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Evolution: functional evolution of nuclear structure.

Wilson KL, Dawson SC - J. Cell Biol. (2011)

Bottom Line: Recent studies have identified many components of the nuclear envelope in living Opisthokonts, the eukaryotic supergroup that includes fungi and metazoan animals.These components include diverse chromatin-binding membrane proteins, and membrane proteins with adhesive lumenal domains that may have contributed to the evolution of nuclear membrane architecture.Further discoveries about the nucleoskeleton suggest that the evolution of nuclear structure was tightly coupled to genome partitioning during mitosis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. klwilson@jhmi.edu

ABSTRACT
The evolution of the nucleus, the defining feature of eukaryotic cells, was long shrouded in speculation and mystery. There is now strong evidence that nuclear pore complexes (NPCs) and nuclear membranes coevolved with the endomembrane system, and that the last eukaryotic common ancestor (LECA) had fully functional NPCs. Recent studies have identified many components of the nuclear envelope in living Opisthokonts, the eukaryotic supergroup that includes fungi and metazoan animals. These components include diverse chromatin-binding membrane proteins, and membrane proteins with adhesive lumenal domains that may have contributed to the evolution of nuclear membrane architecture. Further discoveries about the nucleoskeleton suggest that the evolution of nuclear structure was tightly coupled to genome partitioning during mitosis.

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Identifying nuclear membrane proteins in diverse eukaryotes. Representatives of five eukaryotic supergroup lineages, queried by BLAST search for potential conservation of open reading frames (ORFs) related to Opisthokont nuclear membrane proteins. Chart indicates whether an ORF(s) homologous to each queried polypeptide was detected (+) or not detected (−) in completed genomes of representative supergroup lineages (Opisthokonts, Amoebozoa, Archaeplastida, Chromalveolates, and Excavates) in GenBank using reciprocal BLAST with e-values > 0.01, as detailed in Table I. ORFs homologous to LUMA and nurim are also present in various bacterial lineages (not depicted). The specific evolutionary relationships between each supergroup and the last eukaryotic common ancestor (LECA) are controversial, as reflected by the lack of specific branching order between these groups. However, the detection of a nuclear-associated homologue (e.g., SUN domain, or LUMA) in more than two supergroups might suggest the homologue was present in the LECA. Negative results are not definitive; for example, we did not recover the S. cerevisiae LEM (“HEH”) domain protein Src1 (see next page). The species M. brevicollis and C. owczarsaki represent the Protist lineage within Opisthokonts and are distantly related to Fungi and Animals.
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fig3: Identifying nuclear membrane proteins in diverse eukaryotes. Representatives of five eukaryotic supergroup lineages, queried by BLAST search for potential conservation of open reading frames (ORFs) related to Opisthokont nuclear membrane proteins. Chart indicates whether an ORF(s) homologous to each queried polypeptide was detected (+) or not detected (−) in completed genomes of representative supergroup lineages (Opisthokonts, Amoebozoa, Archaeplastida, Chromalveolates, and Excavates) in GenBank using reciprocal BLAST with e-values > 0.01, as detailed in Table I. ORFs homologous to LUMA and nurim are also present in various bacterial lineages (not depicted). The specific evolutionary relationships between each supergroup and the last eukaryotic common ancestor (LECA) are controversial, as reflected by the lack of specific branching order between these groups. However, the detection of a nuclear-associated homologue (e.g., SUN domain, or LUMA) in more than two supergroups might suggest the homologue was present in the LECA. Negative results are not definitive; for example, we did not recover the S. cerevisiae LEM (“HEH”) domain protein Src1 (see next page). The species M. brevicollis and C. owczarsaki represent the Protist lineage within Opisthokonts and are distantly related to Fungi and Animals.

Mentions: Proposed incremental transition from FECA (no nuclear structure) to LECA (nucleus). The first eukaryotic common ancestor (FECA) is proposed to have lacked nuclear structure. Partitioning of the duplicated genome (yellow/orange) is proposed to be mediated by the polymerization of protein(s) related to bacterial par “motors” (blue; e.g., actin; ATPase; tubulin; DNA-binding coiled-coil protein), bound to centromere proteins (red squares). Over significant time, the FECA is proposed to have given rise to the last eukaryotic common ancestor (LECA), a cell with fully functional NPCs (not depicted) and endomembranes (Neumann et al., 2010) and, we suggest, a nucleoskeleton that included components involved in genome partitioning. After the LECA, further evolution of nuclear structure followed different pathways as seen in the six living eukaryotic supergroups (Hampl et al., 2009; see Fig. 3).


Evolution: functional evolution of nuclear structure.

