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Evolution of linear chromosomes and multipartite genomes in yeast mitochondria.

Valach M, Farkas Z, Fricova D, Kovac J, Brejova B, Vinar T, Pfeiffer I, Kucsera J, Tomaska L, Lang BF, Nosek J - Nucleic Acids Res. (2011)

Bottom Line: Our survey revealed a puzzling variability of genome architecture, including circular- and linear-mapping and multipartite linear forms.We propose that the arrangement of large inverted repeats identified in these genomes plays a crucial role in alterations of their molecular architectures.We suggest that molecular transactions generating linear mitochondrial DNA molecules with defined telomeric structures may parallel the evolutionary emergence of linear chromosomes and multipartite genomes in general and may provide clues for the origin of telomeres and pathways implicated in their maintenance.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry, Comenius University, Mlynska dolina CH-1, 842 15 Bratislava, Slovak republic.

ABSTRACT
Mitochondrial genome diversity in closely related species provides an excellent platform for investigation of chromosome architecture and its evolution by means of comparative genomics. In this study, we determined the complete mitochondrial DNA sequences of eight Candida species and analyzed their molecular architectures. Our survey revealed a puzzling variability of genome architecture, including circular- and linear-mapping and multipartite linear forms. We propose that the arrangement of large inverted repeats identified in these genomes plays a crucial role in alterations of their molecular architectures. In specific arrangements, the inverted repeats appear to function as resolution elements, allowing genome conversion among different topologies, eventually leading to genome fragmentation into multiple linear DNA molecules. We suggest that molecular transactions generating linear mitochondrial DNA molecules with defined telomeric structures may parallel the evolutionary emergence of linear chromosomes and multipartite genomes in general and may provide clues for the origin of telomeres and pathways implicated in their maintenance.

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Restriction enzyme analysis reveals circular-mapping genome isomers. Candida neerlandica (A), C. maltosa (B) and C. sojae (C) mtDNAs were digested with the restriction enzyme combinations BamHI + PvuII, ApaLI + MluI and AgeI + ApaLI, respectively, and electrophoretically separated in 0.9% (w/v) agarose gel. Black arrows indicate the DNA fragments present in both isomers, grey arrows label the pair of fragments specific to the isomers I or II. Schemes illustrate both isomers with the position of inverted repeats (shown bold within the inner circle) and corresponding restriction enzyme fragments (the outer circle).
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Figure 2: Restriction enzyme analysis reveals circular-mapping genome isomers. Candida neerlandica (A), C. maltosa (B) and C. sojae (C) mtDNAs were digested with the restriction enzyme combinations BamHI + PvuII, ApaLI + MluI and AgeI + ApaLI, respectively, and electrophoretically separated in 0.9% (w/v) agarose gel. Black arrows indicate the DNA fragments present in both isomers, grey arrows label the pair of fragments specific to the isomers I or II. Schemes illustrate both isomers with the position of inverted repeats (shown bold within the inner circle) and corresponding restriction enzyme fragments (the outer circle).

Mentions: Since the mitochondrial genome of C. albicans occurs in two isomers (42,71), we examined the presence of genome isomers also in other species with polydisperse mtDNAs. Restriction enzyme analysis of the mtDNAs from C. maltosa, C. neerlandica and C. sojae identified four minor mtDNA fragments (e.g. ∼15, ∼13, ∼9 and ∼7 kb in the case of C. neerlandica mtDNA digested with BamHI and PvuII) indicating that they contain a circular-mapping genome with large repeated regions generating two isomers that are present in a stoichiometric ratio (Figure 2A–C). Subsequent sequence analysis confirmed that all three genomes contain large inverted repeats (LIRs) that could be involved in the flip-flop recombination generating genome isomers. This is in line with the observation that the LIRs represent recombination hotspots in C. albicans mtDNA (42). The LIRs were also detected in the C. alai mtDNA sequence, but the presence of contaminating linear plasmids rendered the identification of isomers by restriction enzyme analysis inconclusive.Figure 2.


