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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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PFGE analysis of the yeast mtDNAs. The whole-cell DNA samples were separated by PFGE using a CHEF Mapper XA Chiller System (Biorad), blotted onto a nylon membrane and hybridized with mtDNA-derived probes as described in ‘Material and Methods’ section. Lane 1—C. viswanathii CBS 4024; lane 2—C. sojae CBS 7871; lane 3—C. maltosa CBS 5611; lane 4—C. neerlandica NRRL Y-27057; lane 5—C. alai NRRL Y-27739; lane 6—C. labiduridarum NRRL Y-27940; lane 7—C. frijolesensis NRRL Y-48060; lane 8—C. subhashii CBS 10753; lane 9—C. jiufengensis CBS 10846; lane 10—C. albicans CBS 562. Note that three discrete bands migrating in the region <50 kb represent three linear mitochondrial chromosomes in C. labiduridarum and C. frijolesensis (lanes 6 and 7). In contrast, four bands in C. alai (lane 5) do not hybridize with mtDNA probes and correspond to linear DNA plasmids (data not shown).
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Figure 1: PFGE analysis of the yeast mtDNAs. The whole-cell DNA samples were separated by PFGE using a CHEF Mapper XA Chiller System (Biorad), blotted onto a nylon membrane and hybridized with mtDNA-derived probes as described in ‘Material and Methods’ section. Lane 1—C. viswanathii CBS 4024; lane 2—C. sojae CBS 7871; lane 3—C. maltosa CBS 5611; lane 4—C. neerlandica NRRL Y-27057; lane 5—C. alai NRRL Y-27739; lane 6—C. labiduridarum NRRL Y-27940; lane 7—C. frijolesensis NRRL Y-48060; lane 8—C. subhashii CBS 10753; lane 9—C. jiufengensis CBS 10846; lane 10—C. albicans CBS 562. Note that three discrete bands migrating in the region <50 kb represent three linear mitochondrial chromosomes in C. labiduridarum and C. frijolesensis (lanes 6 and 7). In contrast, four bands in C. alai (lane 5) do not hybridize with mtDNA probes and correspond to linear DNA plasmids (data not shown).

Mentions: Southern hybridization of PFGE separated yeast DNA samples (Figure 1) was performed with a probe containing an equimolar mixture of PCR products derived from cox2 (345 bp) and nad4 (374 bp) of corresponding species. The following PCR primers were used: 5′-TAGATGTNCCWACWCCWTGAG-3′ and 5′-AYTCRTATTTTCAATATCATTG-3′ (cox2); 5′-AGGTATHWTGGTWAARACACC-3′ and 5′-CAGGWGAWACDAAWCCATG-3′ (nad4). For C. subhashii, the equivalent PCR primers were 5′-CGTCCCAACACCATGAGG-3′ and 5′-ACTCGTACTTCCAGTACCACTG-3′ (cox2); 5′-AGGGATCATGGTCAAGACG-3′ and 5′-CTGGTGAGACTAGCCCGTG-3′ (nad4). In subsequent experiments, we used the following probes: P-668 (668 bp fragment amplified by PCR from the C. frijolesensis mtDNA using primers 5′-ATAATGGGTCAGTGAGTT-3′ and 5′-ACGTTCTCTAGCAGTTGA-3′), EH-1350 (1350 bp EcoRV-HindIII fragment from C. frijolesensis mtDNA), H-1030 (1030 bp HindIII fragment from C. neerlandica mtDNA), and Oligo-32 (32 nt oligonucleotide 5′-AATGAGATGAGGAAGTAAAGGGATAAGGATAA-3′, corresponding to a palindrome sequence in C. viswanathii mtDNA).Figure 1.


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)

PFGE analysis of the yeast mtDNAs. The whole-cell DNA samples were separated by PFGE using a CHEF Mapper XA Chiller System (Biorad), blotted onto a nylon membrane and hybridized with mtDNA-derived probes as described in ‘Material and Methods’ section. Lane 1—C. viswanathii CBS 4024; lane 2—C. sojae CBS 7871; lane 3—C. maltosa CBS 5611; lane 4—C. neerlandica NRRL Y-27057; lane 5—C. alai NRRL Y-27739; lane 6—C. labiduridarum NRRL Y-27940; lane 7—C. frijolesensis NRRL Y-48060; lane 8—C. subhashii CBS 10753; lane 9—C. jiufengensis CBS 10846; lane 10—C. albicans CBS 562. Note that three discrete bands migrating in the region <50 kb represent three linear mitochondrial chromosomes in C. labiduridarum and C. frijolesensis (lanes 6 and 7). In contrast, four bands in C. alai (lane 5) do not hybridize with mtDNA probes and correspond to linear DNA plasmids (data not shown).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

Figure 1: PFGE analysis of the yeast mtDNAs. The whole-cell DNA samples were separated by PFGE using a CHEF Mapper XA Chiller System (Biorad), blotted onto a nylon membrane and hybridized with mtDNA-derived probes as described in ‘Material and Methods’ section. Lane 1—C. viswanathii CBS 4024; lane 2—C. sojae CBS 7871; lane 3—C. maltosa CBS 5611; lane 4—C. neerlandica NRRL Y-27057; lane 5—C. alai NRRL Y-27739; lane 6—C. labiduridarum NRRL Y-27940; lane 7—C. frijolesensis NRRL Y-48060; lane 8—C. subhashii CBS 10753; lane 9—C. jiufengensis CBS 10846; lane 10—C. albicans CBS 562. Note that three discrete bands migrating in the region <50 kb represent three linear mitochondrial chromosomes in C. labiduridarum and C. frijolesensis (lanes 6 and 7). In contrast, four bands in C. alai (lane 5) do not hybridize with mtDNA probes and correspond to linear DNA plasmids (data not shown).
Mentions: Southern hybridization of PFGE separated yeast DNA samples (Figure 1) was performed with a probe containing an equimolar mixture of PCR products derived from cox2 (345 bp) and nad4 (374 bp) of corresponding species. The following PCR primers were used: 5′-TAGATGTNCCWACWCCWTGAG-3′ and 5′-AYTCRTATTTTCAATATCATTG-3′ (cox2); 5′-AGGTATHWTGGTWAARACACC-3′ and 5′-CAGGWGAWACDAAWCCATG-3′ (nad4). For C. subhashii, the equivalent PCR primers were 5′-CGTCCCAACACCATGAGG-3′ and 5′-ACTCGTACTTCCAGTACCACTG-3′ (cox2); 5′-AGGGATCATGGTCAAGACG-3′ and 5′-CTGGTGAGACTAGCCCGTG-3′ (nad4). In subsequent experiments, we used the following probes: P-668 (668 bp fragment amplified by PCR from the C. frijolesensis mtDNA using primers 5′-ATAATGGGTCAGTGAGTT-3′ and 5′-ACGTTCTCTAGCAGTTGA-3′), EH-1350 (1350 bp EcoRV-HindIII fragment from C. frijolesensis mtDNA), H-1030 (1030 bp HindIII fragment from C. neerlandica mtDNA), and Oligo-32 (32 nt oligonucleotide 5′-AATGAGATGAGGAAGTAAAGGGATAAGGATAA-3′, corresponding to a palindrome sequence in C. viswanathii mtDNA).Figure 1.

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