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Peer-reviewed

Enquiry Article

Comparative Genomic Evidence for a Complete Nuclear Pore Complex in the Last Eukaryotic Common Ancestor

• Nadja Neumann,
• Daniel Lundin,
• Anthony Grand. Poole

x

• Published: October viii, 2022
• https://doi.org/10.1371/periodical.pone.0013241

Figures

Abstract

Groundwork

The Nuclear Pore Complex (NPC) facilitates molecular trafficking between nucleus and cytoplasm and is an integral feature of the eukaryote cell. It exhibits viii-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 nineteen Nups (spanning all major protein subcomplexes) are constitute 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 key 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 examination the proposal that transmembrane Pom proteins in vertebrates and yeasts may business relationship for their variant forms of mitosis (open up mitoses in vertebrates, airtight among yeasts). The distribution of homologues of vertebrate Pom121 and yeast Pom152 is not consistent with this suggestion, only the distribution of fungal Pom34 fits a scenario wherein information technology was integral to the evolution of closed mitosis in ascomycetes. Nosotros also written 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 but three supergroup-level differences (one gain and two losses) betwixt 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 agree regardless of the position of the root of the eukaryote tree.

Citation: Neumann N, Lundin D, Poole AM (2010) Comparative Genomic Evidence for a Complete Nuclear Pore Circuitous in the Last Eukaryotic Common Antecedent. PLoS ONE 5(10): e13241. https://doi.org/10.1371/journal.pone.0013241

Editor: Cecile Fairhead, Institut de Genetique et Microbiologie, France

Received: March 9, 2022; Accepted: September 15, 2022; Published: October 8, 2022

Copyright: © 2022 Neumann et al. This is an open up-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in whatever medium, provided the original writer and source are credited.

Funding: Financial support from the Carl Tryggers Foundation (CTS04:329 www.carltryggersstiftelse.se) to AMP is gratefully best-selling. AMP is a Royal Swedish Academy of Sciences (world wide web.kva.se) Research Fellow supported by a grant from the Knut and Alice Wallenberg Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Nuclear pore complexes (NPCs) mediate molecular trafficking betwixt nucleus and cytoplasm [i], [ii]. They are composed of ∼xxx different proteins, called nucleoporins (Nups), that are nowadays in multiple copies in each pore [3], [4], [5]. Most Nups are constituents of specific sub-complexes, which form the major structural units of the pore: cytoplasmic fibrils, central cadre and the nuclear basket (Figure 1a) [6], [7].

Figure 1. NPC structure, composition and Nup conservation beyond eukaryotes.

a) Schematic section through the nuclear pore circuitous. Sub-complexes are indicated as boxes and marked in dissimilar colors to bespeak their position in the pore. b) The tabular array summarizes Nup distribution across eukaryotic super-groups. Color-coding matches that of the subcomplexes in (a). Nucleoporins indicated with bold letters are universally distributed beyond eukaryotes, equally judged past presence in at to the lowest degree one genome from each of the v supergroups.

https://doi.org/10.1371/journal.pone.0013241.g001

The majority of Nups are conserved between mammals and yeasts [3], [4], [7], [viii] and previous genomic studies demonstrate extensive conservation of the NPC also in plants and eukaryotic algae [nine], [x], [11].

The extent of conservation of NPC components outside these groups appears patchy withal [ten], [11]. Equally Mans et al. [10] acknowledged, this makes it difficult to unambiguously establish the complication of the NPC in the Last Eukaryotic Common Ancestor (LECA), since inferences are dependent upon the position of the root of the eukaryote tree. Bapteste et al. [eleven], reporting a comparable distribution of Nups to Mans et al., noted furthermore that proteins involved in anchoring the NPC to the nuclear envelope were express in their distribution. On the basis of this ascertainment, Bapteste et al. ended that the NPC anchoring system appears to have evolved multiple times independently.

This conclusion is moreover interesting in light of the recent suggestion that the yeast-specific transmembrane Nups Pom152 and Pom34 may be intimately linked to the evolution of closed mitosis in yeast [12]. Closed mitosis is not restricted to yeasts, as it is also observed in a range of protists [13], [14]. This raises the question as to whether the evolutionary lability of the anchoring system broadly correlates with the evolution of closed mitosis.

