Origin of the cell nucleus,mitosis and sex: roles of intracellular coevolution

Background  

The transition from prokaryotes to eukaryotes was the most radical change in cell organisation since life began, with the largest ever burst of gene duplication and novelty. According to the coevolutionary theory of eukaryote origins, the fundamental innovations were the concerted origins of the endomembrane system and cytoskeleton, subsequently recruited to form the cell nucleus and coevolving mitotic apparatus, with numerous genetic eukaryotic novelties inevitable consequences of this compartmentation and novel DNA segregation mechanism. Physical and mutational mechanisms of origin of the nucleus are seldom considered beyond the long-standing assumption that it involved wrapping pre-existing endomembranes around chromatin. Discussions on the origin of sex typically overlook its association with protozoan entry into dormant walled cysts and the likely simultaneous coevolutionary, not sequential, origin of mitosis and meiosis.     

Origin of the nucleus and Ran-dependent transport to safeguard ribosome biogenesis in a chimeric cell

Background  

The origin of the nucleus is a central problem about the origin of eukaryotes. The common ancestry of nuclear pore complexes (NPC) and vesicle coating complexes indicates that the nucleus evolved via the modification of a pre-existing endomembrane system. Such an autogenous scenario is cell biologically feasible, but it is not clear what were the selective or neutral mechanisms that had led to the origin of the nuclear compartment.     

Assembly of the cell nucleus

Purified DNA can be assembled into structures that closely resemble cell nuclei. The cell-free systems that allow this can be exploited to study assembly pathways for several components of the nucleus. They also offer great opportunities for the experimental analysis of nuclear function.     

Mononucleotides of the cell nucleus

1. It has been demonstrated by ion exchange chromatography that the cell nucleus contains mononucleotides of adenine, guanine, cytosine, uracil, together with diphosphopyridine nucleotide, and several uridine diphosphate derivatives; the adenine nucleotides predominating in amount. Nucleotide components in the cell nucleus are in close agreement both quantitatively and qualitatively with those found in the cytoplasm. 2. In calf thymus sucrose nuclei, nucleotide monophosphates can be phosphorylated to the energy-rich triphosphate form without participation of cytoplasmic components. As to the nature of the phosphorylation, it has been shown that there exist certain differences as well as resemblances between nuclei and mitochondria. A distinctive feature of nuclear phosphorylation is that only intranuclear monophosphates seem to be phosphorylated. The process is completely inhibited by cyanide, azide, and dinitrophenol. However, certain reagents which block oxidative phosphorylation of mitochondria, namely dicumarol, Janus green B, methylene blue, and calcium ions, have no effect on phosphorylation within the nucleus. 3. The bulk of mononucleotides is preserved within thymus nuclei after their isolation in sucrose. Nucleotides are surprisingly well retained by nuclei in a sucrose medium whether or not electrolytes are present and in buffers ranging from pH 3 to 10; under all conditions sucrose is required for retention. 4. Dilute acetate in sucrose releases nucleotides from the nucleus below pH 5.1. As to the effective pH of acetate, there is a sharp boundary between pH 5.1 and pH 5.9. At pH 5.9, and above, acetate does not remove nucleotides from the nucleus. The effects of propionate, formate, and monochloroacetate on the nuclei are the same as that of acetate. 5. When nuclei are exposed to a wide variety of conditions a close correlation is found between the retention in the nucleus of nucleotides and of potassium. This suggests that both substances are part of a common complex in the cell nucleus. 6. It has been shown that upon removal of nucleotides and potassium from calf thymus sucrose nuclei by acetate, the ability to incorporate C¹⁴-alanine into nuclear protein is greatly impaired.     

Dynamic organization of the cell nucleus

The dynamic organization of the cell nucleus into subcompartments with distinct biological activities represents an important regulatory layer for cell function. Recent studies provide new insights into the principles, by which nuclear organelles form. This process frequently occurs in a self-organizing manner leading to the assembly of stable but plastic structures from multiple relatively weak interaction forces. These can rearrange into different functional states in response to specific modifications of the constituting components or changes in the nuclear environment.     

