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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 hypothesis on the origin of linear chromosomes in yeast mitochondria. (A) A circular-mapping genome represented by linear polydisperse mtDNAs with [e.g. C. glabrata, S. cerevisiae (40)] or potentially without [e.g. C. albicans (42)] a fraction of circular molecules. (B) Genome rearrangements may result in the formation of a palindrome allowing the resolution of a circular-mapping genome into linear chromosomes with defined terminal structures such as t-hairpins. Such genomes were observed in several species [e.g. P. pijperi and W. mrakii (11,44), C. viswanathii] containing uniform linear mtDNAs, with t-hairpins resolved from circular molecules (monomers and dimers) and/or linear polydisperse mtDNAs. (C) Multiple resolution elements (i.e. two types of LIRs) allow the genome fragmentation into multiple linear chromosomes (e.g. C. frijolesensis, C. labiduridarum). (D) The termini of the linear chromosomes may provide a substrate for further elongation via active maintenance mechanisms, such as the t-circle dependent pathway observed in ‘true’ linear genomes (e.g. C. metapsilosis, C. orthopsilosis, C. parapsilosis, C. salmanticensis) (49,50). Defects in the telomere maintenance result in the genome circularization via end-to-end fusion, as in mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis containing circular-mapping genomes (51,52).
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Figure 9: A hypothesis on the origin of linear chromosomes in yeast mitochondria. (A) A circular-mapping genome represented by linear polydisperse mtDNAs with [e.g. C. glabrata, S. cerevisiae (40)] or potentially without [e.g. C. albicans (42)] a fraction of circular molecules. (B) Genome rearrangements may result in the formation of a palindrome allowing the resolution of a circular-mapping genome into linear chromosomes with defined terminal structures such as t-hairpins. Such genomes were observed in several species [e.g. P. pijperi and W. mrakii (11,44), C. viswanathii] containing uniform linear mtDNAs, with t-hairpins resolved from circular molecules (monomers and dimers) and/or linear polydisperse mtDNAs. (C) Multiple resolution elements (i.e. two types of LIRs) allow the genome fragmentation into multiple linear chromosomes (e.g. C. frijolesensis, C. labiduridarum). (D) The termini of the linear chromosomes may provide a substrate for further elongation via active maintenance mechanisms, such as the t-circle dependent pathway observed in ‘true’ linear genomes (e.g. C. metapsilosis, C. orthopsilosis, C. parapsilosis, C. salmanticensis) (49,50). Defects in the telomere maintenance result in the genome circularization via end-to-end fusion, as in mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis containing circular-mapping genomes (51,52).

Mentions: In a number of species, replication of linear-mapping genomes relies on circular intermediates (monomers or dimers) generating linear concatemers via rolling circle and/or recombination-dependent replication mechanisms (44,45). In contrast, no genome-sized circles or genome concatemers were detected in mitochondria of C. parapsilosis and C. subhashii, which harbor uniform linear mtDNA molecules terminating with t-arrays and t-proteins, respectively (10,20,46). Hence, these linear-mapping genomes can be considered as ‘true’ linear genomes. This is further underlined by the presence of active telomere maintenance pathways ensuring their complete replication. We posit that linear-mapping genomes with terminal structures such as t-hairpins correspond to a transient state between circular mapping and ‘truly’ monomeric linear mitochondrial genomes. T-hairpins formed at linear mtDNA termini provide substrates for terminus elongation by an active telomere maintenance pathway [e.g. recombination-dependent mechanism operating in C. parapsilosis mitochondria (49,50)]. Once this pathway ensures the stability of a linear genome, circular replication intermediates and/or polydisperse mtDNAs become dispensable for the system. Conversely, a defect in the telomere-maintenance pathway may result in intramolecular end-to-end fusion, thus re-establishing the original circular-mapping mitochondrial genome architecture (Figure 9).Figure 9.