In the wider context of eukaryote origins, there is great value in the identification of Nup homologues in either archaea or bacteria, since this may shed light on the evolutionary origins of the nucleus. If Nups display similarity to proteins from either or both of these domains, the role of these proteins may provide new insights into the evolutionary emergence of cardinal protein families or folds [10]. In this respect there has also been considerable interest in the nuclear envelope-like internal membranes observed in planctomycete bacteria [fifteen], [16], and whether the putative pores identified from morphological data are constructed from poly peptide components with similarity to eukaryote Nups. To appointment, no homologs to Nups have been identified in the genome of any planctomycete.

An alternative hypothesis, in principle compatible with several theories on eukaryote origins, is that the nucleus evolved autogenously in the eukaryote stem lineage [17], [xviii]. The protocoatomer hypothesis [xviii] in particular addresses the evolution of the NPC in item. In brief, this model posits that the NPC and vesicle-coating complexes evolved from a rudimentary membrane-bending apparatus that generated internal construction through invagination. Devos et al.[18] reported that an NPC subcomplex (yeast Nup84/vertebrate Nup107-160) bears a hit resemblance to vesicle-coating complexes, both containing proteins with a unique β-propeller/α-solenoid architecture. Moreover, Sec13 is a component of both the NPC and the COPII vesicle-coating complex [xix], [twenty]. Mans et al. [10] likewise noted similarities between NPC and vesicle-coating complex components, coming to a similar conclusion on the basis of sequence analyses.

Rapid progress in eukaryote genome sequence projects provides an ideal opportunity to revisit these questions with the benefit of a more comprehensive dataset. We report here the results of a screen covering lx eukaryote genomes (representing five supergroups) with the aim of examining the extent to which protein subcomplexes that comprise the NPC are conserved across eukaryotes. We have as well examined whether coatomer proteins from the COPI, COPII and clathrin complexes are as broadly conserved as NPC complex proteins, since an early on common origin for both the NPC and vesicle coating complexes predicts this. Our results provide further back up for a complete NPC in LECA and, in contrast to before studies, we show that this conclusion holds regardless of the position of the eukaryote root. We conclude that at to the lowest degree 23 and possibly equally many as 26 nucleoporins, including key components of the anchoring arrangement, were already present in LECA. We also report that the distribution of Pom34, merely not Pom152, correlates with the occurrence of closed mitosis among fungi. Despite all-encompassing searches, our screen did not recover clear Nup homologs in either bacterial or archaeal genomes, consistent with the view that the nuclear pore complex evolved within the eukaryote stem, after the deviation of archaea and eukaryotes.