Viscoelastic properties of the cell nucleus

Mechanical factors play an important role in the regulation of cell physiology. One pathway by which mechanical stress may influence gene expression is through a direct physical connection from the extracellular matrix across the plasma membrane and to the nucleus. However, little is known of the mechanical properties or deformation behavior of the nucleus. The goal of this study was to quantify the viscoelastic properties of mechanically and chemically isolated nuclei of articular chondrocytes using micropipet aspiration in conjunction theoretical viscoelastic model. Isolated nuclei behaved as viscoelastic solid materials similar to the cytoplasm, but were 3-4 times stiffer and nearly twice as viscous as the cytoplasm. Quantitative information of the biophysical properties and deformation behavior of the nucleus may provide further insight on the relationships between the stress-strain state of the nucleus and that of the extracellular matrix, as well as potential mechanisms of mechanical signal transduction.     

Origin of the eukaryotic nucleus: eukaryotes and eocytes are genotypically related

The origin of the eukaryotic nucleus is difficult to reconstruct. While eukaryotic organelles (chloroplast, mitochondrion) are eubacterial endosymbionts, the source of nuclear genes has been obscured by multiple nucleotide substitutions. Using evolutionary parsimony, a newly developed rate-invariant treeing algorithm, the eukaryotic rRNA genes are shown to have evolved from the eocytes, a group of extremely thermophilic, sulfur-metabolizing, anucleate cells. The deepest bifurcation yet found separates the reconstructed tree into two taxonomic divisions. These are a proto-eukaryotic group (karyotes) and an essentially bacterial one (parkaryotes). Within the precision of the rooting procedure, the tree is not consistent with either the prokaryotic--eukaryotic or the archaebacterial--eubacterial--eukaryotic groupings. It implies that the last common ancestor of extant life, and the early ancestors of eukaryotes, very likely lacked nuclei, metabolized sulfur, and lived at near boiling temperatures.     

Atomic force microscopy of the cell nucleus

In mammals and plants, the cell nucleus is organized in dynamic macromolecular domains involved in DNA and RNA metabolism. These domains can be visualized by light and electron microscopy and their composition analyzed by using several cytochemical approaches. They are composed of chromatin or ribonucleoprotein structures as interchromatin and perichromatin fibers and granules, coiled bodies, and nuclear bodies. In plants, DNA arrangement defines chromocentric and reticulated nuclei. We used atomic force microscopy to study the in situ structure of the plant cell nucleus. Samples of the plants Lacandonia schismatica and Ginkgo biloba were prepared as for electron microscopy and unstained semithin sections were mounted on glass slides. For comparison, we also examined entire normal rat kidney cells using the same approach. Samples were scanned with an atomic force microscope working in contact mode. Recognizable images of the nuclear envelope, pores, chromatin, and nucleolus were observed. Reticulated chromatin was observed in L. schismatica. Different textures in the nucleolus of G. biloba were also observed, suggesting the presence of nucleolar subcompartments. The observation of nuclear structure in situ with the atomic force microscope offers a new approach for the analysis of this organelle at high resolution.     

The dynamic landscape of the cell nucleus

While the cell nucleus was described for the first time almost two centuries ago, our modern view of the nuclear architecture is primarily based on studies from the last two decades. This surprising late start coincides with the development of new, powerful strategies to probe for the spatial organization of nuclear activities in both fixed and live cells. As a result, three major principles have emerged: first, the nucleus is not just a bag filled with nucleic acids and proteins. Rather, many distinct functional domains, including the chromosomes, resides within the confines of the nuclear envelope. Second, all these nuclear domains are highly dynamic, with molecules exchanging rapidly between them and the surrounding nucleoplasm. Finally, the motion of molecules within the nucleoplasm appears to be mostly driven by random diffusion. Here, the emerging roles of several subnuclear domains are discussed in the context of the dynamic functions of the cell nucleus. Mol. Reprod. Dev. 77: 19–28, 2010. © 2009 Wiley‐Liss, Inc.