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Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes.

1. Introduction

Meiosis is a division of germ-line cells that involves recombination of genetic material and segregation of homologous chromosomes, leading to production of haploid gametes from a diploid cell, while mitosis preserves the initial chromosome number in both daughter cells. Meiosis is an obligatory component in sexual process in eukaryotes. The origin and evolution of the mechanism of meiosis and proteins involved in meiotic processes are a matter of discussion [1-6].

A principal difference between the results of meiosis and mitosis is determined by their difference in genetic control, chromosome structure, and chromosome behavior. A difference at the ultrastructural level appears as formation of meiosis-specific synaptonemal complexes (SCs), the ultrastructures that join homologous chromosomes into bivalents during pachytene stage of meiotic prophase I in the vast majority of eukaryotes. SC is necessary for specific organization of prophase meiotic chromosomes [7-9], synapsis of homologous chromosomes [7, 10, 11], and chiasma number per one SC sufficient for regular homologues segregation [8,12].

SCs are formed of meiosis-specific proteins [11, 13, 14]. General organization of the SC is more or less similar among all eukaryotes examined in this respect, while ultrastructure of its morphological components slightly varies [8, 15]. In addition to the ultrastructural variation, low, if any, similarity was found between the specific proteins that build up SCs in plants, fungi, and animals [11, 14, 16]. It means that the functional conservation of the proteins as the material for constructing SCs is not associated with homology of their amino acid sequences. Thus, the general picture can presumably be presented as follows. Nonhomologous proteins build up the SCs, which are rather conserved ultrastructures of meiocytes and perform a common function in the course of meiosis in eukaryotic organisms [4]. It is still an enigma as to how very dissimilar proteins can build intracellular structures with principally similar morphology and function.

It is worthwhile to consider several details of SC protein diversity. Lateral elements (LEs) of the SC are formed on the basis of chromosomal axial elements, which connect sister chromatids and consist mostly of cohesins [17]. The LEs are joined together to produce the integral SC structure via a zipper of transversal filaments, which pass through the SC central space. Heads of the transversal filaments overlap in the middle of the central space to form a SC central element (CE) [4,13].

Different meiosis-specific proteins of SCs are synthesized in generative cells on the eve or in the course of early stages of meiosis [17, 18]. Since the first SC proteins have been identified, yeast Hop1andZip1 [19-21], rodent SYCP1 [22,23], SYCP2 [24], and SYCP3 [23, 25], the SC proteins that would be universal for all eukaryotes are sought by bioinformatics methods. However, it has been observed that the mammalian SC central space protein SYCP1 is nonhomologous to yeast SC central space protein Zip1 [26]. Their functional analog in plants, ZYP1 from Arabidopsis, has only 20% identity with two former proteins [27, 28]. The same is true for the Drosophila protein encoded by gene c(3)G [29, 30] and for nematode SYP-1 [31]. A secondary structure of some parts of polypeptide chains of all these proteins is only their common feature; that is, all they have globular domains at the N and C ends and a central a-helical domain. The long a-helix (coiled coil) makes the molecule rod shaped [10, 32, 33], which is essential for producing transversal filaments in the SC central space. Murine low-molecular-weight proteins that modify the structure of the SC central space (SYCE1, SYCE2, SYCE3, and TEX12) initially were considered as having only vertebrate orthologs [34-36].

The mammalian LE proteins SYCP2 and SYCP3 have only a low similarity to their counterparts of yeast (Hop1, Red1), nematode (HIM-3), and Arabidopsis (ASY1), identified more recently [23, 37-40]. A HORMA domain is the only feature common for certain proteins of the SC LEs. Thus, the SCs are similar in general morphology (structural plan) but differ in ultrastructure and consist of different proteins in yeast, nematode, Drosophila, mammals, and Arabidopsis. These organisms are hereafter referred to as models to study the SC proteins.

Ramesh et al. [3] have carried out an interesting study, searching for orthologs of key meiotic proteins in the proteomes of Archaea, bacteria, and 15 eukaryotes of different taxa from protists to human. Of all structural meiotic proteins, only the LE component Hop1 was included in the analysis. Hop1 orthologs were found in almost all of the species examined, including human and mouse. The mouse protein was identified as HORMAD1, which is considered below.

Fraune et al. [41] made the next step and found SYCP1 and SYCP3 orthologs in the proteomes of various metazoan taxa, including Placozoa, Porifera, and Coelenterata. Protein fragments identified as the most conserved, rather than total amino acid sequences, were used as queries. A bioinformatics search was supplemented by an experimental verification in the case of Hydra. In a recent study, Fraune et al. [42] extended their experiments and traced the origin of proteins structuring the SC central space. They found that SYCE2 and TEX12 are conserved in Metazoa, SYCE1 appears in Bilateria, and SYCE3 is specific for Vertebrata.

Our hypothesis is that the homology of some polypeptide domains rather than that of whole proteins is critical in constructing ultrastructural components of SCs in remote taxa. The main objective of our work was to search the proteomes of diverse eukaryotic taxa, especially those not yet examined before like different unicellular animals, algae, lower fungi, mosses, and some others, for proteins and their domains similar to the SC proteins of the model organisms. We are the first to consider almost all known SC proteins of the model organisms when seeking related proteins in the proteomes of main eukaryotic taxa in one study. We obtained a large list of proteins, which can serve as a potential source for a targeted search for orthologs of the SC proteins using phylogenetic trees and constructed example trees for groups of organisms so far poorly studied in this respect.

2. Materials and Methods

In total, approximately 11 million proteins from approximately 5000 proteomes of all main eukaryotic groups were tested. The taxonomy available from the NCBI database (http://www.ncbi.nlm.nih.gov/) was used. The SCproteins of the seven model eukaryotic species, namely, yeasts Schizosaccharomyces pombe and Saccharomyces cerevisiae, plant Arabidopsis thaliana, nematode Caenorhabditis elegans, insect Drosophila melanogaster, fish Danio rerio, andmammal Mus musculus (as most common objects in meiosis studies) were used as queries in comparisons with the above proteins (Tables 1 and 2). In these model organisms, SC proteins had been isolated and studied experimentally, except D. rerio whose genome was well studied and SC proteins were revealed with bioinformatic methods. In one experiment, D. rerio was substituted by another fish Anoplopoma fimbria. This is why we did not include Af into list of main model organisms. As soon as the mammalian SC proteins SYCE and TEX, discovered recently, were found in mouse, we consider the mouse as the most representative mammalian species, if only one species is to be chosen as query in laborious computer database monitoring. Human SC proteins are very similar to their mouse counterparts, and their use as queries will add no new results, comparatively to mouse.

The amino acid sequences of SC proteins were sought in the NCBI (http://www.ncbi.nlm.nih.gov/) and UniProtKB/ Swiss-Prot (http://www.uniprot.org/uniprot/) databases. The functional domains of the above proteins were identified using CDART software (http://www.ncbi.nlm.nih.gov/ Structure/cdd/wrpsb.cgi?). Random amino acid sequences were generated on the basis of native proteins by the RandSeq program (http://au.expasy.org/tools/randseq.htm) to serve as a control in estimating protein similarity.

