Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis

Jaime I. Davila, Maria P. Arrieta-Montiel, Yashitola Wamboldt, Jun Cao, Joerg Hagmann, Vikas Shedge, Ying Zhi Xu, Detlef Weigel, Sally A. Mackenzie

Research output: Contribution to journalArticle

104 Citations (Scopus)

Abstract

Background: The mitochondrial genome of higher plants is unusually dynamic, with recombination and nonhomologous end-joining (NHEJ) activities producing variability in size and organization. Plant mitochondrial DNA also generally displays much lower nucleotide substitution rates than mammalian or yeast systems. Arabidopsis displays these features and expedites characterization of the mitochondrial recombination surveillance gene MSH1 (MutS 1 homolog), lending itself to detailed study of de novo mitochondrial genome activity. In the present study, we investigated the underlying basis for unusual plant features as they contribute to rapid mitochondrial genome evolution.Results: We obtained evidence of double-strand break (DSB) repair, including NHEJ, sequence deletions and mitochondrial asymmetric recombination activity in Arabidopsis wild-type and msh1 mutants on the basis of data generated by Illumina deep sequencing and confirmed by DNA gel blot analysis. On a larger scale, with mitochondrial comparisons across 72 Arabidopsis ecotypes, similar evidence of DSB repair activity differentiated ecotypes. Forty-seven repeat pairs were active in DNA exchange in the msh1 mutant. Recombination sites showed asymmetrical DNA exchange within lengths of 50- to 556-bp sharing sequence identity as low as 85%. De novo asymmetrical recombination involved heteroduplex formation, gene conversion and mismatch repair activities. Substoichiometric shifting by asymmetrical exchange created the appearance of rapid sequence gain and loss in association with particular repeat classes.Conclusions: Extensive mitochondrial genomic variation within a single plant species derives largely from DSB activity and its repair. Observed gene conversion and mismatch repair activity contribute to the low nucleotide substitution rates seen in these genomes. On a phenotypic level, these patterns of rearrangement likely contribute to the reproductive versatility of higher plants.

Original languageEnglish (US)
Article number64
JournalBMC Biology
Volume9
DOIs
StatePublished - Sep 27 2011

Fingerprint

Mitochondrial Genome
Arabidopsis
Genetic Recombination
recombination
repair
Repair
genome
Genes
Ecotype
Gene Conversion
gene conversion
DNA Mismatch Repair
ecotype
ecotypes
DNA
Joining
gene
substitution
Substitution reactions
Nucleotides

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

Cite this

Davila, J. I., Arrieta-Montiel, M. P., Wamboldt, Y., Cao, J., Hagmann, J., Shedge, V., ... Mackenzie, S. A. (2011). Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biology, 9, [64]. https://doi.org/10.1186/1741-7007-9-64

Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. / Davila, Jaime I.; Arrieta-Montiel, Maria P.; Wamboldt, Yashitola; Cao, Jun; Hagmann, Joerg; Shedge, Vikas; Xu, Ying Zhi; Weigel, Detlef; Mackenzie, Sally A.

In: BMC Biology, Vol. 9, 64, 27.09.2011.

Research output: Contribution to journalArticle

Davila, JI, Arrieta-Montiel, MP, Wamboldt, Y, Cao, J, Hagmann, J, Shedge, V, Xu, YZ, Weigel, D & Mackenzie, SA 2011, 'Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis', BMC Biology, vol. 9, 64. https://doi.org/10.1186/1741-7007-9-64
Davila JI, Arrieta-Montiel MP, Wamboldt Y, Cao J, Hagmann J, Shedge V et al. Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biology. 2011 Sep 27;9. 64. https://doi.org/10.1186/1741-7007-9-64
Davila, Jaime I. ; Arrieta-Montiel, Maria P. ; Wamboldt, Yashitola ; Cao, Jun ; Hagmann, Joerg ; Shedge, Vikas ; Xu, Ying Zhi ; Weigel, Detlef ; Mackenzie, Sally A. / Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. In: BMC Biology. 2011 ; Vol. 9.
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