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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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Reconstruction of ancestral genomes. The figure shows possible ancestral gene orders and the number of events on each branch found by local optimization for the DCJ model. The intervals show range of numbers of events in equally parsimonious histories. Red connectors in the gene orders for present day and ancestral genomes represent inferred breakpoints on the branch to the nearest ancestor. Due to space constraints, the figure omits tRNA genes (even though the reconstructions were performed including tRNAs); full gene orders including tRNAs are shown in Supplementary Figure S2. The figure includes duplicated genes, which were restored after ancestral gene order reconstruction. Note that the linear and its circularized (mutant) mitochondrial genome forms of C. orthopsilosis were used in the analysis (51,60).
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Figure 7: Reconstruction of ancestral genomes. The figure shows possible ancestral gene orders and the number of events on each branch found by local optimization for the DCJ model. The intervals show range of numbers of events in equally parsimonious histories. Red connectors in the gene orders for present day and ancestral genomes represent inferred breakpoints on the branch to the nearest ancestor. Due to space constraints, the figure omits tRNA genes (even though the reconstructions were performed including tRNAs); full gene orders including tRNAs are shown in Supplementary Figure S2. The figure includes duplicated genes, which were restored after ancestral gene order reconstruction. Note that the linear and its circularized (mutant) mitochondrial genome forms of C. orthopsilosis were used in the analysis (51,60).

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)

Reconstruction of ancestral genomes. The figure shows possible ancestral gene orders and the number of events on each branch found by local optimization for the DCJ model. The intervals show range of numbers of events in equally parsimonious histories. Red connectors in the gene orders for present day and ancestral genomes represent inferred breakpoints on the branch to the nearest ancestor. Due to space constraints, the figure omits tRNA genes (even though the reconstructions were performed including tRNAs); full gene orders including tRNAs are shown in Supplementary Figure S2. The figure includes duplicated genes, which were restored after ancestral gene order reconstruction. Note that the linear and its circularized (mutant) mitochondrial genome forms of C. orthopsilosis were used in the analysis (51,60).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

Figure 7: Reconstruction of ancestral genomes. The figure shows possible ancestral gene orders and the number of events on each branch found by local optimization for the DCJ model. The intervals show range of numbers of events in equally parsimonious histories. Red connectors in the gene orders for present day and ancestral genomes represent inferred breakpoints on the branch to the nearest ancestor. Due to space constraints, the figure omits tRNA genes (even though the reconstructions were performed including tRNAs); full gene orders including tRNAs are shown in Supplementary Figure S2. The figure includes duplicated genes, which were restored after ancestral gene order reconstruction. Note that the linear and its circularized (mutant) mitochondrial genome forms of C. orthopsilosis were used in the analysis (51,60).
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