Results and Discussion

Establishing the accuracy of HMMer-based identification of Nucleoporins

In silico gene notation past sequence similarity is expected to be discipline to a significant degree of error (and maybe subjectivity), and in the current example is also complicated by the dandy evolutionary distances spanning the eukaryote tree. The contempo publication of nucleoporins identified in Trypanosoma brucei using experimental proteomics and structure prediction approaches [32], provided the states with a fortuitous internal command past which to exam the accurateness of our in silico screens for eukaryote Nup homologs. As we had already completed our screen of T. brucei when the DeGrasse et al. study [32] was published, we were able to utilise the identified Nups reported therein equally a bullheaded control, in the spirit of CASP and CAPRI community experiments to examination ab initio 3D protein structure and protein-protein docking prediction methods (reviewed in [33], [34]). Comparing of the candidates identified using our HMMer-based approach with the results reported by DeGrasse et al. is particularly useful in that T. brucei is an outgroup to all sequences included in our grooming dataset. Table 1 compares our predictions with those experimentally shown to be NPC components in T. brucei. Equally is evident from Table 1, our predictions accurately identified homologs for x/ten Nups where DeGrasse et al. concluded orthology could be established. In our assay, we predicted a Seh1 candidate not identified by DeGrasse et al., which could potentially be a fake positive identification. Careful examination of the full Seh1 alignment (see supplementary file SI4) reveals that all sequence identities are contained inside the half dozen WD-echo regions (though nosotros note considerable sequence complexity within these regions, and clear motifs for WD repeats one and 3). Seh1 and Sec13 sequences tin can be difficult to distinguish, though, for T. brucei, DeGrasse et al. and our analyses independently identified the aforementioned Sec13 candidate. While absenteeism of Seh1 sequence identities outside of the WD-repeat regions warrants caution, we were unable to place any other candidate sequences with this same repeat compages, suggesting this sequence may well be a Seh1 candidate, albeit a weak one. It is also worth noting that Seh1 is known non to exist strongly associated with the Nup107-160 circuitous, which may explain its absence from proteomics data. DeGrasse et al. also identified an additional 13 proteins, seven of which comport FG repeats. It is to be expected that comparative approaches volition tend to underestimate the components of any given complex, since the approach is dependent upon the starting dataset. Moreover, every bit FG-echo proteins oftentimes behave no other distinguishing features, we deemed the presence of FG-repeats alone insufficient for assigning membership to the NPC, and such candidates were excluded from our written report (Tabular array one). From the perspective of the current study, the results bespeak that the HMMer-based arroyo used here is conservative merely accurate, as no incorrect assignments were made in our control screen of T. brucei.

Components from all NPC subcomplexes are nowadays in LECA

The results of our full screen for Nups are summarised in Figure ane, with species-level particular given in Tabular array 2 (accession numbers for candidates are given in supplementary Table S1). We report that homologs for nineteen of 31 Nups are found in all five supergroups (Fig. i), significantly extending the findings of previous studies, which were based on the analysis of fewer genomes [10], [xi].

The broadest conservation is establish in plants where nosotros detect 26 candidates, suggesting that the cadre composition of nuclear pore complexes in green plants is highly similar to that seen amidst opisthokonts. The only genome within the Plantae for which no Nups were recovered is the nucleomorph genome of Hemiselmis andersenii, which derives from a red algal endosymbiont [35], [36]. This result mirrors previous results indicating that the nucleomorph genomes of Guillardia theta and Bigelowiella natans are devoid of nucleoporin genes, suggesting that all nucleoporin genes are coded in the main nucleus instead [9]. That all available nucleomorph genomes lack obvious nucleoporin homologs suggests little hindrance to relocation or replacement of nucleoporin genes in these lineages.

Candidate nucleoporins were also readily identified in Amoebozoa (22), Chromalveolates (25) and Excavates (23) (Effigy i, Table 2), with nucleoporins from all key subcomplexes and substructures (cytoplasmic fibrils, scaffold, anchoring organisation, nuclear ring, central channel and nuclear basket) being detected in members of all supergroups.

In previous studies, the conclusion that the LECA possessed a NPC was complicated past the patchy distribution of some nucleoporins, with but nine nucleoporins constitute in any of the supergroups other than Plantae and Opisthokonts [11] [10]. Consequently, the ability to assign a circuitous NPC to LECA differed depending upon the topology of the eukaryote tree; where Excavates were basal (come across [37]), only 7 nucleoporins could be placed in LECA [10]. If the root was placed between unikonts and bikonts [38], [39], 23 Nups could be traced dorsum to LECA, largely on account of candidates identified in plants [ten], [11]. As shown in Table 3, our broad screen significantly expands the extent to which Nup homologues can be identified across the eukaryote tree. Our results increase the number of Nup candidates beyond all eukaryote supergroups where genome data are bachelor (except Opisthokonts, where a total complement had already been characterised in advance of all iii studies). Of particular note, we significantly expand the number of candidates in iii eukaryote supergroups where genome sequence data is still limited (Amoebozoa, Chromalveolates and Excavates). For these supergroups our screen expands the full number of candidate Nups from fewer than 10 in each supergroup to 22 in Amoebozoa 25 in Chromalveolates and 23 in Excavates (Tabular array 3).

