A novel allele of ASY3 promotes meiotic stability in autotetraploid Arabidopsis lyrata

AbstractIn 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 serine-rich 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.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 reduction in the number of meiotic crossovers as well as a shift in their positioning towards the chromosome ends. Of the eight genes, fifty-eight alleles were identified, indicating dynamic population variability at these loci under extreme selection. In addition, widespread allelic 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.

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A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata

PLoS Genetics ◽

10.1371/journal.pgen.1008900 ◽

2020 ◽

Vol 16 (7) ◽

pp. e1008900

Author(s):

Paul J. Seear ◽

Martin G. France ◽

Catherine L. Gregory ◽

Darren Heavens ◽

Roswitha Schmickl ◽

...

Keyword(s):

Arabidopsis Lyrata ◽

Meiotic Stability ◽

Novel Allele

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Interspecific introgression mediates adaptation to whole genome duplication

10.1101/636019 ◽

2019 ◽

Cited By ~ 1

Author(s):

Sarah Marburger ◽

Patrick Monnahan ◽

Paul J. Seear ◽

Simon H. Martin ◽

Jordan Koch ◽

...

Keyword(s):

Gene Flow ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Whole Genome ◽

Arabidopsis Lyrata ◽

Cellular Processes ◽

Interspecific Introgression ◽

Gene Coding ◽

Genomic Study ◽

Meiotic Stability

AbstractAdaptive gene flow is a consequential evolutionary phenomenon across all kingdoms of life. While recognition of widespread gene flow is growing, examples lack of bidirectional gene flow mediating adaptations at specific loci that cooperatively manage core cellular processes. We previously described concerted molecular changes among physically interacting members of the meiotic machinery controlling crossover number and distribution upon adaptation to whole genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that escape from extinction following the trauma of WGD was mediated by adaptive gene flow between A. arenosa and its congener Arabidopsis lyrata. We show that A. lyrata underwent WGD more recently than A. arenosa, indicating that specific pre-adapted alleles donated by A. arenosa underwent selection and rescued the nascent A. lyrata tetraploids from early extinction. At the same time, we detect specific signals of gene flow in the opposite direction at other functionally interacting gene coding loci that display dramatic signatures of selective sweep in both tetraploid species. Cytological analysis shows that A. lyrata tetraploids exhibit similar levels of meiotic stability as A. arenosa tetraploids. Taken together, these data indicate that bidirectional gene flow allowed for an escape from extinction of the young autopolyploids, especially the rare tetraploid A. lyrata, and suggest that the merger of these species is greater than the sum of their parts.

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A conserved filamentous assembly underlies the structure of the meiotic chromosome axis

eLife ◽

10.7554/elife.40372 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 26

Author(s):

Alan MV West ◽

Scott C Rosenberg ◽

Sarah N Ur ◽

Madison K Lehmer ◽

Qiaozhen Ye ◽

...

Keyword(s):

Meiotic Recombination ◽

Budding Yeast ◽

Meiotic Chromosome ◽

Coiled Coil ◽

Chromosome Organization ◽

Molecular Architecture ◽

Master Regulators ◽

Core Proteins ◽

Protein Components ◽

Chromosome Axis

The meiotic chromosome axis plays key roles in meiotic chromosome organization and recombination, yet the underlying protein components of this structure are highly diverged. Here, we show that ‘axis core proteins’ from budding yeast (Red1), mammals (SYCP2/SYCP3), and plants (ASY3/ASY4) are evolutionarily related and play equivalent roles in chromosome axis assembly. We first identify ‘closure motifs’ in each complex that recruit meiotic HORMADs, the master regulators of meiotic recombination. We next find that axis core proteins form homotetrameric (Red1) or heterotetrameric (SYCP2:SYCP3 and ASY3:ASY4) coiled-coil assemblies that further oligomerize into micron-length filaments. Thus, the meiotic chromosome axis core in fungi, mammals, and plants shares a common molecular architecture, and likely also plays conserved roles in meiotic chromosome axis assembly and recombination control.

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Conserved HORMA domain-containing protein Hop1 stabilizes interaction between proteins of meiotic DNA break hotspots and chromosome axis

Nucleic Acids Research ◽

10.1093/nar/gkz754 ◽

2019 ◽

Vol 47 (19) ◽

pp. 10166-10180 ◽

Cited By ~ 2

Author(s):

Ryo Kariyazono ◽

Arisa Oda ◽

Takatomi Yamada ◽

Kunihiro Ohta

Keyword(s):