Proteins similar to SC proteins were sought in the proteomes of main eukaryotic groups using NCBI Protein BLAST software (http://www.ncbi.nlm.nih.gov/blast/Blast .cgi?PROGRAM=blastp&BLASThPROGRAMS=blastp&PAGE _TYPE=BlastSearch&SHOW_DEFAULTS=on&LINK_LOC= blasthome#). The taxa examined are summarized in Tables 3-6. The taxa with only few protein sequences available from the databases were pooled. The parameters of our PROTEIN BLAST search were as follows. Maximum target sequences are 1000 or 5000 in different studies (maximum number of aligned sequences to display; the actual number of alignments may be smaller or greater than this). Expect threshold is 100 (this setting specifies the statistical significance threshold for reporting matches against database sequences. The default value (100) means that 100 such matches are expected to be found merely by chance). The others were default parameters. The similarity index score (BLAST output) is based on three parameters: the number of matching amino acid residues, the number of amino acid residues of the same type, and the number of gaps, that is, cases where a certain position is occupied by an amino acid residue in one protein and is empty in another. For each of the SC proteins, the scores for similarity with proteins of the proteomes of a particular eukaryotic group were compared for the protein in question and its "random" analog. The significance of the similarity index was characterized by the E-value, which reflects the number of similar proteins that might be selected at random by the BLAST program and is calculated by the BLAST itself. Maximal scores, found by BLAST, in their increment order, are summarized in the tables (see Results and Discussion). The SC proteins with a score lower than 50 are not listed because their similarity was considered to be very low. When similar scores were obtained for a native and a "random" protein, we compared their scores averaged over the 10 best search results. Comparisons by Student's t-test were performed using STATISTICA software v.7 (http://www.statsoft.com).

As the score depends on the sequence length, it is incorrect to compare the scores obtained for differently sized proteins. However, a "vertical" score comparison, that is, a comparison of scores obtained for similar proteins from different eukaryotic groups, seems proper. It is also clear that absolute score values are of little importance when the scores are low and comparable with those of random sequences.

Phylogenetic trees were constructed using the constraint-based multiple protein alignment tool (COBALT) from the NCBI package (http://www.ncbi.nlm.nih.gov/tools/cobalt/ cobalt.cgi?CMD=Web). Default parameters were used in multiple sequence alignment. At the final stage of constructing trees, the fast minimum evolution algorithm was employed. Protein IDs are listed in figure captions. Proteins with the highest similarity to Hop1 and ASY1 were considered for each taxon.

3. Results and Discussion

A list of SC proteins of seven model organisms is provided in Table 1. Protein size and some characteristics of their functional domains are shown in Table 2. Similar proteins were sought in proteomes of all eukaryotic species available in databases at the time of study (see Materials and Methods) using the BLAST program. The degree of similarity was estimated as score index (see Materials and Methods).

3.1. Regularities of Distribution of the Studied Proteins among Eukaryotes. As expected, extremely high scores were obtained when comparing yeast SC proteins with yeast proteomes, nematode SC proteins with nematode proteomes, and so forth (i.e., a protein with a cognate proteome). The result testified that the method worked; obviously, these data were not included in the tables. The scores were depending on the protein size. For instance, a score of 178 was obtained for mouse SYCE3 (88 residues), while mouse SYCP2 (1500 residues) had a score of 3106.

3.1.1. Algae, Mosses, Flowering Plants, and Fungi. Proteins similar to the yeast and Arabidopsis SC proteins Hop1, ASY1, and ASY2 were found in the proteomes of algae, mosses, fungi, and higher plants (Table 3). The highest similarity to the vertebrate SYCP1 proteins was observed for proteins from the proteomes of green algae, brown algae, and ascomycetes (Table 3), which seems to be due to their secondary structure similarity (see below). All of the unicellular eukaryotic groups examined had proteins more or less similar to the SC proteins of the model organisms (Table 4). The highest scores were obtained for the group Fornicata-Parabasalia-Heterolobosea. Their Hop1 orthologs are already annotated in databases. Parabasalia is possibly the most ancient eukaryotic group with sexual reproduction [44].

As an example of practical usage of found similarities, we constructed phylogenetic trees of HORMA-domain proteins similar to Hop1 of Saccharomyces cerevisiae and ASY1 of Arabidopsis thaliana. One species whose protein showed the highest similarity to Hop1 and ASY1 was selected from each of the taxonomic groups shown in Tables 3 and 4, with the exception of Ciliophora. The proteins were mostly counterparts. The protein IDs and source species are listed in figure captions. As control, we used a distantly related protein of the archaean Methanococcus voltae that displayed a low but still significant similarity to Hop1. One tree (Figure 1) was constructed for algae, fungi, mosses, and green plants. As expected, the archaean protein was automatically excluded by the program. The protein found in lower fungi (Nosema ceranae, Microsporidia) was also excluded by the program, which might be expected as well. An unexpected finding was that Hop1 of the yeast S. cerevisiae was rather distant from all of the other proteins included in the tree.

Another tree (Figure 2) was constructed for proteins of unicellular eukaryotes and included the known Hop1 and ASY1 proteins. The Methanococcus voltae (Archaea) and Monosiga brevicollis (Choanoflagellata) proteins were excluded automatically, while clustering with Giardia intestinalis (Fornicata) Hop1 at the step of Cobalt tree construction. The Choanoflagellata proteins displayed, in fact, only a minor similarity to the SC proteins of the model organisms.

3.1.2. Animals. Among the multicellular organisms listed in Table 5, mollusks had the highest scores of similarity between some of their proteins and the model SC proteins. SYCP2 and SYCP3 homologs of Crassostrea gigas (maximal scores 80 and 199, resp.) are annotated in the NCBI database. A SYCP3 homolog was additionally found in the proteomes of the sponge Amphimedon queenslandica ([Score.sub.max] = 116) and the coelenterate Hydra magnipapillata (Scoremax = 135). It should be noted that the sponge protein found in our search (Table 5) did not coincide with the SYCP3 described by Fraune et al. [41]. A protein annotated as SC65 occurred in the proteome of an ascarid nematode (Scoremax = 129). As a control, we compared SC65 for mouse and fish (score = 456) and SYCP3 for mouse and fish (score = 263). It is seen that the scores obtained for SC65 and SYCP3 similarities with proteins of the above eukaryotic groups were sufficiently high. All of the eukaryotic groups included in Table 5 had not only proteins similar to animal SC proteins, but also those similar to yeast Hop1 and plant ASY1.

To better understand the above values, it may also be helpful to consider the scores obtained for several other proteins. The highly conserved meiotic enzyme DMC1 showed the following maximal scores in comparisons of mouse DMC1 with proteins of other organisms: 622 for Danio rerio, 307 for Caenorhabditis elegans, 391 for Arabidopsis thaliana, 310 for Drosophila melanogaster, and 372 for Saccharomyces cerevisiae (our data). The maximal scores obtained in similar comparisons for the structural SC protein SYCP1, whose conservation is by far lower, were 320, 49, 38, 42, and 33, respectively. It is clear that scores that exceed 100 in comparisons of the SC proteins with coelenterate or mollusk proteomes may point to some relatedness of certain proteins, although their orthology is out of the question.

The most highly organized animals had proteins directly orthologous or highly similar to the SC proteins of the model organisms (Table 6). The hypothetical protein BRAFLDRAFT_118903 found by us in the proteome of Branchiostoma floridae (subtype Cephalochordata) is similar to different proteins forming the SC transversal filaments. The protein contains multiple Filamin-type immunoglobulin domains (Filamin/ABP280 repeats), and a distinct a-helix forms in the central part of its molecule (our data), as in SC transversal filament proteins of model organisms. The protein CBY10027.1 of Tunicata showed an additional similarity to a random analog of mouse SYCP1 (Table 6). The protein contains GCC2_GCC3 repeats and a Trichoplein domain (for more detail, see below) and similarly forms an a-helix, although it is in the C-terminal region of the molecule.

