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Ancient diversification of eukaryotic MCM DNA replication proteins.

Liu Y, Richards TA, Aves SJ - BMC Evol. Biol. (2009)

Bottom Line: A multifaceted and heterogeneous Mcm2-7 hexamer evolved during the early evolution of the eukaryote cell in parallel with numerous other acquisitions in cell complexity and prior to the diversification of extant eukaryotes.The conservation of all six paralogues throughout the eukaryotes suggests that each Mcm2-7 hexamer component has an exclusive functional role, either by a combination of unique lock and key interactions between MCM hexamer subunits and/or by a range of novel side interactions.Mcm8 is highly divergent in all Drosophila species and may not provide a good model for Mcm8 in other eukaryotes.

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Affiliation: School of Biosciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter, EX4 4QD, UK. yl274@exeter.ac.uk

ABSTRACT

Background: Yeast and animal cells require six mini-chromosome maintenance proteins (Mcm2-7) for pre-replication complex formation, DNA replication initiation and DNA synthesis. These six individual MCM proteins form distinct heterogeneous subunits within a hexamer which is believed to form the replicative helicase and which associates with the essential but non-homologous Mcm10 protein during DNA replication. In contrast Archaea generally only possess one MCM homologue which forms a homohexameric MCM helicase. In some eukaryotes Mcm8 and Mcm9 paralogues also appear to be involved in DNA replication although their exact roles are unclear.

Results: We used comparative genomics and phylogenetics to reconstruct the diversification of the eukaryotic Mcm2-9 gene family, demonstrating that Mcm2-9 were formed by seven gene duplication events before the last common ancestor of the eukaryotes. Mcm2-7 protein paralogues were present in all eukaryote genomes studied suggesting that no gene loss or functional replacements have been tolerated during the evolutionary diversification of eukaryotes. Mcm8 and 9 are widely distributed in eukaryotes and group together on the MCM phylogenetic tree to the exclusion of all other MCM paralogues suggesting co-ancestry. Mcm8 and Mcm9 are absent in some taxa, including Trichomonas and Giardia, and appear to have been secondarily lost in some fungi and some animals. The presence and absence of Mcm8 and 9 is concordant in all taxa sampled with the exception of Drosophila species. Mcm10 is present in most eukaryotes sampled but shows no concordant pattern of presence or absence with Mcm8 or 9.

Conclusion: A multifaceted and heterogeneous Mcm2-7 hexamer evolved during the early evolution of the eukaryote cell in parallel with numerous other acquisitions in cell complexity and prior to the diversification of extant eukaryotes. The conservation of all six paralogues throughout the eukaryotes suggests that each Mcm2-7 hexamer component has an exclusive functional role, either by a combination of unique lock and key interactions between MCM hexamer subunits and/or by a range of novel side interactions. Mcm8 and 9 evolved early in eukaryote cell evolution and their pattern of presence or absence suggests that they may have linked functions. Mcm8 is highly divergent in all Drosophila species and may not provide a good model for Mcm8 in other eukaryotes.