Fission Yeast ◽

Protein Interactions ◽

Meiotic Recombination ◽

Protein Protein Interactions ◽

Dna Double Strand Breaks ◽

Strand Breaks ◽

Multiple Protein ◽

Chromatin Immunoprecipitation Sequencing ◽

The One ◽

Chromosome Axis

Abstract HORMA domain-containing proteins such as Hop1 play crucial regulatory roles in various chromosomal functions. Here, we investigated roles of the fission yeast Hop1 in the formation of recombination-initiating meiotic DNA double strand breaks (DSBs). Meiotic DSB formation in fission yeast relies on multiple protein-protein interactions such as the one between the chromosome axial protein Rec10 and the DSB-forming complex subunit Rec15. Chromatin immunoprecipitation sequencing demonstrated that Hop1 is colocalized with both Rec10 and Rec15, and we observed physical interactions of Hop1 to Rec15 and Rec10. These results suggest that Hop1 promotes DSB formation by interacting with both axis components and the DSB-forming complex. We also show that Hop1 binding to DSB hotspots requires Rec15 and Rec10, while Hop1 axis binding requires Rec10 only, suggesting that Hop1 is recruited to the axis via Rec10, and to hotspots by hotspot-bound Rec15. Furthermore, we introduced separation-of-function Rec10 mutations, deficient for interaction with either Rec15 or Hop1. These single mutations and hop1Δ conferred only partial defects in meiotic recombination, while the combining the Rec15-binding-deficient rec10 mutation with hop1Δ synergistically reduced meiotic recombination, at least at a model hotspot. Taken together, Hop1 likely functions as a stabilizer for Rec15–Rec10 interaction to promote DSB formation.

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Ndj1, a Telomere-Associated Protein, Promotes Meiotic Recombination in Budding Yeast

Molecular and Cellular Biology ◽

10.1128/mcb.26.10.3683-3694.2006 ◽

2006 ◽

Vol 26 (10) ◽

pp. 3683-3694 ◽

Cited By ~ 40

Author(s):

Hsin-Yen Wu ◽

Sean M. Burgess

Keyword(s):

Meiotic Recombination ◽

Double Strand Breaks ◽

Homology Search ◽

Strand Breaks ◽

Homologous Chromosomes ◽

Synaptonemal Complex Formation ◽

Strand Invasion ◽

Double Holliday Junction ◽

Meiosis I

ABSTRACT Dynamic telomere repositioning is a prominent feature of meiosis. Deletion of a telomere-associated protein, Ndj1, results in the failure of both attachment and clustering of telomeres at the nuclear envelope and delays several landmarks of meiosis I, such as pairing, synaptonemal complex formation, and timing of the meiosis I division. We explored the role of Ndj1 in meiotic recombination, which occurs through the formation and repair of programmed double-strand breaks. The ndj1Δ mutation allows for the formation of the first detectable strand invasion intermediate (i.e., single-end invasion) with wild-type kinetics; however, it confers a delay in the formation of the double-Holliday junction intermediate and both crossover and noncrossover products. These results challenge the widely held notion that clustering of telomeres in meiosis promotes the ability of homologous chromosomes to find one another in budding Saccharomyces cerevisiae. We propose that an Ndj1-dependent function is critical for stabilizing analogous strand invasion intermediates that exist in two separate branches of the bifurcated pathway, leading to either noncrossover or crossover formation. These findings provide a link between telomere dynamics and a distinct mechanistic step of meiotic recombination that follows the homology search.

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Genome Duplication Increases Meiotic Recombination Frequency: A Saccharomyces cerevisiae Model

Molecular Biology and Evolution ◽

10.1093/molbev/msaa219 ◽

2020 ◽

Author(s):

Ou Fang ◽

Lin Wang ◽

Yuxin Zhang ◽

Jixuan Yang ◽

Qin Tao ◽

...

Keyword(s):

Saccharomyces Cerevisiae ◽

Meiotic Recombination ◽

Genome Stability ◽

Genome Duplication ◽

Genetic Recombination ◽

Recombination Frequency ◽

Abiotic Factors ◽

Strand Break ◽

Homologous Chromosomes ◽

Almost All

Abstract Genetic recombination characterized by reciprocal exchange of genes on paired homologous chromosomes is the most prominent event in meiosis of almost all sexually reproductive organisms. It contributes to genome stability by ensuring the balanced segregation of paired homologs in meiosis, and it is also the major driving factor in generating genetic variation for natural and artificial selection. Meiotic recombination is subjected to the control of a highly stringent and complex regulating process and meiotic recombination frequency (MRF) may be affected by biological and abiotic factors such as sex, gene density, nucleotide content, and chemical/temperature treatments, having motivated tremendous researches for artificially manipulating MRF. Whether genome polyploidization would lead to a significant change in MRF has attracted both historical and recent research interests; however, tackling this fundamental question is methodologically challenging due to the lack of appropriate methods for tetrasomic genetic analysis, thus has led to controversial conclusions in the literature. This article presents a comprehensive and rigorous survey of genome duplication-mediated change in MRF using Saccharomyces cerevisiae as a eukaryotic model. It demonstrates that genome duplication can lead to consistently significant increase in MRF and rate of crossovers across all 16 chromosomes of S. cerevisiae, including both cold and hot spots of MRF. This ploidy-driven change in MRF is associated with weakened recombination interference, enhanced double-strand break density, and loosened chromatin histone occupation. The study illuminates a significant evolutionary feature of genome duplication and opens an opportunity to accelerate response to artificial and natural selection through polyploidization.