Evolution of linear chromosomes and multipartite genomes in yeast mitochondria.

Valach M, Farkas Z, Fricova D, Kovac J, Brejova B, Vinar T, Pfeiffer I, Kucsera J, Tomaska L, Lang BF, Nosek J - Nucleic Acids Res. (2011)

Restriction enzyme analysis reveals circular-mapping genome isomers. Candida neerlandica (A), C. maltosa (B) and C. sojae (C) mtDNAs were digested with the restriction enzyme combinations BamHI + PvuII, ApaLI + MluI and AgeI + ApaLI, respectively, and electrophoretically separated in 0.9% (w/v) agarose gel. Black arrows indicate the DNA fragments present in both isomers, grey arrows label the pair of fragments specific to the isomers I or II. Schemes illustrate both isomers with the position of inverted repeats (shown bold within the inner circle) and corresponding restriction enzyme fragments (the outer circle).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3105423&req=5

Figure 2: Restriction enzyme analysis reveals circular-mapping genome isomers. Candida neerlandica (A), C. maltosa (B) and C. sojae (C) mtDNAs were digested with the restriction enzyme combinations BamHI + PvuII, ApaLI + MluI and AgeI + ApaLI, respectively, and electrophoretically separated in 0.9% (w/v) agarose gel. Black arrows indicate the DNA fragments present in both isomers, grey arrows label the pair of fragments specific to the isomers I or II. Schemes illustrate both isomers with the position of inverted repeats (shown bold within the inner circle) and corresponding restriction enzyme fragments (the outer circle).
Mentions: Since the mitochondrial genome of C. albicans occurs in two isomers (42,71), we examined the presence of genome isomers also in other species with polydisperse mtDNAs. Restriction enzyme analysis of the mtDNAs from C. maltosa, C. neerlandica and C. sojae identified four minor mtDNA fragments (e.g. ∼15, ∼13, ∼9 and ∼7 kb in the case of C. neerlandica mtDNA digested with BamHI and PvuII) indicating that they contain a circular-mapping genome with large repeated regions generating two isomers that are present in a stoichiometric ratio (Figure 2A–C). Subsequent sequence analysis confirmed that all three genomes contain large inverted repeats (LIRs) that could be involved in the flip-flop recombination generating genome isomers. This is in line with the observation that the LIRs represent recombination hotspots in C. albicans mtDNA (42). The LIRs were also detected in the C. alai mtDNA sequence, but the presence of contaminating linear plasmids rendered the identification of isomers by restriction enzyme analysis inconclusive.Figure 2.

Bottom Line: Our survey revealed a puzzling variability of genome architecture, including circular- and linear-mapping and multipartite linear forms.We propose that the arrangement of large inverted repeats identified in these genomes plays a crucial role in alterations of their molecular architectures.We suggest that molecular transactions generating linear mitochondrial DNA molecules with defined telomeric structures may parallel the evolutionary emergence of linear chromosomes and multipartite genomes in general and may provide clues for the origin of telomeres and pathways implicated in their maintenance.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry, Comenius University, Mlynska dolina CH-1, 842 15 Bratislava, Slovak republic.

ABSTRACT
Mitochondrial genome diversity in closely related species provides an excellent platform for investigation of chromosome architecture and its evolution by means of comparative genomics. In this study, we determined the complete mitochondrial DNA sequences of eight Candida species and analyzed their molecular architectures. Our survey revealed a puzzling variability of genome architecture, including circular- and linear-mapping and multipartite linear forms. We propose that the arrangement of large inverted repeats identified in these genomes plays a crucial role in alterations of their molecular architectures. In specific arrangements, the inverted repeats appear to function as resolution elements, allowing genome conversion among different topologies, eventually leading to genome fragmentation into multiple linear DNA molecules. We suggest that molecular transactions generating linear mitochondrial DNA molecules with defined telomeric structures may parallel the evolutionary emergence of linear chromosomes and multipartite genomes in general and may provide clues for the origin of telomeres and pathways implicated in their maintenance.

Show MeSH
Related in: MedlinePlus