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 hypothesis on the origin of linear chromosomes in yeast mitochondria. (A) A circular-mapping genome represented by linear polydisperse mtDNAs with [e.g. C. glabrata, S. cerevisiae (40)] or potentially without [e.g. C. albicans (42)] a fraction of circular molecules. (B) Genome rearrangements may result in the formation of a palindrome allowing the resolution of a circular-mapping genome into linear chromosomes with defined terminal structures such as t-hairpins. Such genomes were observed in several species [e.g. P. pijperi and W. mrakii (11,44), C. viswanathii] containing uniform linear mtDNAs, with t-hairpins resolved from circular molecules (monomers and dimers) and/or linear polydisperse mtDNAs. (C) Multiple resolution elements (i.e. two types of LIRs) allow the genome fragmentation into multiple linear chromosomes (e.g. C. frijolesensis, C. labiduridarum). (D) The termini of the linear chromosomes may provide a substrate for further elongation via active maintenance mechanisms, such as the t-circle dependent pathway observed in ‘true’ linear genomes (e.g. C. metapsilosis, C. orthopsilosis, C. parapsilosis, C. salmanticensis) (49,50). Defects in the telomere maintenance result in the genome circularization via end-to-end fusion, as in mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis containing circular-mapping genomes (51,52).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

Figure 9: A hypothesis on the origin of linear chromosomes in yeast mitochondria. (A) A circular-mapping genome represented by linear polydisperse mtDNAs with [e.g. C. glabrata, S. cerevisiae (40)] or potentially without [e.g. C. albicans (42)] a fraction of circular molecules. (B) Genome rearrangements may result in the formation of a palindrome allowing the resolution of a circular-mapping genome into linear chromosomes with defined terminal structures such as t-hairpins. Such genomes were observed in several species [e.g. P. pijperi and W. mrakii (11,44), C. viswanathii] containing uniform linear mtDNAs, with t-hairpins resolved from circular molecules (monomers and dimers) and/or linear polydisperse mtDNAs. (C) Multiple resolution elements (i.e. two types of LIRs) allow the genome fragmentation into multiple linear chromosomes (e.g. C. frijolesensis, C. labiduridarum). (D) The termini of the linear chromosomes may provide a substrate for further elongation via active maintenance mechanisms, such as the t-circle dependent pathway observed in ‘true’ linear genomes (e.g. C. metapsilosis, C. orthopsilosis, C. parapsilosis, C. salmanticensis) (49,50). Defects in the telomere maintenance result in the genome circularization via end-to-end fusion, as in mitochondrial telomere mutants of C. metapsilosis and C. orthopsilosis containing circular-mapping genomes (51,52).
Mentions: In a number of species, replication of linear-mapping genomes relies on circular intermediates (monomers or dimers) generating linear concatemers via rolling circle and/or recombination-dependent replication mechanisms (44,45). In contrast, no genome-sized circles or genome concatemers were detected in mitochondria of C. parapsilosis and C. subhashii, which harbor uniform linear mtDNA molecules terminating with t-arrays and t-proteins, respectively (10,20,46). Hence, these linear-mapping genomes can be considered as ‘true’ linear genomes. This is further underlined by the presence of active telomere maintenance pathways ensuring their complete replication. We posit that linear-mapping genomes with terminal structures such as t-hairpins correspond to a transient state between circular mapping and ‘truly’ monomeric linear mitochondrial genomes. T-hairpins formed at linear mtDNA termini provide substrates for terminus elongation by an active telomere maintenance pathway [e.g. recombination-dependent mechanism operating in C. parapsilosis mitochondria (49,50)]. Once this pathway ensures the stability of a linear genome, circular replication intermediates and/or polydisperse mtDNAs become dispensable for the system. Conversely, a defect in the telomere-maintenance pathway may result in intramolecular end-to-end fusion, thus re-establishing the original circular-mapping mitochondrial genome architecture (Figure 9).Figure 9.

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