Wilson KL, Dawson SC - J. Cell Biol. (2011)

Identifying nuclear membrane proteins in diverse eukaryotes. Representatives of five eukaryotic supergroup lineages, queried by BLAST search for potential conservation of open reading frames (ORFs) related to Opisthokont nuclear membrane proteins. Chart indicates whether an ORF(s) homologous to each queried polypeptide was detected (+) or not detected (−) in completed genomes of representative supergroup lineages (Opisthokonts, Amoebozoa, Archaeplastida, Chromalveolates, and Excavates) in GenBank using reciprocal BLAST with e-values > 0.01, as detailed in Table I. ORFs homologous to LUMA and nurim are also present in various bacterial lineages (not depicted). The specific evolutionary relationships between each supergroup and the last eukaryotic common ancestor (LECA) are controversial, as reflected by the lack of specific branching order between these groups. However, the detection of a nuclear-associated homologue (e.g., SUN domain, or LUMA) in more than two supergroups might suggest the homologue was present in the LECA. Negative results are not definitive; for example, we did not recover the S. cerevisiae LEM (“HEH”) domain protein Src1 (see next page). The species M. brevicollis and C. owczarsaki represent the Protist lineage within Opisthokonts and are distantly related to Fungi and Animals.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3198171&req=5

fig3: Identifying nuclear membrane proteins in diverse eukaryotes. Representatives of five eukaryotic supergroup lineages, queried by BLAST search for potential conservation of open reading frames (ORFs) related to Opisthokont nuclear membrane proteins. Chart indicates whether an ORF(s) homologous to each queried polypeptide was detected (+) or not detected (−) in completed genomes of representative supergroup lineages (Opisthokonts, Amoebozoa, Archaeplastida, Chromalveolates, and Excavates) in GenBank using reciprocal BLAST with e-values > 0.01, as detailed in Table I. ORFs homologous to LUMA and nurim are also present in various bacterial lineages (not depicted). The specific evolutionary relationships between each supergroup and the last eukaryotic common ancestor (LECA) are controversial, as reflected by the lack of specific branching order between these groups. However, the detection of a nuclear-associated homologue (e.g., SUN domain, or LUMA) in more than two supergroups might suggest the homologue was present in the LECA. Negative results are not definitive; for example, we did not recover the S. cerevisiae LEM (“HEH”) domain protein Src1 (see next page). The species M. brevicollis and C. owczarsaki represent the Protist lineage within Opisthokonts and are distantly related to Fungi and Animals.
Mentions: Proposed incremental transition from FECA (no nuclear structure) to LECA (nucleus). The first eukaryotic common ancestor (FECA) is proposed to have lacked nuclear structure. Partitioning of the duplicated genome (yellow/orange) is proposed to be mediated by the polymerization of protein(s) related to bacterial par “motors” (blue; e.g., actin; ATPase; tubulin; DNA-binding coiled-coil protein), bound to centromere proteins (red squares). Over significant time, the FECA is proposed to have given rise to the last eukaryotic common ancestor (LECA), a cell with fully functional NPCs (not depicted) and endomembranes (Neumann et al., 2010) and, we suggest, a nucleoskeleton that included components involved in genome partitioning. After the LECA, further evolution of nuclear structure followed different pathways as seen in the six living eukaryotic supergroups (Hampl et al., 2009; see Fig. 3).

Bottom Line: Recent studies have identified many components of the nuclear envelope in living Opisthokonts, the eukaryotic supergroup that includes fungi and metazoan animals.These components include diverse chromatin-binding membrane proteins, and membrane proteins with adhesive lumenal domains that may have contributed to the evolution of nuclear membrane architecture.Further discoveries about the nucleoskeleton suggest that the evolution of nuclear structure was tightly coupled to genome partitioning during mitosis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. klwilson@jhmi.edu

ABSTRACT
The evolution of the nucleus, the defining feature of eukaryotic cells, was long shrouded in speculation and mystery. There is now strong evidence that nuclear pore complexes (NPCs) and nuclear membranes coevolved with the endomembrane system, and that the last eukaryotic common ancestor (LECA) had fully functional NPCs. Recent studies have identified many components of the nuclear envelope in living Opisthokonts, the eukaryotic supergroup that includes fungi and metazoan animals. These components include diverse chromatin-binding membrane proteins, and membrane proteins with adhesive lumenal domains that may have contributed to the evolution of nuclear membrane architecture. Further discoveries about the nucleoskeleton suggest that the evolution of nuclear structure was tightly coupled to genome partitioning during mitosis.

Show MeSH
Related in: MedlinePlus