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Taxonomic distribution of Mcm2-9 and a summarised phylogenetic tree of MCMs. This analysis shows that Mcm2-9 are present in the majority of the major eukaryotic 'supergroups' and that each MCM forms a moderate to strongly supported monophyletic group. Together these data demonstrate that Mcm2-9 were present in the last common eukaryotic ancestor. (A) Comparative genomic survey of MCM paralogues in 37 eukaryotic taxa. Mcm2-9 are shown on the x-axis and taxa are shown on the y-axis. Black circles indicate detections and open circles indicate no orthologues detected. Numbers within the black circles indicate the number of that specific MCM paralogue found in the taxa. Asterisks indicate species used for the "Noah's Ark" subset: for the results of the phylogenetic analysis see Additional file 5. (B) A summarised phylogenetic tree of MCMs based on Additional files 1, 2, 3, 4, emphasising the ML bootstrap support values for each MCM family, and relationships between each family which in most cases are weakly supported. The Archaea were used as an outgroup for reconstructing MCM phylogeny.
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Figure 1: Taxonomic distribution of Mcm2-9 and a summarised phylogenetic tree of MCMs. This analysis shows that Mcm2-9 are present in the majority of the major eukaryotic 'supergroups' and that each MCM forms a moderate to strongly supported monophyletic group. Together these data demonstrate that Mcm2-9 were present in the last common eukaryotic ancestor. (A) Comparative genomic survey of MCM paralogues in 37 eukaryotic taxa. Mcm2-9 are shown on the x-axis and taxa are shown on the y-axis. Black circles indicate detections and open circles indicate no orthologues detected. Numbers within the black circles indicate the number of that specific MCM paralogue found in the taxa. Asterisks indicate species used for the "Noah's Ark" subset: for the results of the phylogenetic analysis see Additional file 5. (B) A summarised phylogenetic tree of MCMs based on Additional files 1, 2, 3, 4, emphasising the ML bootstrap support values for each MCM family, and relationships between each family which in most cases are weakly supported. The Archaea were used as an outgroup for reconstructing MCM phylogeny.

Mentions: BLAST algorithms were used to identify MCM homologues encoded by the eukaryotic genomes of the 37 species listed in Table 1, covering five of the six eukaryotic supergroups [24,26-28] (Rhizaria unsampled). In Naegleria and Xenopus there were two proteins that grouped with Mcm3, and in Xenopus two Mcm6 proteins were found [29], providing the only examples of recent MCM duplication events among the taxa investigated. Comparative genomics and phylogenetic analysis (Fig. 1) showed that genes encoding six MCM proteins, Mcm2-7 homologues, were present in every eukaryotic genome sampled. These data suggest that the last common eukaryotic ancestor (LCEA) possessed all six Mcm2-7 paralogues and this ancient cell was therefore likely to contain a multi-subunit MCM protein complex composed of six paralogous proteins. These data suggest that an intricate and heterogeneous MCM protein complex evolved in an early phase of eukaryotic evolution.


Ancient diversification of eukaryotic MCM DNA replication proteins.

Liu Y, Richards TA, Aves SJ - BMC Evol. Biol. (2009)

Taxonomic distribution of Mcm2-9 and a summarised phylogenetic tree of MCMs. This analysis shows that Mcm2-9 are present in the majority of the major eukaryotic 'supergroups' and that each MCM forms a moderate to strongly supported monophyletic group. Together these data demonstrate that Mcm2-9 were present in the last common eukaryotic ancestor. (A) Comparative genomic survey of MCM paralogues in 37 eukaryotic taxa. Mcm2-9 are shown on the x-axis and taxa are shown on the y-axis. Black circles indicate detections and open circles indicate no orthologues detected. Numbers within the black circles indicate the number of that specific MCM paralogue found in the taxa. Asterisks indicate species used for the "Noah's Ark" subset: for the results of the phylogenetic analysis see Additional file 5. (B) A summarised phylogenetic tree of MCMs based on Additional files 1, 2, 3, 4, emphasising the ML bootstrap support values for each MCM family, and relationships between each family which in most cases are weakly supported. The Archaea were used as an outgroup for reconstructing MCM phylogeny.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667178&req=5