The identification of and then many new Nup candidates beyond Amoebozoa, Chromalveolates and Excavates is meaning because it enables us to trace a complex NPC back to LECA regardless of ongoing dubiety about the position of the root of the eukaryote tree (Figure ii), thereby providing robust evidence for the early on evolutionary origin of the NPC in the eukaryote lineage independently of tree topology. By contrast, previous studies could only unambiguously identify a complex NPC in the common ancestor of Opisthokonts and the Plantae. Under the unikont/bikont rooting (Figure 2, right tree), we tin trace 26 nucleoporins back to LECA (Fig 2), with 4 gains in the Opisthokonts. Of these, three are clearly lineage-specific gains: Pom121 is restricted to vertebrates, while Pom34 and Pom152 are establish only in fungi. Nup37 is institute in metazoa and some ascomycetes, suggesting either that we have failed to observe all orthologs, or that this Nup has been bailiwick to a series of losses in the Opisthokonts — the recent identification of a Nup37 homolog in Aspergillus nidulans [40] confirms these ascomycete candidates are not spurious predictions.

Figure 2. NPC components are traceable to LECA.

NPC pore composition in LECA based on two alternative rootings of the eukaryote tree. In the left hand tree, Excavates are the outgroup. The right mitt tree is rooted on the ground of the unikont/bikont bifurcation. Gains (+) and losses (–) in different lineages are indicated under each scenario. Where gains and losses are equally probable, these are marked with (?).

https://doi.org/10.1371/journal.pone.0013241.g002

It is as well interesting that Amoebozoa appear from Effigy two to accept lost a number of Nups. Withal losses (as indicated on both trees in Figure two) should be treated with caution in that information technology is difficult to distinguish between genuine loss and missing data. In this context, it will be interesting to analyse genome information from the anaerobic amoebozoan, Breviata abomination, which is proposed to represent a deep-branching member of this supergroup [41], [42].

A cursory examination of Table 2 indicates that we accept had only limited success in finding Nup candidates amid some parasitic lineages, and observations supporting morphologically complex nuclear pores amidst excavates [32], [43], underscore the necessarily bourgeois nature of comparative genomic analyses. That aside, the information however provide a clear indication that LECA possessed betwixt 23 and 26 Nups. Given ongoing uncertainty apropos the structure of the eukaryote tree [42], [44], nosotros note that, assuming the genomes screened in the present study are correctly placed in the proposed five supergroups, a star tree would still suggest between 19 and 22 Nups in LECA (where 19 are found in at least one representative genome from each supergroup and 22 is the minimum number of Nups in any one supergroup — Figure 1). That all major subcomplexes are represented even in the about conservative estimate (19 Nups) suggests LECA possessed a NPC comparable in complexity to NPCs in modernistic eukaryotes.

Evidence for a rudimentary NPC anchoring organisation in LECA

While the NPC does not traverse the lipid bilayer of either the inner our outer nuclear membrane, several nucleoporins are involved in anchoring the NPC to the nuclear envelope (reviewed in [two], [6]). Amidst characterised Nups involved in anchoring, Pom34 and Pom152 are thought to be restricted to fungi, whereas Pom121 and Gp210 are vertebrate-specific (reviewed in [40]). The apparent lack of overlap led to the proffer that the anchoring system may either be restricted to opisthokonts, or that it evolved by convergence [11]. Ndc1, a known transmembrane Nup from yeast, has recently been demonstrated to be a constituent of a range of fungal and vertebrate NPCs [45], [46], [47], indicating that parts of the anchoring system evolved earlier the divide of vertebrates and fungi.

Our results significantly extend this view (Figure ane & Table two). We identify homologs for Gp210 across all 5 supergroups, with multiple candidates across Amoebozoa, Plants, Chromalveolates and Excavates. It therefore seems probable that the absenteeism of Gp210 from Fungi, where elective Nups have been extensively characterised [48], is the result of secondary loss. Identification of Ndc1 homologs is somewhat more restricted; it is readily detected in green algae and plants (Table 2), but simply a unmarried candidate is detected among the Chromalveolates (Phytophthora infestans), likewise among Excavates (Trichomonas vaginalis), and we found no candidates amid the Amoebozoa. As shown in Effigy 2, the distribution of Ndc1 nevertheless suggests this Nup can be placed in LECA, under either rooting. Splitstree analyses showed the Ndc1 dataset was noisy; a simple distance-based tree (BioNJ, JTT, γ, 100 bootstrap replicates) does not indicate contempo horizontal gene transfer from either Plantae or Opisthokonts to either of these lineages (Supplementary Effigy S1).

