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The evolution of the nuclear envelope
Stockholm University, Faculty of Science, Department of Molecular Biology and Functional Genomics. (Anthony Poole)
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The nucleus is one of the defining features of eukaryotes and the question of its origin is intimately linked to the evolution of the eukaryotic cell. It is delimited by a double lipid bilayer called the nuclear envelope, which separates the nuclear interior from the cytoplasm. The inner and outer membranes of the nucleus are continuous with one another creating a single folded envelope, interrupted by nuclear pore complexes (NPCs), which enable transport of proteins and RNA between nucleoplasm and cytoplasm.

A combination of proteomic and bioinformatic analyses has shown that numerous Nups are conserved between yeast and vertebrates. As this only describes a subset of eukaryotic diversity, comparative genomic analyses were used to establish the extent to which the NPC is conserved across the eukaryotic tree. NPCs have been suggested to share a common origin with vesicle coat proteins of the endomembrane system. An additional goal of this work was therefore to establish the distribution of three complexes involved in vesicle transport between organelles of the secretory pathway, called COPI, COPII and Clathrin.

Using profile hidden Markov models in combination with BLAST resulted in identification of nucleoporins and coat protein homologs across all five eukaryotic supergroups for which sequence data is available, indicating both were already present in the Last Eukaryotic Common Ancestor (LECA).Nup homologs were shown to be definitively absent from vestigial nucleomorph nuclei, resultant from secondary endosymbioses, suggesting that Nup genes have either been relocated to the host nuclear genome or that the same set of Nups are used for constructing both the NPC of the main nucleus and nucleomorph.´

We also tested the proposal that transmembrane Nups in vertebrates and yeasts may account for their variant forms of mitosis (‘open’ in vertebrates, ‘closed’ among yeasts). Consistent with this suggestion, the distribution of fungal Pom34 fits a scenario wherein it was integral to the evolution of 'closed’ mitosis in ascomycetes.A unique arrangement for the chromosomes occurs during early meiosis, where the telomeres cluster at the nuclear envelope, forming a distinct ‘bouquet’ arrangement. This forms prior to homolog pairing and recombination in meiosis I. Hypotheses concerning the antiquity of the bouquet were tested by examining the extent of conservation of proteins involved in this stage of meiosis. Distribution appeared patchy, so its presence in LECA could not be unequivocally established and is discussed together with a model aimed at explaining the functional role of the bouquet.

Place, publisher, year, edition, pages
Stockholm: Department of Molecular Biology and Functional Genomics, Stockholm University , 2010. , 58 p.
Keyword [en]
Nuclear pore complex, bouquet, meiosis, nucleus, eukaryote evolution, nucleoporin, tree of life, stem group, recombination
National Category
Biochemistry and Molecular Biology
Research subject
Molecular Biology
Identifiers
URN: urn:nbn:se:su:diva-42259ISBN: 978-91-7155-956-2 (print)OAI: oai:DiVA.org:su-42259DiVA: diva2:345420
Public defence
2010-10-04, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
Opponent
Supervisors
Note
At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 3: Manuscript. Paper 4: manuscript.Available from: 2010-09-12 Created: 2010-08-20 Last updated: 2012-05-24Bibliographically approved
List of papers
1. Comparative Genomic Evidence for a Complete Nuclear Pore Complex in the Last Eukaryotic Common Ancestor
Open this publication in new window or tab >>Comparative Genomic Evidence for a Complete Nuclear Pore Complex in the Last Eukaryotic Common Ancestor
2010 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 5, no 10, e13241- p.Article in journal (Refereed) Published
Abstract [en]

Background: The Nuclear Pore Complex (NPC) facilitates molecular trafficking between nucleus and cytoplasm and is an integral feature of the eukaryote cell. It exhibits eight-fold rotational symmetry and is comprised of approximately 30 nucleoporins (Nups) in different stoichiometries. Nups are broadly conserved between yeast, vertebrates and plants, but few have been identified among other major eukaryotic groups. Methodology/Principal Findings: We screened for Nups across 60 eukaryote genomes and report that 19 Nups (spanning all major protein subcomplexes) are found in all eukaryote supergroups represented in our study (Opisthokonts, Amoebozoa, Viridiplantae, Chromalveolates and Excavates). Based on parsimony, between 23 and 26 of 31 Nups can be placed in LECA. Notably, they include central components of the anchoring system (Ndc1 and Gp210) indicating that the anchoring system did not evolve by convergence, as has previously been suggested. These results significantly extend earlier results and, importantly, unambiguously place a fully-fledged NPC in LECA. We also test the proposal that transmembrane Pom proteins in vertebrates and yeasts may account for their variant forms of mitosis (open mitoses in vertebrates, closed among yeasts). The distribution of homologues of vertebrate Pom121 and yeast Pom152 is not consistent with this suggestion, but the distribution of fungal Pom34 fits a scenario wherein it was integral to the evolution of closed mitosis in ascomycetes. We also report an updated screen for vesicle coating complexes, which share a common evolutionary origin with Nups, and can be traced back to LECA. Surprisingly, we find only three supergroup-level differences (one gain and two losses) between the constituents of COPI, COPII and Clathrin complexes. Conclusions/Significance: Our results indicate that all major protein subcomplexes in the Nuclear Pore Complex are traceable to the Last Eukaryotic Common Ancestor (LECA). In contrast to previous screens, we demonstrate that our conclusions hold regardless of the position of the root of the eukaryote tree.