3.1.3. Taxa without "Standard" SC Proteins. Several eukaryotic taxa were not found to have proteins with a considerable similarity to the SC proteins of the model species selected for our comparisons. We did not include these taxa in the tables and just list them here. These were Rhodophyta, Euglenophyta, Chrysophyta, Charophyta, Xanthophyta, and Dinoflagellata among algae. Among animals, there were Mesozoa, Gnathostomulida, Bryozoa, Cycliophora, Myzostomida, and Nemertea; also there are Rotifera, Nematomorpha, Scalidophora, Acanthocephala, Entoprocta, and Gastrotricha from Coelomata. Likewise, no proteins similar to SC proteins were found in Tardigrada and Onychophora (Protostomia) and in Hyperotreti, Hyperoartia, and Chondrichthyes (Chordata).

Proteins with significant similarity to only FKBP6 (peptidyl-prolyl cis-trans isomerase) were found for several taxa, which were also not listed in the tables. The taxa included Cryptophyta, Diatoms, and Pelagophyceae (algae) and Perkinsea, Oomycota, and Labyrinthulomycota (Labyrinthulida), the two last groups additionally having proteins similar to mouse SYCP1. Among animals, Rhizaria, Myxosporea, amoeboid protists, and Annelida also have proteins similar to mouse FKBP6.

We did not detect any proteins similar to structural meiotic proteins in these eukaryotic groups possibly because only few of their proteins are available in databases. The exceptions are Rhodophyta, Dinoflagellata, Chondrichthyes, Oomycota, Rhizaria, and Annelida. For each of these phyla more than 10 proteomes are annotated in databases. It means that SCs in these taxonomic groups, if exist at all, lack typical proteins of model SCs and could be built of noncanonical proteins.

3.1.4. Meiosis without SC and with Nontypical SCs. Meiosis is thought to appear simultaneously with mitosis [5] or to originate from mitosis [6]. Most components of molecular machinery necessary for initiating homologous pairing (e.g., meiosis-specific cohesin Rec8 and others) might arise as early as at the time of origin of protoeukaryotes [6], while SC components are possibly of a more recent origin. Key meiotic proteins have been found in the protist Giardia intestinalis, although the organism presumably lacks meiosis [3]. Both Ramesh et al. [3] and Cavalier-Smith [1] have assumed that meiosis arose quite early in eukaryotic evolution. However, only Hop1 of all SC proteins has been included in their analysis.

We could not establish whether SCs form during meiosis in all of our subjects. Meiosis proceeds without SCs formation in lower fungi, such as Schizosaccharomyces pombe and Aspergillus nidulans (cited from [8]). Meiosis is absent in the ascomycete Candida albicans and present in Candida lusitaniae, but both of the species similarly lack key SC proteins resembling SC proteins of the model organisms [45]. At the same time, the SC forms in the ascomycete Neurospora crassa andbasidiomycete Coprinus cinereus [46-48]. The SCs form also in Eimeria tenella (Apicomplexa) [49] but not in its distant relative Tetrahymena thermophila (Ciliophora), while residual SC-like structures are observed in the protist Stylonychia [50]. The brown alga Ectocarpus siliculosus has meiosis [51], but only its Hop1 is annotated in databases (Table 3). Red algae and diatoms form the SCs [46]. The proteomes of algae, mosses, green plants, and fungi listed in Table 3 include proteins similar to yeast and plant LE proteins, including Hop1, ASY1, and ASY2. Yet the algal, moss, and fungal proteomes were not found to have proteins similar to yeast Zipl or Arabidopsis ZYP1, which form transversal filaments in the SC. We detected only the proteins that have a rather low similarity to vertebrate transversal filament proteins. These eukaryotic groups evolved independently of each other [51]. Their SCs might include still unidentified proteins with a secondary structure characteristic of SC transversal filaments.

Interestingly, proteins with a high similarity to any known SC protein were not detected in the proteomes of Choanoflagellata, which are thought tobe the nearest relatives of Metazoa among all unicellular organisms [52]. This observation may indicate that the known SC proteins arose in more highly organized eukaryotes. It is possible that each of the independent evolutionary lineages of multicellular eukaryotes (red and brown algae, green plants, fungi, and animals) has two categories of meiosis-specific proteins: a common set of basic meiotic proteins, as may be suggested from the findings reported by Ramesh et al. [3], and, additionally, a lineage-specific set of structural proteins, including SC proteins. The hypothesis is supported by the fact that proteins similar to SYCP1 and SYCP3 are found in the proteomes of basic Metazoa [41] and are absent from fungi and plants.

Certain structural meiotic proteins were established to be closer to bacterial proteins in their origin, while some others are more similar to the Archaeal proteins [53]. However, the SC proteins generally show a low, if any, similarity with prokaryotic proteins, which does not exceed that between random amino acid sequences and prokaryotic proteins [53]. These findings have led to the conclusion that the SC proteins arose relatively recently in evolution, when primary eukaryotes evolved.

3.2. SC Proteins of the Model Organisms with Highest Similarity to Proteins of the Eukaryotes Examined. Yeast Hop1 and Arabidopsis ASY1, among all LE components, have similarities primarily with proteins of the algal, moss, fungal, plant, and unicellular animal proteomes. Related proteins were additionally found in the proteomes of highly organized animals. These proteins have the HORMA domain, which structures the chromosomes. The other SC components, such as mouse and fish SC65, SYCP2, and SYCP3, showed significant similarities only with proteins of multicellular organisms.

A consistently high similarity with proteins of even unicellular eukaryotes was observed for FKBP6, which is annotated as an SC component only in mouse. The maximal scores obtained for FKBP6 reached 115 in plants (Table 3), 133 in unicellular eukaryotes (Table 4), 208 in sponges and placozoans (Table 5), and 402 with a molecule size of 327 residues in vertebrates (Table 6). Distant relatives of FKBP6 were found even in prokaryotic proteomes (eubacterial and Archaeal) with maximal scores of 77 and 41, respectively (our data). The SC central space proteins that form transversal filaments (Zip1, C(3)G, ZYP1, SYP-1, and SYCP1) showed a low, but still significant, similarity with proteins from almost all unrelated eukaryotic groups. A quite high similarity was observed with proteins of related groups.

Proteins related to vertebrate SYCE2 were found in the proteomes of Mollusca, Cnidaria (Table 5), and Echinodermata (Table 6). These proteins are possibly not restricted to vertebrates, contrary to the initial assumption [34]. This conclusion agrees with a possible appearance of the SYCE2like proteins in early Metazoa, as proposed by Fraune et al. [42]. The SC component SC65 occurs not only in Deuterostomia (Table 6), but also, possibly, in Coelenterata, Porifera, and certain Protostomia as well (Table 5). It is remarkable that this protein is annotated in the database for nematodes.

3.3. "Exclusive Proteins" in the Proteomes of Certain Eukaryotic Groups. When comparing the SC transversal filament proteins of the model organisms with proteins of Sporozoa, Placozoa, Mollusca, Echinodermata, and Hemichordata, significant similarity of scores was obtained not only for the native proteins, but also for random amino acid sequences generated on the basis of the native proteins by a special program to have the same size and the same amino acid proportion (italicized in Tables 4-6). The same scores were found for the native and random "SC proteins" used as queries. Generally, the scores obtained for random (control) sequences did not exceed 40 and in many cases were below 30. In the above eukaryotic groups, the maximal score reached 70 (e.g., for mouse SYCP1 random analog). The maximal scores obtained with the native proteins for various proteomes were rather low, but still significant: 70-77 for Zip1, 63-70 for C(3)G, 56-83 for ZYP1a, 53-70 for ZYPlb, 67-99 for mouse SYCP1, 44-66 for fish SYCP1, and 50-68 for nematode SYP-1. E-values were sufficiently high, ranging, for instance, from [e.sup.-9] down to [e.sup.-18] for the native proteins and from [e.sup.-07] down to [e.sup.-12] for random "proteins" in the case of Placozoa; that is, these results were reliable.

