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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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Phylogenetic tree based on mtDNA encoded proteins. Phylogenetic tree was calculated from multiple sequence alignments of mitochondrial proteins by PhyloBayes (65). Posterior probabilities are shown at corresponding branches. The mitochondrial genome forms were reported elsewhere (10,20,22,51,55–57,60,86–89) or analyzed in this study. C—circular-mapping genome; L1, L2 and L3 indicate the type of linear-mapping genomes according to the telomeric structures, i.e. t-hairpins, t-arrays and invertron like with t-proteins, respectively; 3xL1—tripartite linear-mapping genome with t-hairpins (see Table 1 for details).
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Figure 6: Phylogenetic tree based on mtDNA encoded proteins. Phylogenetic tree was calculated from multiple sequence alignments of mitochondrial proteins by PhyloBayes (65). Posterior probabilities are shown at corresponding branches. The mitochondrial genome forms were reported elsewhere (10,20,22,51,55–57,60,86–89) or analyzed in this study. C—circular-mapping genome; L1, L2 and L3 indicate the type of linear-mapping genomes according to the telomeric structures, i.e. t-hairpins, t-arrays and invertron like with t-proteins, respectively; 3xL1—tripartite linear-mapping genome with t-hairpins (see Table 1 for details).

Mentions: We took advantage of the mtDNA-derived data and analyzed phylogenetic relationship of investigated yeast species by Bayesian and maximum likelihood methods. All three methods resulted essentially in the same tree topology. The tree calculated by PhyloBayes (Figure 6) is supported by high posterior probabilities on most branches and is consistent with the study of Fitzpatrick et al. (53) indicating that the monophyletic ‘CTG clade’ splits into two major lineages: the first represented by D. hansenii and P. sorbitophila, and the second by the C. albicans–C. parapsilosis group. Incorporation of additional recently described species (81–84) in the phylogenetic analysis revealed more detailed relationship among species in the latter lineage. This lineage splits into three subgroups (i.e. L. elongisporus–C. parapsilosis, C. maltosa–C. tropicalis and C. subhashii–C. alai) each containing species with circular- and linear-mapping mtDNAs. The occurrence of different types of mitochondrial telomeres (i.e. t-arrays in C. metapsilosis, C. orthopsilosis and C. parapsilosis; t-hairpins in C. viswanathii and C. frijolesensis; inverton-like telomeres with a t-protein in C. subhashii) in each subgroup is consistent with the tree topology. Similar to C. parapsilosis, the linear mitochondrial genome of C. salmanticensis terminates with t-arrays, although the sequence of its mitochondrial telomeres is different. Since C. salmanticensis belongs to early branching hemiascomycete lineages this linear mitochondrial genome emerged independently on linear mtDNAs in species from the ‘CTG clade’, presumably by employing similar molecular mechanism(s).Figure 6.


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)

Phylogenetic tree based on mtDNA encoded proteins. Phylogenetic tree was calculated from multiple sequence alignments of mitochondrial proteins by PhyloBayes (65). Posterior probabilities are shown at corresponding branches. The mitochondrial genome forms were reported elsewhere (10,20,22,51,55–57,60,86–89) or analyzed in this study. C—circular-mapping genome; L1, L2 and L3 indicate the type of linear-mapping genomes according to the telomeric structures, i.e. t-hairpins, t-arrays and invertron like with t-proteins, respectively; 3xL1—tripartite linear-mapping genome with t-hairpins (see Table 1 for details).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

Figure 6: Phylogenetic tree based on mtDNA encoded proteins. Phylogenetic tree was calculated from multiple sequence alignments of mitochondrial proteins by PhyloBayes (65). Posterior probabilities are shown at corresponding branches. The mitochondrial genome forms were reported elsewhere (10,20,22,51,55–57,60,86–89) or analyzed in this study. C—circular-mapping genome; L1, L2 and L3 indicate the type of linear-mapping genomes according to the telomeric structures, i.e. t-hairpins, t-arrays and invertron like with t-proteins, respectively; 3xL1—tripartite linear-mapping genome with t-hairpins (see Table 1 for details).
Mentions: We took advantage of the mtDNA-derived data and analyzed phylogenetic relationship of investigated yeast species by Bayesian and maximum likelihood methods. All three methods resulted essentially in the same tree topology. The tree calculated by PhyloBayes (Figure 6) is supported by high posterior probabilities on most branches and is consistent with the study of Fitzpatrick et al. (53) indicating that the monophyletic ‘CTG clade’ splits into two major lineages: the first represented by D. hansenii and P. sorbitophila, and the second by the C. albicans–C. parapsilosis group. Incorporation of additional recently described species (81–84) in the phylogenetic analysis revealed more detailed relationship among species in the latter lineage. This lineage splits into three subgroups (i.e. L. elongisporus–C. parapsilosis, C. maltosa–C. tropicalis and C. subhashii–C. alai) each containing species with circular- and linear-mapping mtDNAs. The occurrence of different types of mitochondrial telomeres (i.e. t-arrays in C. metapsilosis, C. orthopsilosis and C. parapsilosis; t-hairpins in C. viswanathii and C. frijolesensis; inverton-like telomeres with a t-protein in C. subhashii) in each subgroup is consistent with the tree topology. Similar to C. parapsilosis, the linear mitochondrial genome of C. salmanticensis terminates with t-arrays, although the sequence of its mitochondrial telomeres is different. Since C. salmanticensis belongs to early branching hemiascomycete lineages this linear mitochondrial genome emerged independently on linear mtDNAs in species from the ‘CTG clade’, presumably by employing similar molecular mechanism(s).Figure 6.

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