Evolution and diversification of the nuclear envelope

Abstract

Eukaryotic cells arose ~1.5 billion years ago, with the endomembrane system a central feature, facilitating evolution of intracellular compartments. Endomembranes include the nuclear envelope (NE) dividing the cytoplasm and nucleoplasm. The NE possesses universal features: a double lipid bilayer membrane, nuclear pore complexes (NPCs), and continuity with the endoplasmic reticulum, indicating common evolutionary origin. However, levels of specialization between lineages remains unclear, despite distinct mechanisms underpinning various nuclear activities. Several distinct modes of molecular evolution facilitate organellar diversification and to understand which apply to the NE, we exploited proteomic datasets of purified nuclear envelopes from model systems for comparative analysis. We find enrichment of core nuclear functions amongst the widely conserved proteins to be less numerous than lineage-specific cohorts, but enriched in core nuclear functions. This, together with consideration of additional evidence, suggests that, despite a common origin, the NE has evolved as a highly diverse organelle with significant lineage-specific functionality.

Evolution and diversification of the nuclear pore complex

“…Paradoxically ELYS is present in most taxa, except excavates or TSAR, suggesting a probable ancient origin [12,[17][18][19][20][21]. As neither plants nor fungi share a lamina with metazoa, ELYS functions are unclear [33,34]. Even more unusual is that the S. pombe ELYS ortholog is located on the cytoplasmic side of the NPC, potentially precluding obvious nucleoplasmic roles [13].…”

Editorial for the SEB 2020 special issue ‘dynamic organisation of the nucleus across kingdoms’

“…Understanding the origins of the structural components of the nucleus underpins many of our efforts to advance understanding of mechanisms and function. This collection of papers provides significant insights -both across kingdoms [3] and in detailed reviews of the current state of knowledge in higher plants [4,5]. One of the fascinations of studying the dynamic structure of the nucleus is the way in which a range of conserved functions are carried out by such a diversity of lineage-specific components.…”

“…While a small number of highly conserved proteins point back to their presence in the Last Eukaryotic Common Ancestor, many show a surprising diversification and even functionally conserved proteins show a wide range of structural characteristics. Indeed, from this collection of papers, the reader can only wonder whether the statement of Padilla-Meija et al [3] that 'findings suggest a rather surprising level of divergence associated with a structure that, in a very real sense, defines the eukaryotic cell' is, in fact, an understatement.…”

“…While recognizing the limitations imposed by the challenges of defining the nuclear proteome, Padilla-Meija and coworkers [3] provide detailed comparative insights into its evolution using carefully selected data from protozoans to mammals. Through a comparative analysis of previously described datasets from model systems and by expansion of this data, for instance, by searching using queries from Trypanosoma brucei, they provide a valuable coverage of nuclear constituents, structure and function, providing insights and a data set of great value for further exploration.…”

Cell, Time and Knowledge: Some Conjectures

“…Based on cell-theory [1][2][3][4][5], today we know that life is generated from preexisting life, i.e. the basic unit of life that is a cell originates from another cell [6], this process is called the cell cycle and consists of several phases [7,8] (i) DNA synthesis and replication or data transfer; (ii) cell division, here the already duplicated DNA molecules separate to original nuclei, the nuclei have identical genetic content to the original cell and (iii) fi nally, cytokinesis where reorganisation of the cell membrane occurs in the new nuclei forming the new cells. These phases are more complex and give rise to multiple additional processes that we will not mention here because this analysis is not about molecular biology.…”