulus. Finally, for four Silene vulgaris mitogenomes (361-429 kb in size) analyzed in aggregate (63), AC frequency averaged only 0.8% (median = 0.7%, range = 0.2-1.5%) for the 13 repeat pairs with a length of 50-100 bp for which at least five ACs were detected. The number of the repeats for which zero to four ACs were recovered was not reported, and therefore AC frequency again is markedly lower than in Viscum.…”