To study the reason of almost equal scores for native and random "proteins", domain and secondary structure analyses were carried out by us for the proteins occurring in the proteomes of the above eukaryotic groups and displaying a high similarity to the SC transversal filament proteins. The proteins turned to be few; for example, only one "exclusive" protein was found in each of the Mollusca, Hemichordata, and Echinodermata proteomes. The exclusive proteins had large size in all of the proteomes tested, from 3906 residues in Hemichordata to 7710 residues in Placozoa. A similarity to the SC proteins was restricted to their Cterminal regions, which were taken for further analyses. The domain composition of the C-terminal region slightly differed among these exceptional proteins. For instance, myosin 10 and GCC2_GCC3 functional domains were found in Mollusca proteins. The Smc domain, which is responsible for cell division and chromosome segregation, was detected in the Apicomplexa proteins. We found the GCC2_GCC3 and Trichoplein domains in Hemichordata, the Trichoplein domain in Echinodermata, and many various domains, including two Trichoplein and several myosin domains, in Placozoa. The SMC domains, which structure the chromatin and recruit other proteins, are also of particular importance. These domains were found in certain SC proteins (Table 2). It is noteworthy that all of the domains (i.e., the corresponding protein regions) form a distinct a-helix, as characteristic of SC transversal filament proteins. The Trichoplein is also of interest, being annotated as a meiosis-specific nuclear structural protein.

We performed a "reverse" BLAST search for two proteins, searching the mouse and Drosophila proteomes for proteins similar to the Trichoplax adhaerens (Placozoa) exclusive proteins XP_002107637.1 and XTh002111687.1. Apart from one large mouse protein, the mouse and Drosophila proteins found were small and showed a similarity to the C-terminal regions of the two T adhaerens proteins. The set included various myosins and, in the case of Drosophila, cytoplasmic linker proteins. Both myosins and linker proteins have a-helical domains, as the C-terminal domains of the T. adhaerens proteins (the program COILS from ExPASy tools was used (http://www.ch.embnet.org/software/ COILS_form.html)).

According to bioinformatics criteria, SC transversal filament proteins have much in common with the so-called intermediate proteins, which include proteins of the nuclear lamina, nuclear matrix, and spindle pole body, the myosin heavy chain, and several other proteins. The proteins form an a-helical structure, and all a-helices have approximately 20% similarity with each other. This is due to repetitive "reference" hydrophobic amino acid residues [13, 22, 32]. The same situation was observed in the case of the abovementioned exclusive proteins.

Why the proteins found in certain eukaryotic groups are similar not only to the SC transversal filament proteins, but also to random amino acid sequences generated on the basis of the native proteins? Two explanations are possible. First, similar amino acid combinations might occur in the SC proteins and their random "analogs" because repeats are characteristic of the a-helices present in the former. Second, errors might occur during computer assembly of the sequenced genomes and corresponding proteomes. Genome sites, coding every revealed protein, may be responsible not for a long, but for two shorter polypeptides, the second one being similar to SC protein. This is why C-terminal regions of the proteins found in our work may belong to SC transversal filament proteins or other intermediate proteins. The hypothesis is based on the fact that a-helical proteins occur in many proteomes, while the above phenomenon was only observed for a few proteins from certain eukaryotic proteomes.

4. Conclusions and Prospects

Our comparisons enable a conclusion that Hop1, ASY1, and ASY2 are the most universal of all structural SC proteins (Table 7). They have the HORMA functional domain, which recognizes chromatin states and acts as an adaptor that recruits other proteins. We have assumed previously that HORMA domain-containing proteins play a universal role in formation of SCs in higher eukaryotes as well [4]. Similarly, mouse HORMAD1 was recently found to play an essential role in the SC formation and the correct progress of meiosis [54]. Since SC forms on the basis of chromosome axes via protein-protein interactions, it is clear that similar proteins involved in chromosome organization should occur in the proteomes of all eukaryotes capable of meiosis, and this was actually observed in our study.

The LE proteins are possibly the most ancient of all SC proteins. This assumption seems most plausible given that chromosome axes have formed earlier than SC transversal filaments. SYCP2 and SYCP3 replaced Hop1 and Red1 in animals, although HORMA domain-containing proteins are also active in their meiosis [54]. The replacement was possibly associated with complication of genomes. Yet plants with very large genomes have the Hop1 ortholog ASY1. It is possible that SYCP2 and SYCP3 were recruited in vertebrate animals because chromosome-structuring protein complexes had been complicated to include meiosis-specific cohesins and accessory proteins in Vertebrata. SYCP1 and SYCP3 orthologs, which have recently been found in invertebrates [41], display only a low similarity to their vertebrate counterparts (Table?). The proteins seem to have evolved quite rapidly in parallel with genome complication.

We used mainly the BLAST program with constructing only two phylogenetic trees as examples. It cannot be excluded that protein similarities revealed by using BLAST only cannot provide a basis for phylogenetic inferences [55, 56]. We did not seek particular orthologs for the known SC proteins. Our intention was to find out whether proteins similar to the known SC proteins occur in the proteomes of a particular eukaryotic group. Our results can be used as a basis for a targeted search for orthologs of the SC proteins with the help of phylogenetic trees. The taxa most interesting for such a study were revealed in present investigation and include Chlorophyta, Phaeophyceae, Apicomplexa, Porifera, Placozoa, and Mollusca (Table 7).

The significance of our results usually was high or very high according to the E-values obtained which ranged from low significant [3e.sup.-05] for Zipl Sc in the proteomes of Parabasalia, Fornicata, and Heterolobosea to very highly significant [8e.sup.-171] for SC65 Dr in the mammalian proteomes or even 0.0 for SC65 Mm in the amphibian and avian proteomes. The estimates are comparable with or even higher than those specified as essential for correct phylogenetic inferences in the literature, from [e.sup.-5] [57] down to [e.sup.-20] [58].

Thus, we obtained new evidence for the earlier assumption that different proteins whose common feature is the presence of domains with a certain conformation are used to form the SC in different eukaryotic taxa [4, 59]. Here we extended this conclusion from green plants, fungi, and vertebrates to include protozoans and red and brown algae, while Fraune et al. [41] extended it for invertebrates.

The independent evolutionary lineages of multicellular eukaryotes [51] possibly had a common set of basic meiotic proteins, as may be derived from the results of Ramesh et al. [3], and a lineage-specific set of structural proteins, including the SC proteins. Proteins of SC central space are most evolutionarily variable. It implies that different protein-protein interactions can exist to connect two LEs into SC. At the same time, it looks like HORMA domain is the most valuable to assembly the LE itself from different proteins.