Figure 1: Taxonomic distribution of Mcm2-9 and a summarised phylogenetic tree of MCMs. This analysis shows that Mcm2-9 are present in the majority of the major eukaryotic 'supergroups' and that each MCM forms a moderate to strongly supported monophyletic group. Together these data demonstrate that Mcm2-9 were present in the last common eukaryotic ancestor. (A) Comparative genomic survey of MCM paralogues in 37 eukaryotic taxa. Mcm2-9 are shown on the x-axis and taxa are shown on the y-axis. Black circles indicate detections and open circles indicate no orthologues detected. Numbers within the black circles indicate the number of that specific MCM paralogue found in the taxa. Asterisks indicate species used for the "Noah's Ark" subset: for the results of the phylogenetic analysis see Additional file 5. (B) A summarised phylogenetic tree of MCMs based on Additional files 1, 2, 3, 4, emphasising the ML bootstrap support values for each MCM family, and relationships between each family which in most cases are weakly supported. The Archaea were used as an outgroup for reconstructing MCM phylogeny.
Mentions: BLAST algorithms were used to identify MCM homologues encoded by the eukaryotic genomes of the 37 species listed in Table 1, covering five of the six eukaryotic supergroups [24,26-28] (Rhizaria unsampled). In Naegleria and Xenopus there were two proteins that grouped with Mcm3, and in Xenopus two Mcm6 proteins were found [29], providing the only examples of recent MCM duplication events among the taxa investigated. Comparative genomics and phylogenetic analysis (Fig. 1) showed that genes encoding six MCM proteins, Mcm2-7 homologues, were present in every eukaryotic genome sampled. These data suggest that the last common eukaryotic ancestor (LCEA) possessed all six Mcm2-7 paralogues and this ancient cell was therefore likely to contain a multi-subunit MCM protein complex composed of six paralogous proteins. These data suggest that an intricate and heterogeneous MCM protein complex evolved in an early phase of eukaryotic evolution.

Bottom Line: A multifaceted and heterogeneous Mcm2-7 hexamer evolved during the early evolution of the eukaryote cell in parallel with numerous other acquisitions in cell complexity and prior to the diversification of extant eukaryotes.The conservation of all six paralogues throughout the eukaryotes suggests that each Mcm2-7 hexamer component has an exclusive functional role, either by a combination of unique lock and key interactions between MCM hexamer subunits and/or by a range of novel side interactions.Mcm8 is highly divergent in all Drosophila species and may not provide a good model for Mcm8 in other eukaryotes.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Biosciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter, EX4 4QD, UK. yl274@exeter.ac.uk

ABSTRACT

Background: Yeast and animal cells require six mini-chromosome maintenance proteins (Mcm2-7) for pre-replication complex formation, DNA replication initiation and DNA synthesis. These six individual MCM proteins form distinct heterogeneous subunits within a hexamer which is believed to form the replicative helicase and which associates with the essential but non-homologous Mcm10 protein during DNA replication. In contrast Archaea generally only possess one MCM homologue which forms a homohexameric MCM helicase. In some eukaryotes Mcm8 and Mcm9 paralogues also appear to be involved in DNA replication although their exact roles are unclear.

Results: We used comparative genomics and phylogenetics to reconstruct the diversification of the eukaryotic Mcm2-9 gene family, demonstrating that Mcm2-9 were formed by seven gene duplication events before the last common ancestor of the eukaryotes. Mcm2-7 protein paralogues were present in all eukaryote genomes studied suggesting that no gene loss or functional replacements have been tolerated during the evolutionary diversification of eukaryotes. Mcm8 and 9 are widely distributed in eukaryotes and group together on the MCM phylogenetic tree to the exclusion of all other MCM paralogues suggesting co-ancestry. Mcm8 and Mcm9 are absent in some taxa, including Trichomonas and Giardia, and appear to have been secondarily lost in some fungi and some animals. The presence and absence of Mcm8 and 9 is concordant in all taxa sampled with the exception of Drosophila species. Mcm10 is present in most eukaryotes sampled but shows no concordant pattern of presence or absence with Mcm8 or 9.

Conclusion: A multifaceted and heterogeneous Mcm2-7 hexamer evolved during the early evolution of the eukaryote cell in parallel with numerous other acquisitions in cell complexity and prior to the diversification of extant eukaryotes. The conservation of all six paralogues throughout the eukaryotes suggests that each Mcm2-7 hexamer component has an exclusive functional role, either by a combination of unique lock and key interactions between MCM hexamer subunits and/or by a range of novel side interactions. Mcm8 and 9 evolved early in eukaryote cell evolution and their pattern of presence or absence suggests that they may have linked functions. Mcm8 is highly divergent in all Drosophila species and may not provide a good model for Mcm8 in other eukaryotes.

Show MeSH
Related in: MedlinePlus