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Coprinus cinereus rad50Mutants Reveal an Essential Structural Role for Rad50 in Axial Element and Synaptonemal Complex Formation, Homolog Pairing and Meiotic Recombination

Genetics ◽

10.1534/genetics.108.092775 ◽

2008 ◽

Vol 180 (4) ◽

pp. 1889-1907 ◽

Cited By ~ 15

Author(s):

Sonia N. Acharya ◽

Alexander M. Many ◽

Andrew P. Schroeder ◽

Felicia M. Kennedy ◽

Oleksandr P. Savytskyy ◽

...

Keyword(s):

Complex Formation ◽

Synaptonemal Complex ◽

Meiotic Recombination ◽

Coprinus Cinereus ◽

Structural Role ◽

Homolog Pairing ◽

Synaptonemal Complex Formation ◽

Axial Element

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Critical Role of Caenorhabditis elegansHomologs of Cds1 (Chk2)-Related Kinases in Meiotic Recombination

Molecular and Cellular Biology ◽

10.1128/mcb.21.4.1329-1335.2001 ◽

2001 ◽

Vol 21 (4) ◽

pp. 1329-1335 ◽

Cited By ~ 20

Author(s):

Isao Oishi ◽

Kenji Iwai ◽

Yukiko Kagohashi ◽

Hiroko Fujimoto ◽

Ken-Ichi Kariya ◽

...

Keyword(s):

Meiotic Recombination ◽

Critical Role ◽

Microscopic Analysis ◽

Electron Microscopic ◽

Synaptonemal Complex Formation ◽

Genetic Interference ◽

Multicellular Organisms ◽

Critical Process ◽

Novel Protein

ABSTRACT Although chromosomal segregation at meiosis I is the critical process for genetic reassortment and inheritance, little is known about molecules involved in this process in metazoa. Here we show by utilizing double-stranded RNA (dsRNA)-mediated genetic interference that novel protein kinases (Ce-CDS-1 and Ce-CDS-2) related to Cds1 (Chk2) play an essential role in meiotic recombination inCaenorhabditis elegans. Injection of dsRNA into adult animals resulted in the inhibition of meiotic crossing over and induced the loss of chiasmata at diakinesis in oocytes of F1animals. However, electron microscopic analysis revealed that synaptonemal complex formation in pachytene nuclei of the same progeny of injected animals appeared to be normal. Thus, Ce-CDS-1 and Ce-CDS-2 are the first example of Cds1-related kinases that are required for meiotic recombination in multicellular organisms.

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Genetic interactions between the chromosome axis-associated protein Hop1 and homologous recombination determinants in Schizosaccharomyces pombe

10.1101/190439 ◽

2017 ◽

Author(s):

Simon David Brown ◽

Olga Dorota Jarosinska ◽

Alexander Lorenz

Keyword(s):

Homologous Recombination ◽

Schizosaccharomyces Pombe ◽

Fission Yeast ◽

Synaptonemal Complex ◽

Meiotic Recombination ◽

Dna Breaks ◽

Dna Break ◽

Chromosome Axis ◽

Break Formation ◽

Double Strand Dna

AbstractHop1 is a component of the meiosis-specific chromosome axis and belongs to the evolutionarily conserved family of HORMA domain proteins. Hop1 and its orthologs in higher eukaryotes are a major factor in promoting double-strand DNA break formation and inter-homolog recombination. In budding yeast and mammals they are also involved in a meiotic checkpoint kinase cascade monitoring the completion of double-strand DNA break repair. We used the fission yeast, Schizosaccharomyces pombe, which lacks a canonical synaptonemal complex to test whether Hop1 has a role beyond supporting the generation of double-strand DNA breaks and facilitating inter-homolog recombination events. We determined how mutants of homologous recombination factors genetically interact with hop1, studied the role(s) of the HORMA domain of Hop1, and characterized a bio-informatically predicted interactor of Hop1, Aho1 (SPAC688.03c). Our observations indicate that in fission yeast, Hop1 does require its HORMA domain to support wild-type levels of meiotic recombination and localization to meiotic chromatin. Furthermore, we show that hop1Δ only weakly interacts genetically with mutants of homologous recombination factors, and in fission yeast likely has no major role beyond break formation and promoting inter-homolog events. We speculate that after the evolutionary loss of the synaptonemal complex, Hop1 likely has become less important for modulating recombination outcome during meiosis in fission yeast, and that this led to a concurrent rewiring of genetic pathways controlling meiotic recombination.

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