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

Sloan D.B., Müller K., McCauley D.E., Taylor D.R., Štorchová H.
NEW PHYTOLOGIST 196: 1228-1239, 2012

Keywords: cytoplasmic male sterility, endosymbiotic gene transfer, mitochondrial genome structure, polymorphism, 454 pyrosequencing
Abstract: In angiosperms, mitochondrial-encoded genes can cause cytoplasmic male sterility (CMS), which results in the co-existence of phenotypically female and hermaphroditic individuals within a population (gynodioecy). However, the scarcity of whole mitochondrial genome sequences from naturally gynodioecious populations limits our evolutionary understanding of these systems. To characterize patterns of mitochondrial DNA (mtDNA) variation within a gynodioecious species, we compared four complete mitochondrial genomes from the bladder campion Silene vulgaris (Caryophyllaceae) and found unprecedented levels of intraspecific diversity for plant 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 their gene complement, with the ribosomal proteins 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 repeat sequences (<250 bp). Some mitochondrial genes exhibit atypically high frequencies of single nucleotide polymorphisms (SNPs), 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 characterized by the coexistence of both monomeric circles and multimeric forms. Taken together, our observations show that S. vulgaris harbors an unusually high amount of variation in mtDNA sequence and structure. We discuss the extent to which this variation might be related to CMS.
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IEB authors: Karel Müller, Helena Štorchová