Based on our findings, the lack of proteins similar to the SC proteins of the model organisms in Rhodophyta, Euglenophyta, Chrysophyta, Charophyta, Xanthophyta, and Dinoflagellata makes it possible to assume that meiosis in these algae differs from classical meiosis in proceeding without any SC or that unknown new proteins form SCs in these algae. Either alternative is of interest to investigate.

http://dx.doi.org/10.1155/2014/856230

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Acknowledgments

This work was supported by the Russian Foundation for Basic Research (Grant no. 13-04-02071-a) and the Program "Living Nature" (subprogram "Gene Pool Dynamics and Preservation") of the Presidium of the Russian Academy of Sciences. The authors are grateful to Professor Abraham Korol (Haifa, Israel) for critical-reading the paper and valuable suggestions. The authors acknowledge with thanks assistance of Tatiana Tkacheva in preparing the English version of the paper.

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Tatiana M. Grishaeva and Yuri F. Bogdanov

Vavilov Institute of General Genetics, Russian Academy of Sciences, Gubkin Street 3, GSP-1 Russian Federation, Moscow 119991, Russia

Correspondence should be addressed to Tatiana M. Grishaeva; grishaeva@vigg.ru

Received 1 March 2014; Revised 2 June 2014; Accepted 24 June 2014; Published 23 July 2014

Academic Editor: Yoko Satta

TABLE 1: Eukaryotic SC proteins compared as queries with
unidentified proteins from the proteomes of other eukaryotes.

Number   SC protein       Corresponding model organism

1           ASY1         Plant Arabidopsis thaliana (At)
2           ASY2         Plant Arabidopsis thaliana (At)
3          C(2)M       Insect Drosophila melanogaster (Dm)
4          C(3)G       Insect Drosophila melanogaster (Dm)
5          CORONA      Insect Drosophila melanogaster (Dm)
6          FKBP6            Mammal Mus musculus (Mm)
7          HIM-3      Nematode Caenorhabditis elegans (Ce)
8           Hop1       Yeast Saccharomyces cerevisiae (Sc)
9           Hop1      Yeast Schizosaccharomyces pombe (Sp)
10         Rec10      Yeast Schizosaccharomyces pombe (Sp)
11          Red1       Yeast Saccharomyces cerevisiae (Sc)
12          SC65              Fish Danio rerio (Dr)
13          SC65            Mammal Mus musculus (Mm)
14       SYCE1-like           Fish Danio rerio (Dr)
15         SYCE1            Mammal Mus musculus (Mm)
16         SYCE2              Fish Danio rerio (Dr)
17         SYCE2            Mammal Mus musculus (Mm)
18         SYCE3            Mammal Mus musculus (Mm)
19         SYCP1              Fish Danio rerio (Dr)
20         SYCP1            Mammal Mus musculus (Mm)
21         SYCP2              Fish Danio rerio (Dr)
22         SYCP2            Mammal Mus musculus (Mm)
23       SYCP3-like           Fish Danio rerio (Dr)
24         SYCP3            Mammal Mus musculus (Mm)
25         SYP-1      Nematode Caenorhabditis elegans (Ce)
26         SYP-2      Nematode Caenorhabditis elegans (Ce)
27         SYP-3      Nematode Caenorhabditis elegans (Ce)
28         SYP-4      Nematode Caenorhabditis elegans (Ce)
29         TEX12          Fish Anoplopoma fimbria (Af)
30         TEX12            Mammal Mus musculus (Mm)
31          Zip1       Yeast Saccharomyces cerevisiae (Sc)
32         ZYP1a         Plant Arabidopsis thaliana (At)
33         ZYP1b         Plant Arabidopsis thaliana (At)

Number        Database and
               protein ID

1         RefSeq: NP_564896.1
2         RefSeq: NP_194947.2
3         RefSeq: NP.609788.1
4         GenBank: ACI96726.1
5         GenBank: AAF55549.2
6          Swiss-Prot: Q91XW8
7          Swiss-Prot: G5EBG0
8         RefSeq: NP.012193.1
9         RefSeq: NP.596448.1
10        RefSeq: NP.594524.1
11        RefSeq: NP.013365.1
12       RefSeq: NP_00n19910.1
13        GenBank: CAM23031.1
14        RefSeq: XP.694355.3
15       RefSeq: NP.001137237.1
16        GenBank: AAI33854.1
17       RefSeq: NP.001161718.1
18       RefSeq: NP.001156354.1
19        GenBank: AAH45503.1
20        RefSeq: NP.035646.2
21         Swiss-Prot: F1QMZ4
22        RefSeq: NP.796165.2
23       RefSeq: NP.001035440.1
24        RefSeq: NP.035647.2
25         Swiss-Prot: G5EGS8
26        GenBank: AAC19209.1
27        GenBank: CAB03087.2
28        RefSeq: NP.491960.1
29        GenBank: ACQ58790.1
30        GenBank: AAH61081.1
31        RefSeq: NP.010571.1
32        GenBank: AAY46119.1
33        GenBank: AAY46120.1

TABLE 2: Eukaryotic SC proteins, their functional domains, and the
total protein size (amino acid residues, aa).

                  SC central space proteins

Protein           Functional        Total
                  domains (a)      size, aa

Zip1 Sc (b)       Bacterial SMC,     875
                  Smc, AAA_13

ZYP1a At          Two bacterial      871
                  SMC domains

ZYP1b At          Two bacterial      856
                  SMC domains,
                  PRK00409

C(3)G Dm          Two bacterial      744
                  SMC domains

CORONA Dm         --                 207

SYP-1 Ce          Smc                489

SYP-2 Ce          --                 213

SYP-3 Ce          SGNH_plant_        224
                  lipase_like

SYP-4 Ce          --                 605

SYCP1 Dr          SCP-1              537

SYCE1-like Dr     --                 206

SYCE2 Dr          --                 187

TEX12 Af          --                 135

SYCP1 Mm          SCP-1              993

SYCE1 Mm          Bacterial          329
                  SMC

SYCE2 Mm          --                 177

SYCE3 Mm          --                  88

TEX12 Mm          --                 123

                  LE proteins and other
                  SC proteins

Protein           Functional        Total
                  domains (a)      size, aa

Hop1 Sc           HORMA              605

Red1Sc            Rec10/Red1         827

Hop1 Sp,          RING finger        528
a linear
element
component

Rec10 Sp,         Rec10/Red1         791
a linear
element
component

ASY1 At           HORMA, SWIRM       596

ASY2 At           HORMA              1399

C(2)M Dm          Rad21_Rec8_N       570
                  cohesin domain

HIM-3 Ce          HORMA              291

SYCP2 Dr          --                 995

SYCP3-like Dr     COR1               240

SC65 Dr, a SC     Bacterial          426
protein           rpoC2_cyan

SYCP2 Mm          Bacterial          1500
                  COG4399

SYCP3 Mm          COR1               254

SC65 Mm, a SC     --                 443
protein

FKBP6 Mm,         FKBP.C, TPR        327
peptidyl-prolyl
cis-trans
isomerase

(a) According to the CDART output.

(b) The model organisms are designated as in Table 1. See protein
IDs in Table 1.

The SMC, Smc, SCP-1, COR1, and RAD21 domains are characteristic
of structural chromosome proteins. The HORMA domain recognizes
the chromatin state and facilitates the interactions with other
proteins. PRK00409 is involved in recombination. Cis-trans
isomerases catalyze the isomerization of protein molecules having
double bonds. The other domains are not related to meiosis.

TABLE 3: SC proteins similar to proteins from the proteomes of
algae, mosses, fungi, and green plants.

