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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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A hypothetical pathway leading to mitochondrial genomes of C. parapsilosis and C. jiufengensis from the most recent common ancestor. We propose a simple scenario allowing delineation of the gene order found in both the circular-mapping genome of C. jiufengensis and the ‘true’ linear genome of C. parapsilosis from a reconstructed circular-mapping ancestor inferred by the analysis shown in Figure 7 and Supplementary Figure S2. The process includes reciprocal recombination events between the gene pairs (i) rnl/cox1 and nad3/atp6 or (ii) cox2/trnN and cob/atp9, followed by opening of the circular-mapping genome between the genes nad3 and atp6 in the latter case. Note that the circular-mapping genome intermediate prior its linearization has identical gene order as the mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis (51,52).
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Figure 8: A hypothetical pathway leading to mitochondrial genomes of C. parapsilosis and C. jiufengensis from the most recent common ancestor. We propose a simple scenario allowing delineation of the gene order found in both the circular-mapping genome of C. jiufengensis and the ‘true’ linear genome of C. parapsilosis from a reconstructed circular-mapping ancestor inferred by the analysis shown in Figure 7 and Supplementary Figure S2. The process includes reciprocal recombination events between the gene pairs (i) rnl/cox1 and nad3/atp6 or (ii) cox2/trnN and cob/atp9, followed by opening of the circular-mapping genome between the genes nad3 and atp6 in the latter case. Note that the circular-mapping genome intermediate prior its linearization has identical gene order as the mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis (51,52).

Mentions: Our previous reports (10,46) as well as the comparison of mtDNAs examined in this study revealed a number of conserved gene clusters. This prompted us to use the gene orders of 15 species from the ‘CTG clade’ for reconstruction of possible ancestral mitochondrial genomes in corresponding nodes of the phylogenetic tree (Figure 7), using the DCJ model (69) and local optimization procedures (70). For example, the presumed ancestor of C. parapsilosis and C. jiufengensis, which differ by the genome form, had a circular-mapping genome. We propose a simple evolutionary scenario leading to the linear-mapping mitochondrial genome (Figure 8). In this scenario, a resolution of a recombination transaction between the gene pairs cox2-trnN and cob-atp9 results in the formation of mtDNA with the gene order observed in circularized mutants of C. orthopsilosis and C. metapsilosis and its subsequent linearization between the genes nad3 and atp6 generates a linear mtDNA with genetic organization observed in the linear-mapping mitochondrial genomes of C. metapsilosis, C. orthopsilosis and C. parapsilosis. In contrast, recombination between the gene pairs rnl-cox1 and atp6-nad3 in the presumed ancestral genome leads to the identical arrangement of genes as is present in the C. jiufengensis mtDNA.Figure 7.


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)

A hypothetical pathway leading to mitochondrial genomes of C. parapsilosis and C. jiufengensis from the most recent common ancestor. We propose a simple scenario allowing delineation of the gene order found in both the circular-mapping genome of C. jiufengensis and the ‘true’ linear genome of C. parapsilosis from a reconstructed circular-mapping ancestor inferred by the analysis shown in Figure 7 and Supplementary Figure S2. The process includes reciprocal recombination events between the gene pairs (i) rnl/cox1 and nad3/atp6 or (ii) cox2/trnN and cob/atp9, followed by opening of the circular-mapping genome between the genes nad3 and atp6 in the latter case. Note that the circular-mapping genome intermediate prior its linearization has identical gene order as the mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis (51,52).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

Figure 8: A hypothetical pathway leading to mitochondrial genomes of C. parapsilosis and C. jiufengensis from the most recent common ancestor. We propose a simple scenario allowing delineation of the gene order found in both the circular-mapping genome of C. jiufengensis and the ‘true’ linear genome of C. parapsilosis from a reconstructed circular-mapping ancestor inferred by the analysis shown in Figure 7 and Supplementary Figure S2. The process includes reciprocal recombination events between the gene pairs (i) rnl/cox1 and nad3/atp6 or (ii) cox2/trnN and cob/atp9, followed by opening of the circular-mapping genome between the genes nad3 and atp6 in the latter case. Note that the circular-mapping genome intermediate prior its linearization has identical gene order as the mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis (51,52).
Mentions: Our previous reports (10,46) as well as the comparison of mtDNAs examined in this study revealed a number of conserved gene clusters. This prompted us to use the gene orders of 15 species from the ‘CTG clade’ for reconstruction of possible ancestral mitochondrial genomes in corresponding nodes of the phylogenetic tree (Figure 7), using the DCJ model (69) and local optimization procedures (70). For example, the presumed ancestor of C. parapsilosis and C. jiufengensis, which differ by the genome form, had a circular-mapping genome. We propose a simple evolutionary scenario leading to the linear-mapping mitochondrial genome (Figure 8). In this scenario, a resolution of a recombination transaction between the gene pairs cox2-trnN and cob-atp9 results in the formation of mtDNA with the gene order observed in circularized mutants of C. orthopsilosis and C. metapsilosis and its subsequent linearization between the genes nad3 and atp6 generates a linear mtDNA with genetic organization observed in the linear-mapping mitochondrial genomes of C. metapsilosis, C. orthopsilosis and C. parapsilosis. In contrast, recombination between the gene pairs rnl-cox1 and atp6-nad3 in the presumed ancestral genome leads to the identical arrangement of genes as is present in the C. jiufengensis mtDNA.Figure 7.

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