The alternative reality of plant mitochondrial DNA: One ring does not rule them all

Alexander Kozik, Beth A. Rowan, Dean Lavelle, Lidija Berke, M. Eric Schranz, Richard W Michelmore, Alan C. Christensen

Research output: Contribution to journalArticle

Abstract

Plant mitochondrial genomes are usually assembled and displayed as circular maps based on the widely-held view across the broad community of life scientists that circular genome-sized molecules are the primary form of plant mitochondrial DNA, despite the understanding by plant mitochondrial researchers that this is an inaccurate and outdated concept. Many plant mitochondrial genomes have one or more pairs of large repeats that can act as sites for inter- or intramolecular recombination, leading to multiple alternative arrangements (isoforms). Most mitochondrial genomes have been assembled using methods unable to capture the complete spectrum of isoforms within a species, leading to an incomplete inference of their structure and recombinational activity. To document and investigate underlying reasons for structural diversity in plant mitochondrial DNA, we used long-read (PacBio) and short-read (Illumina) sequencing data to assemble and compare mitochondrial genomes of domesticated (Lactuca sativa) and wild (L. saligna and L. serriola) lettuce species. We characterized a comprehensive, complex set of isoforms within each species and compared genome structures between species. Physical analysis of L. sativa mtDNA molecules by fluorescence microscopy revealed a variety of linear, branched, and circular structures. The mitochondrial genomes for L. sativa and L. serriola were identical in sequence and arrangement and differed substantially from L. saligna, indicating that the mitochondrial genome structure did not change during domestication. From the isoforms in our data, we infer that recombination occurs at repeats of all sizes at variable frequencies. The differences in genome structure between L. saligna and the two other Lactuca species can be largely explained by rare recombination events that rearranged the structure. Our data demonstrate that representations of plant mitochondrial genomes as simple, circular molecules are not accurate descriptions of their true nature and that in reality plant mitochondrial DNA is a complex, dynamic mixture of forms.

Original languageEnglish (US)
Pages (from-to)e1008373
JournalPLoS genetics
Volume15
Issue number8
DOIs
StatePublished - Aug 1 2019

Fingerprint

Plant DNA
Mitochondrial Genome
Mitochondrial DNA
mitochondrial DNA
genome
Lettuce
Plant Genome
Protein Isoforms
Lactuca sativa
Genetic Recombination
Genome
recombination
Lactuca saligna
Lactuca serriola
Lactuca
plant architecture
mitochondrial genome
fluorescence microscopy
domestication
Complex Mixtures

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Kozik, A., Rowan, B. A., Lavelle, D., Berke, L., Schranz, M. E., Michelmore, R. W., & Christensen, A. C. (2019). The alternative reality of plant mitochondrial DNA: One ring does not rule them all. PLoS genetics, 15(8), e1008373. https://doi.org/10.1371/journal.pgen.1008373

The alternative reality of plant mitochondrial DNA : One ring does not rule them all. / Kozik, Alexander; Rowan, Beth A.; Lavelle, Dean; Berke, Lidija; Schranz, M. Eric; Michelmore, Richard W; Christensen, Alan C.

In: PLoS genetics, Vol. 15, No. 8, 01.08.2019, p. e1008373.

Research output: Contribution to journalArticle

Kozik, A, Rowan, BA, Lavelle, D, Berke, L, Schranz, ME, Michelmore, RW & Christensen, AC 2019, 'The alternative reality of plant mitochondrial DNA: One ring does not rule them all', PLoS genetics, vol. 15, no. 8, pp. e1008373. https://doi.org/10.1371/journal.pgen.1008373
Kozik A, Rowan BA, Lavelle D, Berke L, Schranz ME, Michelmore RW et al. The alternative reality of plant mitochondrial DNA: One ring does not rule them all. PLoS genetics. 2019 Aug 1;15(8):e1008373. https://doi.org/10.1371/journal.pgen.1008373
Kozik, Alexander ; Rowan, Beth A. ; Lavelle, Dean ; Berke, Lidija ; Schranz, M. Eric ; Michelmore, Richard W ; Christensen, Alan C. / The alternative reality of plant mitochondrial DNA : One ring does not rule them all. In: PLoS genetics. 2019 ; Vol. 15, No. 8. pp. e1008373.
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