Eukaryotic taxa        Total proteins
                        in the NCBI

                        database (a)

Chlorophyta                156803
(green algae
and
[Yiridiplantae])

Phaeophyceae               27435
(brown algae
and
[Stramenopiles])

Bryophyta,                 95921
Anthocerotophyta,
and Marchantiophyta
(mosses and
[Yiridiplantae])

Lycopodiophyta             71720
([Viridiplantae] and
Trachaeophyta)

Euphyllophyta             2066225
([Viridiplantae] and
Trachaeophyta)

Microsporidia              20596
(unicellular lower
fungi and
[Opisthokonta])

Blastocladiomycota,        12709
Chytridiomycota,
Glomeromycota, and
Fungi insertae sedis
(Zygomycota) (lower
fungi and
[(Opisthokonta)]

Ascomycota                1819825
[(Opisthokonta)]-
higher fungi

Basidiomycota              461746
[(Opisthokonta)] and
higher fungi

Eukaryotic taxa           Proteins of the SC central space

                       1                  2

                       From animals (#)   From plants and
                                          fungi (#)

Chlorophyta            SYCP1 Mm (50)      Low similarity
(green algae
and
[Yiridiplantae])

Phaeophyceae           SYCP1 Mm (53)      Low similarity
(brown algae
and
[Stramenopiles])

Bryophyta,             Low similarity     Low similarity
Anthocerotophyta,
and Marchantiophyta
(mosses and
[Yiridiplantae])

Lycopodiophyta         Low similarity     [ZYPla At (111),
([Viridiplantae] and                      ZYPlb At (112)]
Trachaeophyta)

Euphyllophyta          Low similarity     [ZYP1 annotated
([Viridiplantae] and                      for various
Trachaeophyta)                            species] (b)

Microsporidia          Low similarity     Low similarity
(unicellular lower
fungi and
[Opisthokonta])

Blastocladiomycota,    Low similarity     Low similarity
Chytridiomycota,
Glomeromycota, and
Fungi insertae sedis
(Zygomycota) (lower
fungi and
[(Opisthokonta)]

Ascomycota             SYCP1 Mm (50),     Low similarity (b)
[(Opisthokonta)]-      SYCP1 Dr (51)
higher fungi

Basidiomycota          Low similarity     Low similarity
[(Opisthokonta)] and
higher fungi

Eukaryotic taxa             Lateral element proteins and
                                   other SC proteins

                       3                    4

                       From plants          From
                       and fungi (#)        animals (#)

Chlorophyta            [ASY2 At (117)],     HIM-3 Ce (54),
(green algae           [ASY1 At (163)],     FKBP6 Mm (87)
and                    Hopl Sc (99)
[Yiridiplantae])

Phaeophyceae           ASY2 At (65),        FKBP6 Mm (85)
(brown algae           [ASY1 At (124)],
and                    Hopl Sc (71), Hopl
[Stramenopiles])       annotated for
                       Ectocarpus
                       siliculosus

Bryophyta,             [ASY2 At (183)],     [FKBP6 Mm (104)]
Anthocerotophyta,      [ASY1 At (278)],
and Marchantiophyta    Hopl Sc (86)
(mosses and
[Yiridiplantae])

Lycopodiophyta         [ASY2 At (197)],     SYCP2 Mm (60),
([Viridiplantae] and   [ASY1 At (291)],     [FKBP6 Mm (106)]
Trachaeophyta)         Hopl Sc (96)

Euphyllophyta          [ASY1 annotated      [FKBP6 Mm (115)]
([Viridiplantae] and   for] Brassica
Trachaeophyta)         oleracea; (b)
                       [Hopl Sc (100)]

Microsporidia          ASY1 At (53),
(unicellular lower     Hopl Sp (50),
fungi and              Hopl Sc (55)
[Opisthokonta])

Blastocladiomycota,    ASY2 At (87),        [FKBP6 Mm (102)]
Chytridiomycota,       [ASY1 At (126),
Glomeromycota, and     Hopl Sc (106)]
Fungi insertae sedis
(Zygomycota) (lower
fungi and
[(Opisthokonta)]

Ascomycota             ASY2 At (75),        HIM-3 Ce (50),
[(Opisthokonta)]-      [ASY1 At (100)],     FKBP6 Mm (77)
higher fungi           Hopl-like
                       annotated (b)

Basidiomycota          ASY2 At (85),        HIM-3 Ce (56),
[(Opisthokonta)] and   [ASY1 At (123)],     FKBP6 Mm (72)
higher fungi           Hopl Sp (74),
                       [Hopl Sc (141)]

(a) As of the time of study start (September 2011).

(b) Similarity with cognate proteins is not shown.

Maximal scores are indicated in parentheses. Proteins with high
scores (100 and higher) are in bold. The model organisms are
designated as in Table 1.

(#) Hereinafter: SC proteins from animals are those of Dm, Ce,
Dr, Mm, and from fungi and plants those of Sc, Sp, and At.

Note: Proteins with high scores (100 and higher) are indicated
with []

TABLE 4: SC proteins with similarities to proteins from the
proteomes of unicellular eukaryotes.

Eukaryotic      Total proteins      Proteins of the SC central space
taxa             in the NCBI
                 database (a)
                                         1                   2
                                   From animals         From plants
                                                         and fungi

Parabasalia +       174018        Low similarity       ZYPla At (50)
Fornicata ++
Heterolobosea
(primitive
unicellular
eukaryotes)

Apicomplexa         241035        SYP-1 Ce (57),      ZYPlb At (59),
(sporozoans                      SYCP1 Mm (67) (c)   ZYPla At (60) (c)
of the group
Alveolata)

Ciliophora          144165         SYCP1 Dr (60)       ZYPlb At (51)
(infusoria,
Alveolata)

Euglenozoa          187312         SYCP1 Mm (56)      Low similarity
(euglenic
protozoans)

Choano-             30401         C(3)G Dm (57),      ZYPla At (52),
flagellata                         SYCP1 Mm (65)      ZYPlb At (61),
                                                       Zipl Sc (52)

Eukaryotic           Lateral element proteins and other
taxa                            SC proteins

                         3                      4
                    From plants            From animals
                     and fungi

Parabasalia +   ASY2 At (107), ASY1    HIM-3 Ce (55), SYCP2
Fornicata ++     At (194), Hopl Sc           Mm (51)
Heterolobosea       (104), Hopl
(primitive         annotated for
unicellular     Giardia intestinalis
eukaryotes)      and Hopl-like, for
                    Trichomonas
                     vaginalis

Apicomplexa     ASY2 At (107), ASY1       FKBP6 Mm (133)
(sporozoans      At (148), Hopl Sc
of the group            (99)
Alveolata)

Ciliophora         Low similarity         FKBP6 Mm (114)
(infusoria,
Alveolata)

Euglenozoa       ASY2 At (91), ASY1    HIM-3 Ce (52), FKBP6
(euglenic        At (115), Hopl Sc           Mm (78)
protozoans)             (94)

Choano-          ASY1 At (78), Hopl    SYCP2 Mm (53), FKBP6
flagellata            Sc (56)                Mm (76)

(a) As of the time of study (November 2011-November 2012).

(c) These scores (with E-value = [5e.sup.-08]) approximate the
scores obtained for the random analogs of the SC proteins (E-
value = [5e.sup.-04]) (italicized). Other designations are as in
Table 3.

TABLE 5: SC proteins with similarities to proteins from the
proteomes of multicellular eukaryotes.

