doi: 10.1155/2014/856230. Epub 2014 Jul 23.
Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes
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- PMID:25147749
- PMCID: PMC4132317
- DOI: 10.1155/2014/856230
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Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes
Tatiana M Grishaeva et al. Int J Evol Biol.2014.
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Abstract
The problems of the origin and evolution of meiosis include the enigmatic variability of the synaptonemal complexes (SCs) which, being morphology similar, consist of different proteins in different eukaryotic phyla. Using bioinformatics methods, we monitored all available eukaryotic proteomes to find proteins similar to known SC proteins of model organisms. We found proteins similar to SC lateral element (LE) proteins and possessing the HORMA domain in the majority of the eukaryotic taxa and assume them the most ancient among all SC proteins. Vertebrate LE proteins SYCP2, SYCP3, and SC65 proved to have related proteins in many invertebrate taxa. Proteins of SC central space are most evolutionarily variable. It means that different protein-protein interactions can exist to connect LEs. Proteins similar to the known SC proteins were not found in Euglenophyta, Chrysophyta, Charophyta, Xanthophyta, Dinoflagellata, and primitive Coelomata. We conclude that different proteins whose common feature is the presence of domains with a certain conformation are involved in the formation of the SC in different eukaryotic phyla. This permits a targeted search for orthologs of the SC proteins using phylogenetic trees. Here we consider example of phylogenetic trees for protozoans, fungi, algae, mosses, and flowering plants.
Figures
Phylogenetic tree of algae, fungi, mosses, and green plants based on proteins similar to Hop1/ASY1 in proteomes of these organisms found with the use of maximal scores. The initial set of proteins used to construct the fast minimum evolution tree included RefSeq: XP_002957345 (Volvox carteri, Chlorophyta); GenBank: CBN75586, annotated as Hop1 homolog (Ectocarpus siliculosus, Phaeophyceae); RefSeq: XP_002995702 (Nosema ceranae, Microsporidia); GenBank: EGF80506 (Batrachochytrium dendrobatidis, Chytridiomycota); RefSeq: NP_012193.1, SC protein Hop1 (Saccharomyces cerevisiae, Ascomycota); GenBank: GAA98305 (Mixia osmundae, Basidiomycota); RefSeq: XP_001760173 (Physcomitrella patens, Bryophyta); RefSeq: XP_002969766 (Selaginella moellendorffii, Lycopodiophyta); RefSeq: NP_564896.1, SC protein ASY1 (Arabidopsis thaliana, Euphyllophyta). The archaeal protein RefSeq: YP_003707339.1 (Methanococcus voltae, Archaea) was taken as control. Only species and higher taxa are indicated on the tree. Three proteins (from Archaea, Microsporidia, and Ascomycota) were automatically removed from the final version of the tree. The evolutionary distance between two sequences was modeled as expected fraction of amino acid substitutions per site given the fraction of mismatched amino acids in the aligned region (according to [43]).
Phylogenetic tree of Hop1/ASY1-similar proteins found in the proteomes of unicellular eukaryotes. The initial set of proteins used to construct the fast minimum evolution tree included RefSeq: NP_012193.1, SC protein Hop1 (Saccharomyces cerevisiae, Ascomycota); RefSeq: NP_564896.1, SC protein ASY1 (Arabidopsis thaliana, Euphyllophyta); RefSeq: XP_001321336 (Trichomonas vaginalis, Parabasalia); RefSeq: XP_002675215 (Naegleria gruberi, Heterolobosea); GenBank: EET02094, annotated as Hop1 homolog (Giardia intestinalis, Fornicata); RefSeq: XP_626119 (Cryptosporidium parvum, Apicomplexa); GenBank: CCC51501 (Trypanosoma vivax, Euglenozoa); RefSeq: XP_001742099 (Monosiga brevicollis, Choanoflagellata). The archaeal protein RefSeq: YP_003707339.1 (Methanococcus voltae, Archaea) was taken as control. Only species and higher taxa are indicated on tree. Two proteins (from Archaea and Choanoflagellata) were automatically removed from the final version of the tree. The evolutionary distance between two sequences was modeled as expected fraction of amino acid substitutions per site given the fraction of mismatched amino acids in the aligned region (according to [43]).
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References
- Cavalier-Smith T. Origins of the machinery of recombination and sex. Heredity. 2002;88(2):125–141. - PubMed
- Li W, Zheng G-C. A resurgent phoenix—a hypothesis for the origin of meiosis. IUBMB Life. 2002;54(1):9–12. - PubMed
- Ramesh MA, Malik S, Logsdon JM., Jr. A phylogenomic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Current Biology. 2005;15(2):185–191. - PubMed
- Bogdanov YF, Grishaeva TM, Dadashev SY. Similarity of the domain structure of proteins as a basis for the conservation of meiosis. International Review of Cytology. 2007;257:83–142. - PubMed
- Egel R, Penny D. On the origin of meiosis in eukaryotic evolution: coevolution of meiosis and mitosis from feeble beginnings. In: Egel R, Lankenau D-H, editors. Genome Dynamics and Stability. Vol. 3. Berlin, Germany: Springer; 2007. pp. 249–288.
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