National Category
Biological Sciences
Research subject
Molecular Biology
Identifiers
urn:nbn:se:su:diva-51744 (URN)10.1371/journal.pone.0013241 (DOI)000282676700015 ()
Note
3Available from: 2011-01-12 Created: 2011-01-12 Last updated: 2017-12-11Bibliographically approved
2. Outsourcing the Nucleus: Nuclear Pore Complex Genes are no Longer Encoded in Nucleomorph Genomes
Open this publication in new window or tab >>Outsourcing the Nucleus: Nuclear Pore Complex Genes are no Longer Encoded in Nucleomorph Genomes
2006 (English)In: Evolutionary Bioinformatics, ISSN 1176-9343, E-ISSN 1176-9343, Vol. 2, 23-34 p.Article in journal (Refereed) Published
Abstract [en]

The nuclear pore complex (NPC) facilitates transport between nucleus and cytoplasm. The protein constituents of the NPC, termed nucleoporins (Nups), are conserved across a wide diversity of eukaryotes. In apparent exception to this, no nucleoporin genes have been identified in nucleomorph genomes. Nucleomorphs, nuclear remnants of once free-living eukaryotes, took up residence as secondary endosymbionts in cryptomonad and chlorarachniophyte algae. As these genomes are highly reduced, Nup genes may have been lost, or relocated to the host nucleus. However, Nup genes are often poorly conserved between species, so absence may be an artifact of low sequence similarity. We therefore constructed an evolutionary bioinformatic screen to establish whether the apparent absence of Nup genes in nucleomorph genomes is due to genuine absence or the inability of current methods to detect homologues. We searched green plant (Arabidopsis and rice), green alga (Chlamydomonas reinhardtii) and red alga (Cyanidioschyzon merolae) genomes, plus two nucleomorph genomes (Bigelowiella natans and Guillardia theta) with profile hidden Markov models (HMMs) from curated alignments of known vertebrate/yeast Nups. Since the plant, algal and nucleomorph genomes all belong to the kingdom Plantae, and are evolutionarily distant from the outgroup (vertebrate/yeast) training set, we use the plant and algal genomes as internal positive controls for the sensitivity of the searches in nucleomorph genomes. We find numerous Nup homologues in all plant and free-living algal species, but none in either nucleomorph genome. BLAST searches using identified plant and algal Nups also failed to detect nucleomorph homologues. We conclude that nucleomorph Nup genes have either been lost, being replaced by host Nup genes, or, that nucleomorph Nup genes have been transferred to the host nucleus twice independently; once in the evolution of the red algal nucleomorph and once in the green algal nucleomorph.

Keyword
nuclear pore complex, nucleomorph, nucleoporin, reductive evolution, gene loss
National Category
Biological Sciences
Research subject
Molecular Biology
Identifiers
urn:nbn:se:su:diva-14135 (URN)
Available from: 2008-06-13 Created: 2008-06-13 Last updated: 2017-12-13Bibliographically approved
3. Is the bouquet arrangement in meiosis an ancient solution to the hotspot conversion paradox?
Open this publication in new window or tab >>Is the bouquet arrangement in meiosis an ancient solution to the hotspot conversion paradox?
(English)Manuscript (preprint) (Other academic)
Keyword
Bouquet, meiosis, recombination, hotspot conversion paradox, LECA, evolution, telomere
Identifiers
urn:nbn:se:su:diva-42632 (URN)
Available from: 2010-09-10 Created: 2010-09-10 Last updated: 2010-09-13Bibliographically approved
4. Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis
Open this publication in new window or tab >>Reconciling an archaeal origin of eukaryotes with engulfment: a biologically plausible update of the Eocyte hypothesis
2011 (English)In: Research in Microbiology, ISSN 0923-2508, E-ISSN 1769-7123, Vol. 162, no 1, 71-76 p.Article in journal (Refereed) Published
Abstract [en]

An archaeal origin of eukaryotes is often equated with the engulfment of the bacterial ancestor of mitochondria by an archaeon. Such an event is problematic in that it is not supported by archaeal cell biology. We show that placing phylogenetic results within a stem-and-crown framework eliminates such incompatibilities, and that an archaeal origin for eukaryotes (as suggested from recent phylogenies) can be uncontroversially reconciled with phagocytosis as the mechanism for engulfment of the mitochondrial ancestor. This is significant because it eliminates a perceived problem with eukaryote origins: that an archaeal origin of eukaryotes (as under the Eocyte hypothesis) cannot be reconciled with existing cell biological mechanisms through which bacteria may take up residence inside eukaryote cells.

Keyword
Stem group, Crown group, Eocyte hypothesis, Phagocytosis, Eukaryotes, Archaea
National Category
Biological Sciences
Research subject
Molecular Biology
Identifiers
urn:nbn:se:su:diva-68644 (URN)10.1016/j.resmic.2010.10.002 (DOI)000289500000008 ()
Note

2

Available from: 2012-01-07 Created: 2012-01-04 Last updated: 2017-12-08Bibliographically approved

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