Eukaryotic taxa           Total
                       proteins in
                         the NCRT
                       database (a)

Porifera and              16445
Placozoa (sponges,
placozoans, and
Metazoa)

Coelenterates:            81390
Cnidaria (stingers),
Ctenophora (sea
walnuts), and
Eumetazoa

Platyhelminthes           81455
(flat worms,
Eumetazoa,
Bilateria, and
Acoelomata)

Nematoda (round           297231
worms, Bilateria,
Coelomata, and
Protostomia)

Mollusca                  121831
(Protostomia)

Chelicerata               125005
(Panarthropoda 2 and
Protostomia)

Mandibulata              1624768
(Panarthropoda 3 and
Protostomia)

Eukaryotic taxa             Proteins of the SC central space

                                1                     2
                           From animals          From plants
                                                  and fungi

Porifera and            SYP-1 Ce (56) (c),    ZYPla At (83) (c),
Placozoa (sponges,      C(3)G Dm (70) (c),    ZYPlb At (64) (c),
placozoans, and         SYCP1 Dr (66)(c),      Zipl Sc (72) (c)
Metazoa)                SYCP1 Mm (88) (c)

Coelenterates:         SYCE2 Dr (52), SYCE2     Low similarity
Cnidaria (stingers),         Mm (63)
Ctenophora (sea
walnuts), and
Eumetazoa

Platyhelminthes           SYCP1 Mm (53)         Low similarity
(flat worms,
Eumetazoa,
Bilateria, and
Acoelomata)

Nematoda (round        C(3)G Dm (50), SYCP1     ZYPla At (52),
worms, Bilateria,       Dr (51), SYCP1 Mm        Zipl Sc (50)
Coelomata, and               (50) (b)
Protostomia)

Mollusca                C(3)G Dm (68) (c),    ZYPlb At (71) (c),
(Protostomia)           SYP-1 Ce (68) (c),    ZYPla At (81) (c),
                        SYCP1 Dr (64) (c),     Zipl Sc (77) (c)
                        SYCP1 Mm (99) (c),
                          SYCE2 Mm (51)

Chelicerata               Low similarity        Low similarity
(Panarthropoda 2 and
Protostomia)

Mandibulata            Low similarity apart     Low similarity
(Panarthropoda 3 and       from cognate
Protostomia)               proteins (b)

Eukaryotic taxa               Lateral element proteins and
                                    other SC proteins

                                3                     4
                          From plants            From animals
                            and fungi

Porifera and           ASY2 At (76), ASY1    HIM-3 Ce (56), SC65
Placozoa (sponges,      At (137), Hopl Sc     Dr (102), SC65 Mm
placozoans, and               (71)           (110), SYCP3-like Dr
Metazoa)                                       (112), SYCP3 Mm
                                               (116), FKBP6 Mm
                                             (208), SCP3(SYCP3)-
                                              like annotated for
                                                  Amphimedon
                                                queenslandica

Coelenterates:         ASY2 At (78), ASY1    HIM-3 Ce (68), SC65
Cnidaria (stingers),    At (137), Hopl Sc     Mm (100), SC65 Dr
Ctenophora (sea               (82)           (105), SYCP3-like Dr
walnuts), and                                  (143), SYCP3 Mm
Eumetazoa                                      (148), FKBP6 Mm
                                              (194), SYCP3-like
                                             annotated for Hydra
                                                magnipapillata

Platyhelminthes        ASY1 At (105), ASY2   HIM-3 Ce (68), SYCP2
(flat worms,            At (62), Hopl Sc      Mm (53), FKBP6 Mm
Eumetazoa,                    (57)                  (138)
Bilateria, and
Acoelomata)

Nematoda (round        Hopl Sc (75), ASY2    SC65 Dr (123), SC65
worms, Bilateria,       At (86), ASY1 At      Mm (130), FKBP6 Mm
Coelomata, and                (124)          (77), SC65 annotated
Protostomia)                                 for Ascaris suum and
                                              HIM-3, for several
                                                Caenorhabditis
                                               species (maximal
                                                 score = 43)b

Mollusca               ASY1 At (89), Hopl    SC65 Dr (57), SYCP3-
(Protostomia)                Sc (55)         like Dr (199), SC65
                                              Mm (66), SYCP2 Mm
                                                (80), FKBP6 Mm
                                               (171), SYCP3 Mm
                                               (197), SYCP2 and
                                             SYCP3 annotated for
                                              Crassostrea gigas

Chelicerata              Low similarity       SC65 Dr (88), SC65
(Panarthropoda 2 and                          Mm (99), FKBP6 Mm
Protostomia)                                        (179)

Mandibulata            ASY1 At (63), Hopl    SC65 Dr (143), FKBP6
(Panarthropoda 3 and    Sp (55), Hopl Sc      Mm (156), SC65 Mm
Protostomia)                  (60)                  (169)b

(a) As of the time of study (October 2012-April 2013).

(b) Similarity with cognate proteins is not shown.

(c) These scores (with E-values ranging from [3e.sup.-10] to
[2e.sup.-20]) approximate the scores obtained for the random
analogs of the SC proteins (E-values ranging from [2e.sup.-04] to
[le.sup.-11]) (italicized).

Other designations are as in Table 3.

TABLE 6: SC proteins of the model organisms with similarities to
proteins from the proteomes of Deuterostomia.

Eukaryotic taxa       Total proteins
                       in the NCBI
                       database (a)

Echinodermata             41869
(Deuterostomia 1)

Elemichordata,            14118
Xenoturbellida, and
Chaetognatha
(Deuterostomia 2)

Cephalochordata           60054
(Deuterostomia 3)

Tunicata                  51435
(Deuterostomia,
Chordata)

Actinopterygii            451775
(Chordata,
Vertebrata, and
Teleostomi)

Amphibia                  162402
(Vertebrata,
Teleostomi)

Sauropsida                372873
(Vertebrata,
Teleostomi)

Mammalia                 2272182
(Yertebrata,
Teleostomi)

Eukaryotic taxa             Proteins of the SC central space

                               1                      2
                          From animals         From plants and
                                                    fungi

Echinodermata         SYCE2 Dr (50), SYCE2   ZYPlb At (65), ZYPla
(Deuterostomia 1)      Mm (68), SYCP1 Mm         At (74) (c)
                       (76) (c), C(3)G Dm
                      (63), SYP-1 Ce (59),
                      SYCE2-like annotated
                              for
                       Strongylocentrotus
                           purpuratus

Elemichordata,         SYCP1 Mm (69) (c),     ZYPlb At (53) (c),
Xenoturbellida, and   C(3)G Dm (68), SYP-     ZYPla At (56) (c),
Chaetognatha               1 Ce (50)             Zipl Sc (70)
(Deuterostomia 2)

Cephalochordata        SYCP1 Dr (69 (d)),     ZYPla At (68 (d)),
(Deuterostomia 3)     SYCE2 Mm (72), SYCP1      ZYPlb At (69)
                       Mm (81 (d)), C(3)G
                          Dm (59 (d))

Tunicata              SYCP1 Dr (55), SYCP1   ZYPla At (57), ZYPlb
(Deuterostomia,        Mm (57), C(3)G Dm           At (66)
Chordata)                     (57)

Actinopterygii        TEX12 Mm (57), SYCE2   ZYPla At (57), Zipl
(Chordata,             Mm (67), SYCES Mm           Sc (56)
Vertebrata, and       (73), SYCE1 Mm (84),
Teleostomi)           SYCP1 Mm (320) (b),
                      C(3)G Dm (59), SYP-
                           1 Ce (50)

Amphibia              SYCEl-like Dr (50),       Low similarity
(Vertebrata,          TEX12 Af (56), TEX12
Teleostomi)            Mm (72), SYCE2 Mm
                      (84), SYCE1 Mm (93),
                        SYCE3 Mm (110);
                       SYCEl-like, SYCE2-
                        like, TEX12-like
                         annotated for
                       Xenopus tropicalis

