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Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis
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 ye...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2011
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3193812/ https://www.ncbi.nlm.nih.gov/pubmed/21951689 http://dx.doi.org/10.1186/1741-7007-9-64 |
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author | Davila, Jaime I Arrieta-Montiel, Maria P Wamboldt, Yashitola Cao, Jun Hagmann, Joerg Shedge, Vikas Xu, Ying-Zhi Weigel, Detlef Mackenzie, Sally A |
author_facet | Davila, Jaime I Arrieta-Montiel, Maria P Wamboldt, Yashitola Cao, Jun Hagmann, Joerg Shedge, Vikas Xu, Ying-Zhi Weigel, Detlef Mackenzie, Sally A |
author_sort | Davila, Jaime I |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-3193812 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2011 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-31938122011-10-16 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 BMC Biol Research Article 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. BioMed Central 2011-09-27 /pmc/articles/PMC3193812/ /pubmed/21951689 http://dx.doi.org/10.1186/1741-7007-9-64 Text en Copyright ©2011 Davila et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Article 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 |
title | Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis |
title_full | Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis |
title_fullStr | Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis |
title_full_unstemmed | Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis |
title_short | Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis |
title_sort | double-strand break repair processes drive evolution of the mitochondrial genome in arabidopsis |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3193812/ https://www.ncbi.nlm.nih.gov/pubmed/21951689 http://dx.doi.org/10.1186/1741-7007-9-64 |
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