Bolstering the proposition that LECA possessed an anchoring organisation is the broad distribution of Nup35 (known as Nup53 in yeast and some vertebrates [vi]), which is also conserved beyond all five supergroups. Nup35 is integral to NPC assembly [49], [fifty], it interacts straight with Ndc1 [47], [49] and may also contribute to anchoring of the NPC to the nuclear envelope via an amphipathic α-helix [51]. We therefore propose that Gp210 and Ndc1, peradventure with the inclusion of Nup35, establish the ancestral anchoring arrangement in LECA.

Does the distribution of integral membrane Nups shed whatsoever light on the development of variant mitoses?

In stark dissimilarity to the results for Gp210, Ndc1 and Nup35, the other integral membrane Nups (Pom34, Pom121 & Pom152) display a more limited distribution (Table 2). Information technology has been noted that the non-overlapping distribution of these three transmembrane Nups correlates with open mitoses in vertebrates (Pom121) and closed mitoses in yeasts (Pom34 and Pom152) [12]. In closed mitosis, the nuclear envelope remains intact during cell division, whereas in open mitosis, the nuclear envelope disintegrates, and envelope and NPC must be reassembled following partitioning [52], though there appear to be many variations therein [thirteen], [53]. Stunningly, experimental studies have demonstrated partial disassembly of the NPC during so-called 'closed' mitosis in Aspergillus nidulans [54]. Nonetheless, Pom152 remains associated with the nuclear envelope. In a Saccharomyces cerevisiae pom34ΔN nup188Δ double mutant, Miao et al. [12] observed disassembly of some of the same FG echo-containing Nups equally were disassociated during airtight mitosis in A. nidulans, raising the possibility that both may be central to (partial) pore maintenance during closed mitoses.

While a degree of caution is warranted concerning the open/closed mitosis dichotomy [53], particularly among the Fungi (but besides in early development in Drosophila and Caenorhabditis species, where early embryonic nuclei divide in a syncytium), our data do shed some light on the correlations noted by Miao et al. [12].

In the instance of animals, it seems that Pom121 is restricted to vertebrates (Table 2): we discover no homologs of Pom121 in diptera, tunicate or nematode genomes analysed, nor do we find a candidate in Monosiga brevicollis, a Choanoflagellate (sis group to metazoa — [55]; all of these groups undergo open mitoses [13], [56]). On these data, it seems hard to assign a general office for Pom121 in open up mitosis, though a specific office in this process in vertebrates is of course plausible [57].

A more informative picture emerges across the fungal genomes nonetheless. We note that Ascomycetes as a group are characterised by closed mitoses [xiii], whereas amid Basidiomycetes no cases of closed mitosis have been reported, and open mitoses are well-characterised in a number of species (reviewed in [58]).

Our initial analyses (Tabular array 2) indicated that Pom152 was present across all fungi, but no Pom34 homologs were present in the two Basidiomycetes included in our screen, Ustilago maydis & Cryptococcus neoformans, both of which showroom open mitosis [58], [59]. To farther examine this pattern, we screened four additional Basidiomycete genomes (Phanerochaete chrysosporium, Laccaria bicolour, Coprinossis cinea & Malassesezia globosa) as well as that of the zygomycete Rhizopus oryza, which is thought to likewise undergo open mitosis [58]. As is articulate from Table 4, all fungal genomes screened carry both Ndc1 and Pom152 homologs, only Pom34 is restricted to Ascomycetes. Given the broad phylogenetic distribution of ascomycete species included in our analysis [lx], it seems reasonable to conclude that Pom34 was present in the ancestor of this group, but not in that of Basidiomycetes as suggested by the complete absenteeism of Pom34 homologs among those fungi.

