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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.

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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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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).
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fig1: 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).

Mentions: The early evolution of the eukaryotic lineage remains murky, in large part because the genetic diversity of extant—particularly single-celled—eukaryotes remains unclear (Dawson and Pace, 2002). Indeed, the greatest genetic diversity is seen among microbial (single-celled) eukaryotes (Sogin and Silberman, 1998). However as Pace (2009) pointed out, genome sequence comparisons of living eukaryotes provide “no evidence whatsoever” as to whether the earliest eukaryotes actually had nuclear membranes or NPCs as morphological features. This simple idea, that the first eukaryotic common ancestor (FECA) lacked nuclear morphology, frees one to consider how specific types of proteins in the FECA might have contributed to the subsequent incremental evolution of nuclear structure present in the last common eukaryotic ancestor (LECA; Fig. 1). As discussed in this review, new evidence based on the ancestral nature of endomembrane proteins suggests that the eukaryotic endomembrane system coevolved with, or spawned, the nuclear membranes and NPCs, which appear to have been fully functional in the LECA (Neumann et al., 2010).


Evolution: functional evolution of nuclear structure.

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

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).
© Copyright Policy - openaccess
Related In: Results  -  Collection

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

fig1: 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).
Mentions: The early evolution of the eukaryotic lineage remains murky, in large part because the genetic diversity of extant—particularly single-celled—eukaryotes remains unclear (Dawson and Pace, 2002). Indeed, the greatest genetic diversity is seen among microbial (single-celled) eukaryotes (Sogin and Silberman, 1998). However as Pace (2009) pointed out, genome sequence comparisons of living eukaryotes provide “no evidence whatsoever” as to whether the earliest eukaryotes actually had nuclear membranes or NPCs as morphological features. This simple idea, that the first eukaryotic common ancestor (FECA) lacked nuclear morphology, frees one to consider how specific types of proteins in the FECA might have contributed to the subsequent incremental evolution of nuclear structure present in the last common eukaryotic ancestor (LECA; Fig. 1). As discussed in this review, new evidence based on the ancestral nature of endomembrane proteins suggests that the eukaryotic endomembrane system coevolved with, or spawned, the nuclear membranes and NPCs, which appear to have been fully functional in the LECA (Neumann et al., 2010).

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