Conservation and Variability of Synaptonemal Complex Proteins in Phylogenesis of Eukaryotes

Grishaeva, T. M.; Bogdanov, Yu. F.

doi:10.1155/2014/856230

Cited by 42 publications

(36 citation statements)

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“…Although SC proteins are evolutionarily variable and share only a low similarity [51], the obvious loss of the synaptonemal complex (SC) components SYP-1/2/3/4, may not be compatible with homologous chromosome pairing in D. coronatus. …”

Section: Resultsmentioning

confidence: 99%

Genome analysis of Diploscapter coronatus: insights into molecular peculiarities of a nematode with parthenogenetic reproduction

et al. 2017

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BackgroundSexual reproduction involving the fusion of egg and sperm is prevailing among eukaryotes. In contrast, the nematode Diploscapter coronatus, a close relative of the model Caenorhabditis elegans, reproduces parthenogenetically. Neither males nor sperm have been observed and some steps of meiosis are apparently skipped in this species. To uncover the genomic changes associated with the evolution of parthenogenesis in this nematode, we carried out a genome analysis.ResultsWe obtained a 170 Mbp draft genome in only 511 scaffolds with a N50 length of 1 Mbp. Nearly 90% of these scaffolds constitute homologous pairs with a 5.7% heterozygosity on average and inversions and translocations, meaning that the 170 Mbp sequences correspond to the diploid genome. Fluorescent staining shows that the D. coronatus genome consists of two chromosomes (2n = 2). In our genome annotation, we found orthologs of 59% of the C. elegans genes. However, a number of genes were missing or very divergent. These include genes involved in sex determination (e.g. xol-1, tra-2) and meiosis (e.g. the kleisins rec-8 and coh-3/4) giving a possible explanation for the absence of males and the second meiotic division. The high degree of heterozygosity allowed us to analyze the expression level of individual alleles. Most of the homologous pairs show very similar expression levels but others exhibit a 2–5-fold difference.ConclusionsOur high-quality draft genome of D. coronatus reveals the peculiarities of the genome of parthenogenesis and provides some clues to the genetic basis for parthenogenetic reproduction. This draft genome should be the basis to elucidate fundamental questions related to parthenogenesis such as its origin and mechanisms through comparative analyses with other nematodes. Furthermore, being the closest outgroup to the genus Caenorhabditis, the draft genome will help to disclose many idiosyncrasies of the model C. elegans and its congeners in future studies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3860-x) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Genome analysis of Diploscapter coronatus: insights into molecular peculiarities of a nematode with parthenogenetic reproduction

et al. 2017

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“…To overcome this and resolve individual haplotypes, we amplified, cloned and Sanger sequenced the coding regions of the eight meiosis genes from diploid A. arenosa SNO and A. lyrata PER populations, tetraploid A. arenosa, SEN, TBG and WEK populations, as well as A. lyrata KAG and MAU populations. This approach provided high-resolution sequence polymorphism data for a total of three hundred and twenty cDNA transcripts, consisting of fifty-eight alleles with an average of seven alleles for each of the eight meiosis genes, thus allowing us to detect both structural variation including indels and divergent SNP variation conserved at the secondary and tertiary amino acid level, rather than at the primary sequence [29]. It is therefore difficult to infer functional or non-functional amino acid polymorphisms with complete confidence, but results from KinasePhos2.0 and NetPhos3.1 suggest that overall 45% of those we detect were either loss or gain of putative serine/threonine phosphosites and 55% were nonphosphosites.…”