This issue suggests that Pom34, merely non Pom152, is primal to this distinction, at least within dikaryote fungi. We failed to find evidence of either Pom34 or Pom152 in the microsporidian Encephalitozoon cuniculi, which undergoes closed mitosis [61], indicating that if Pom34 is integral to the evolution of closed mitosis in Fungi, this may but be limited to Ascomycetes. Having said that, simply seven Nups were detected in Eastward. cuniculi, and the combination of reductive adaptation to a parasitic lifestyle and rapid sequence-level evolution for some genes [62] may complicate homolog detection in this lineage. In this respect, information technology does seem that at least office of the anchoring system may well accept evolved multiple times [11]. In that there appears to be a spectrum between open and closed forms of mitosis [53], and given that open and closed mitoses probable have a complex evolutionary history [thirteen] [63], experimental screens may well yield a broader diversity of pore membrane (POM) proteins than hitherto recognised.

Complete coatomer complex components are traceable to LECA

The ascertainment that Nups and coatomer proteins share a common architecture [18], [64] has led to the proposal that these also share a mutual evolutionary origin. This protocoatomer hypothesis [18] is supported by the observation that vesicle coat proteins are well conserved across eukaryotes [65], [66], [67], [68] and take expanded via duplication and divergence [67], [69], [lxx]. Vesicle glaze complexes are involved in movement of cargo betwixt the various organelles that establish the endomembrane arrangement, and are one part of this evolutionarily conserved arrangement that also includes the evolutionarily ancient just distinct ESCRT organization [67], [71].

While previous analyses leave picayune doubt that the COPI, COPII, clathrin/adaptin complexes, are a characteristic of LECA, less focus has been placed on patterns of conservation at the level of private components. We therefore screened for private protein subunits from each complex across a representative dataset spanning five supergroups. In dissimilarity to the overall pattern of conservation of the NPC, the COPI, II and clathrin/AP complexes were extremely well conserved and orthology predictions were assessable using phylogenies (see Supplementary file SI4). At the level of supergroups there are only four discernible differences (Table 5; accession numbers are in supplementary Table S2). Apm2, a clathrin adaptor protein medium (µ)-chain poly peptide homolog, appears restricted to Saccharomycetes, and tin be readily attributed to cistron duplication (supplementary Figure S2). However, it remains unclear whether Apm2 is a bona fide component of Clathrin complexes. Data to appointment indicate no discernible phenotype in yeast knockouts [72], it has non been ascribed to any AP complexes in yeast [73], [74], and interaction with Apl2p (a constituent of the AP-1 clathrin adaptor circuitous) is merely clearly observed when Apm2p is overexpressed [75].

Vertebrate Apl1 has likewise clearly evolved via duplication from the more broadly distributed Apl2 (supplementary Figure S3). Fungi also comprise both Apl1 and Apl2, just these form distinct phylogenetic clans (Figure S3), suggesting fungal Apl1 and Apl2 are paralogues that did not evolve via duplication in an early fungal lineage. Non-Ophisthokont Apl2 sequences appear to grade two separate clans in the unrooted tree inconsistent with eukaryote supergroups, suggesting that Apl2 and fungal Apl1 accept evolved via a circuitous blueprint of ancient duplications and losses. The trees are non sufficiently robust to establish all events with confidence, but a robust minimal conclusion is that vertebrate and fungal Apl1 accept dissever evolutionary origins.

Nosotros observe only ii other instances where an entire supergroup lacks a component; both impact COPII: the two amoebozoa represented hither (Entamoeba histolytica and Dictyostelium discoideum) lack Sec16, a COPII constitutent, but in dissimilarity to previous analyses [65] we do find candidates for all other COPII components in this group. The other supergroup-level absence is Sfb3, for which no homologs were recovered from either Excavates or Chromalveolates. In S. cerevisiae, Sfb3 is involved in vesicle budding and ship of cargo from the ER but non vesicle fusion with the Golgi trunk. Its function tin can be compensated for at lower temperatures by Sec24, with which it is homologous [76]. We identified Sec24 homologs in all Excavate and Chromalveolate genomes we screened, so in a scenario where Excavates and Chromalveolates represent the deepest branches of the eukaryote tree (as per Effigy 2, left hand tree), the only innovation since LECA would be a single proceeds of a duplicate cistron in the lineage leading to Plantae, Amoebozoa and Opisthokonts. Under the Unikont/Bikont rooting (cf Figure two, right manus tree), this 'innovation' vanishes and is instead two losses. That such extreme conservation of components exists at the supergroup level is stunning.