Sauropsida            TEX12 Af (60), SYCE2       Zipl Sc (50)
(Vertebrata,          Dr (63), SYCEl-like
Teleostomi)            Dr (72), TEX12 Mm
                        (117), SYCE2 Mm
                        (129), SYCE3 Mm
                        (139), SYCE1 Mm
                        (154), SYCP1 Dr
                        (196), SYCP1 Mm
                        (394), C(3)G Dm
                       (52), SYCPl-like,
                       SYCEl-like, SYCE2-
                       like, SYCE3-like,
                      TEX12-like annotated
                        for various bird
                            species

Mammalia              TEX12 Af (64), SYCE2      Low similarity
(Yertebrata,          Dr (68), SYCEl-like
Teleostomi)            Dr (86), SYCP1 Dr
                       (226) (b), SYCP1,
                      SYCE1, SYCE2, SYCES,
                      TEX12 annotated for
                        various species

Eukaryotic taxa           Lateral element proteins and other
                                      SC proteins

                               3                     4
                        From plants and         From animals
                             fungi

Echinodermata         ASY2 At (69), ASY1      FKBP6 Mm (104),
(Deuterostomia 1)     At (125), Elopl Sc      SYCP2 Mm (118),
                             (75)           SYCP3-like Dr (157),
                                            SYCP3 Mm (169), SC65
                                             Dr (176), SC65 Mm
                                              (179), SCP3-like
                                               annotated for
                                             Strongylocentrotus
                                                 purpuratus

Elemichordata,        ASY2 At (59), ASY1    FKBP6 Mm (95), SC65
Xenoturbellida, and   At (121), Elopl Sc     Dr (177), SC65 Mm
Chaetognatha                 (85)             (182), leprecan-
(Deuterostomia 2)                             like = SC65-like
                                               annotated for
                                                Saccoglossus
                                                kowalevskii

Cephalochordata       ASY2 At (50d), ASY1     SYCP2 Mm (115),
(Deuterostomia 3)     At (87d), Elopl Sc    FKBP6 Mm (125), SC65
                             (52d)           Dr (127), SC65 Mm
                                            (144), SYCP3-like Dr
                                              (193), SYCP3 Mm
                                                   (194)

Tunicata                Low similarity        SYCP3 Mm (136),
(Deuterostomia,                             SYCP3-like Dr (140),
Chordata)                                   SC65 Mm (150), SC65
                                             Dr (153), FKBP6 Mm
                                             (175), similar to
                                            SCP3-like annotated
                                                 for Ciona
                                              intestinalis and
                                            leprecan = SC65, for
                                            Molgula tectiformis

Actinopterygii        ASY2 At (70), ASY1      SYCP3 Mm (263),
(Chordata,            At (119), Elopl Sc      FKBP6 Mm (321),
Vertebrata, and              (81)           SYCP2 Mm (343), SC65
Teleostomi)                                 Mm (471)b, E1IM-3 Ce
                                              (73), SC65-like
                                               annotated for
                                            various fish species

Amphibia              ASY2 At (82), ASY1       SYCP2 Dr (50),
(Vertebrata,               At (117)         SYCP3-like Dr (272),
Teleostomi)                                   SYCP3 Mm (307),
                                              FKBP6 Mm (402),
                                            SYCP2 Mm (410), SC65
                                             Dr (464), SC65 Mm
                                              (523), HIM-3 Ce
                                              (63), SYCP2 and
                                            SYCP3 annotated forX
                                             tropicalis, SYCP2-
                                            like and SYCP3, for
                                                X. laevis-,
                                            leprecan-like = SC65
                                             precursor, for X.
                                               tropicalis, X.
                                                   laevis

Sauropsida            ASY2 At (90), ASY1       SYCP2 Dr (57),
(Vertebrata,               At (124)         SYCP3-like Dr (275),
Teleostomi)                                   SYCP3 Mm (346),
                                            FKBP6 Mm (387), SC65
                                             Dr (484), SYCP2 Mm
                                               (498), SC65 Mm
                                              (574), HIM-3 Ce
                                             (74), SYCP2-like,
                                              SCP3, SC65-like
                                                 annotated

Mammalia              ASY2 At (84), ASY1      SYCP2 Dr (149),
(Yertebrata,          At (119), Elopl Sc    SYCP3-like Dr (275),
Teleostomi)                  (78)           SC65 Dr (489)b, HIM-
                                             3 Ce (79), SYCP2,
                                                SYCP3, SC65
                                               annotated for
                                              various species

(a) As of the time of study start (January-February 2013).

(b) Similarity with cognate proteins is not shown.

(c) These scores (with E-values ranging from [6e.sup.-07] to
[le.sup.-13]) approximate the scores obtained for the random
analogs of the SC proteins (E-values ranging from [e.sup.-04] to
[4e.sup.-08]) (italicized).

(d) The same proteins (different in different cells of the table)
from several proteomes under study showed a maximal similarity to
the native protein indicated.

Other designations are as in Table 3.

TABLE 7: SC proteins with highest scores and corresponding
eukaryotic taxa.

SC proteins      Maximal     Corresponding taxa (b)
                scores (a)

                Proteins of the SC central space

SYCP1 Mm (c)     320, 394    Actinopterygii, Sauropsida

SYCE3 Mm         110, 139    Amphibia, Sauropsida

SYCE1, SYCE2,    117-154     Sauropsida
and TEX12 Mm

SYCP1 Dr         196, 226    Sauropsida, Mammalia

ZYP1a and        111-112     Lycopodiophyta
ZYP1b At

                Lateral element proteins and other
                SC proteins

ASY1 At          > = 100     Algae, Fungi, Parabasalia+,
                             Apicomplexa, Euglenozoa,
                             Porifera, Placozoa,
                             Coelenterates,
                             Platyhelminthes, Nematoda,
                             Deuterostomia 1 and 2, and all
                             Vertebrata

ASY1 At          278, 291    Mosses, Lycopodiophyta

ASY2 At          > = 100     Chlorophyta, Parabasalia+, and
                             Apicomplexa

ASY2 At          183,197     Mosses, Lycopodiophyta

Hop1 Sc          > = 100     Euphyllophyta, lower fungi,
                             and Parabasalia+

Hop1 Sc            141       Basidiomycota

SC65 Mm and      > = 100     Porifera, Placozoa,
SC65 Dr                      Coelenterates, Nematoda,
                             Mandibulata, and all
                             Deuterostomia

SC65 Mm          523, 574    Amphibia, Sauropsida

SC65 Dr          484, 489    Sauropsida, Mammalia

SYCP3 Mm and     > = 100     Porifera, Placozoa,
SYCP3-like Dr                Coelenterates, Mollusca,
                             Echinodermata, and
                             Cephalochordata, Tunicata, all
                             Vertebrata

SYCP3 Mm         343, 346    Actinopterygii, Sauropsida

SYCP3-like Dr      275       Sauropsida, Mammalia

SYCP2 Mm         > = 100     Echinodermata,
                             Cephalochordata,
                             Actinopterygii, and Amphibia

SYCP2 Mm           498       Sauropsida

SYCP2 Dr           149       Mammalia

(a) Similarity with cognate proteins is not shown.

(b) For details see corresponding tables.

(c) The model organisms are designated as in Table 1.
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Title Annotation:Research Article
Author:Grishaeva, Tatiana M.; Bogdanov, Yuri F.
Publication:International Journal of Evolutionary Biology
Article Type:Report
Date:Jan 1, 2014
Words:10182
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