Section: Adaptive Polymorphisms In Meiosis Genesmentioning

confidence: 99%

A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

Seear

Gregory

Heavens

et al. 2019

Preprint

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In this study we performed a genotype-phenotype association analysis of meiotic stability in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations collected from the Wachau region and East Austrian Forealps. The aim was to determine the effect of eight meiosis genes under extreme selection upon adaptation to whole genome duplication. Individual plants were genotyped by high-throughput sequencing of the eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation and phenotyped by assessing meiotic metaphase I chromosome configurations. Our results reveal that meiotic stability varied greatly (20-100%) between individual tetraploid plants and was associated with segregation of a novel allele orthologous to the budding yeast RED1 chromosome axis protein, Asynapsis3 (ASY3), derived from A. lyrata. The adaptive ASY3 protein possesses a putative in-frame tandem duplication (TD) of a serinerich region upstream of the coiled-coil domain that has arisen at sites of DNA microhomology. The frequency of multivalents observed in plants homozygous for the ASY3 TD haplotype was significantly lower than plants heterozygous for TD/ND (non-duplicated) ASY3 haplotypes. Chiasma distribution was significantly altered in the stable plants compared to the unstable plants with a shift from proximal and interstitial to predominantly distal locations. The number of HEI10 foci at pachtyene that mark class I crossovers was significantly reduced in meiotic nuclei from ASY3 TD homozygous plants compared to ASY3 ND/TD heterozygotes, indicating an adaptive consequence of the ASY3 TD allele.From the ten populations, fifty-eight alleles of these 8 meiosis genes were identified, demonstrating dynamic population variability at these loci which nevertheless exhibit signatures of strong hard selective sweeps. Widespread chimerism between alleles originating from A. lyrata/A. arenosa and diploid/tetraploids indicates that this group of rapidly evolving genes provide precise adaptive control over meiotic recombination in the tetraploids, the very process that gave rise to them. | P a g e Author summaryWhole genome duplication can promote adaptability, but is a dramatic mutation usually resulting in meiotic catastrophe and genome instability. Here we focus on a case of coordinated stabilization of meiotic recombination in ten autotetraploid Arabidopsis lyrata and A. lyrata/A. arenosa hybrid populations from the Wachau region and East Austrian Forealps. We fuse population genomic data with a genotype-phenotype association study, concentrating on the effects of eight meiosis genes (ASY1, ASY3, PDS5b, PRD3, REC8, SMC3, ZYP1a/b) implicated in synaptonemal complex formation in the tetraploids under extreme selection. Our analysis demonstrates that a novel allele of the meiotic chromosome axis protein Asynapsis3 that contains an in-frame duplication of a serine-rich region is the major determinant of male meiotic stability. This adaptive restabilisation appears to be achieved by a...

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“…(Marcon & Moens, 2005; Egel & Penny, 2007; Bogdanov, Grishaeva & Dadashev, 2007; Grishaeva & Bogdanov, 2014). The objective of our work is accordingly to analyze the structural features of meiotic SGOs by a set of bioinformatical methods, such as COBALT, CDART, MEME, COILS program, Mobile portal—charge, and Compute pI/Mw tool.…”

Section: Introductionmentioning

confidence: 99%

Bioinformatical analysis of eukaryotic shugoshins reveals meiosis-specific features of vertebrate shugoshins

Grishaeva

Kulichenko

Bogdanov

2016

PeerJ

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BackgroundShugoshins (SGOs) are proteins that protect cohesins located at the centromeres of sister chromatids from their early cleavage during mitosis and meiosis in plants, fungi, and animals. Their function is to prevent premature sister-chromatid disjunction and segregation. The study focused on the structural differences among SGOs acting during mitosis and meiosis that cause differences in chromosome behavior in these two types of cell division in different organisms.MethodsA bioinformatical analysis of protein domains, conserved amino acid motifs, and physicochemical properties of 32 proteins from 25 species of plants, fungi, and animals was performed.ResultsWe identified a C-terminal amino acid motif that is highly evolutionarily conserved among the SGOs protecting centromere cohesion of sister chromatids in meiotic anaphase I, but not among mitotic SGOs. This meiotic motif is arginine-rich in vertebrates. SGOs differ in different eukaryotic kingdoms by the sets and locations of amino acid motifs and the number of α-helical regions in the protein molecule.DiscussionThese structural differences between meiotic and mitotic SGOs probably could be responsible for the prolonged SGOs resistance to degradation during meiotic metaphase I and anaphase I. We suggest that the “arginine comb” in C-end meiotic motifs is capable of interaction by hydrogen bonds with guanine bases in the minor groove of DNA helix, thus protecting SGOs from hydrolysis. Our findings support independent evolution of meiosis in different lineages of multicellular organisms.

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Conservation and Variability of Synaptonemal Complex Proteins in Phylogenesis of Eukaryotes

Cited by 42 publications

References 58 publications

Genome analysis of Diploscapter coronatus: insights into molecular peculiarities of a nematode with parthenogenetic reproduction

Genome analysis of Diploscapter coronatus: insights into molecular peculiarities of a nematode with parthenogenetic reproduction

A novel allele ofASY3promotes meiotic stability in autotetraploidArabidopsis lyrata

Bioinformatical analysis of eukaryotic shugoshins reveals meiosis-specific features of vertebrate shugoshins

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