WD-repeats are present in Leaner and Archaea

Previous analyses report the presence of weak homologs to NPC components in bacteria and archaea, though no published information point to nuclear pore complex constituents in the genomes of either domain [10], [eleven]. Supplementary Table S3 summarizes the results of our HMMer-based screen every bit applied to 49 bacterial and archaeal genomes. We found numerous hits in both archaea and bacteria to WD-echo containing proteins. WD-repeat proteins possess a characteristic β-propellor fold [77] and are important for poly peptide binding equally they tin can form reversible complexes with several proteins, allowing coordination of sequential and/or simultaneous interactions that involve several sets of proteins at the same time. They contain a large family unit involved in a variety of essential biological functions such as signal transduction, transcription regulation and apoptosis [78]. While to our cognition no WD-echo proteins accept been characterized in Archaea, a small number take been characterized in leaner, including AglU, which is required for gliding motility and development of spores in Myxococcus xanthus [79], and the Hat poly peptide from Synechocystis sp. PCC6803, required for control of high affinity transport of inorganic carbon [80].

While nosotros detect proteins with similarity to WD-repeat containing Nups (including in planctomycete genomes), sequence similarity is restricted to the WD-repeat regions alone; characteristic motifs that enable Nup identification (such as the SIEGR-motif in Rae1) are absent. That WD-domains are consistently identified in genomic screens of all three domains supports the view that these are extremely ancient [10], [11], [77], but WD-repeat containing nucleoporins, like other Nups, announced to be a eukaryote-specific innovation.

Conclusions

The number of features that can be traced dorsum to LECA is truly stunning, and includes the nucleus and endomembrane systems [67], [68], [81], [82], [83], linear chromosomes with telomeres [84], mitochondria [85], [86], peroxisomes [87], the cell division apparatus, mitosis and meiosis [88], [89], [90], [91], [92], phagocytosis [81], [93], [94], introns and the spliceosomal apparatus [95] and sterol synthesis [96]. Our screen for NPC components farther establishes the view that LECA was a complex entity, and enables a complex nuclear pore to be ascribed to LECA, building on and confirming the conclusions of earlier studies [ten], [11].

However, the immense gap between eukaryote Nucleoporins and the express detection of related components in either bacterial or archaeal genomes leaves usa no closer to establishing how these structures evolved. Mans et al. aptly referred to this as an 'result horizon' [10], [97], and nosotros note that while the availability of additional eukaryote genomes is leading to a successively clearer picture of the nature of the LECA, screens of bacteria and archaea are not narrowing this gap. Structural screens and experimental characterisation are generating of import new functional data, such equally with the recent characterisation of structural proteins resembling eukaryote membrane-coat proteins in Gemmata obscuriglobus [98], [99]. However it is difficult to place such data within the context of eukaryote stem evolution as multiple interpretations are possible.

In the current case, the emerging flick is of an extremely well conserved set of vesicle-blanket complexes beyond eukaryotes, with a similar conclusion possible for the NPC. As all these complexes are traceable to the eukaryote root, information technology is not formally possible to fully evaluate the protocoatomer hypothesis [18] using comparative genomic data. While some have advocated gene phylogenies [83], Nups show low levels of sequence conservation, complicating attempts to examine the deep phylogeny of the related components of vesicle coats and the NPC. Having said that, the predictive power of the protocoatomer hypothesis is clear: a prediction of this hypothesis is that, if the NPC dates back to LECA, then so should at least one set of vesicle-coating complex components. Nosotros can uncontroversially assign the unabridged set of coatomer complex components from COPI, COPII and clathrin-containing complexes to LECA.

Comparative genomic studies accept the power to generate a wide overview of evolutionary conservation, and are in this respect helpful tools in understanding the evolution of cellular structures. Such studies can therefore provide a valuable starting point for focused investigation of the cell biology of a specific species. At the same time, they are dependent upon experimental observation, just tin also suggest fruitful avenues for subsequent experimental study. Further investigation of the evolution of variant mitoses (broadly classified as open and closed) may well be worthwhile within the context of the development of the nuclear pore circuitous.

Materials and Methods

Nup sequences were collected, aligned and alignments vetted every bit previously described [9]. As conservation between fungi and metazoan sequences was in some cases poor, dissever fungal and metazoan alignments were created where necessary. Alignments were used to build local and global hmm profiles using HMMER 2.three.2 (http://hmmer.wustl.edu/) [21]. Species from which training data were derived are given in Table two. Using hmmsearch from the HMMER package, annotated protein sequences derived from eukaryote genomes (given in Table ii) were screened for nucleoporin homologs.

Candidate Nup homologs were assessed using domain information in UniProt (http://www.uniprot.org/) and PFAM (http://pfam.sanger.air-conditioning.great britain) [22], likewise as our examination of all alignments. Sequences lacking typical motifs/domains associated with a given Nup were removed from the analysis. All remaining candidate Nup sequences were dorsum-blasted (blastp) confronting the non-redundant database (NCBI). Candidates that returned best hits against other proteins were removed.

For any given eukaryote genome, where no homologs were detected for a particular Nup, the genome was screened using Nups from closely related species using blastp and tblastn.

Planctomycete genome sequences (Gemmata obscuriglobus, Kuenenia stuttgartiensis, Planctomyces maris, Planctomyces limnophilus, Rhodopirellula baltica) were additionally queried with our profile HMMs using Genomewise from the Wise 2.ii.0 package [23].

Sequences for the individual components of the COPI, COPII and Clathrin coatomer complexes in Southward. cerevisiae were retrieved from the SGD database (http://www.yeastgenome.org) using the respective vesicle coat names as query. Sequences were used to seed initial PSI blast searches [24] against the nr protein database at NCBI. Sequences were evaluated past ways of reciprocal blastp searches, every bit to a higher place. Alignments from the obtained sequences were generated using probcons [25] and profile hmms were created from alignments for local and global hmm profile searches. All profiles were calibrated to increase search sensitivity. Sequences obtained were evaluated as described above for Nups.

Equally an help in assigning orthology, phylogenetic networks (NeighborNet [26]) were built for NPC and coatomer components using SplitsTree [27], [28]. Phylogenetic trees were synthetic using raxML 7.two.ii [29] and BioNJ [30], [31]. Phylogenies were reliable for coatomer components but non beyond Nups. Full Nup alignments (in clustal format) and coatomer trees (in splitstree format) are provided as supplementary material (supplementary File S1).

Supporting Information

Figure S2.

Neighbor-Joining tree of Apm1 and Apm2. Apm2 is restricted to the Saccharomycetes and probable evolved via gene duplication. The position of the Apm2 from Yarrowia lipolytica is poorly supported and likely spurious. The tree (BioNJ, JTT, γ, 100 BS replicates) was generated from protein sequence alignments.

https://doi.org/ten.1371/journal.pone.0013241.s005

(0.eighteen MB DOC)

Figure S3.

Unrooted PhyML tree of Apl1 and Apl2. Vertebrate Apl1 (bluish) and Apl2 evolved via gene duplication. Apl1 from fungi (night blue) announced paralogous to vertebrate Apl1, and the results do not back up development by duplication and departure from fungal Apl2. The tree was generated from protein sequence alignments using the phylogeny.fr server (Dereeper A, et al. 2008 Nucleic Acids Res. 36:W465-9). Co-operative back up (approximate likelihood ratio test: SH-like). Similar topologies were obtained with both ML and neighbour-joining methods, and with a range of parameters and models.

https://doi.org/10.1371/journal.pone.0013241.s006

(1.00 MB DOC)

Author Contributions

Conceived and designed the experiments: NN AMP. Performed the experiments: NN DL. Analyzed the data: NN DL AMP. Wrote the paper: NN AMP.

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