Cited by <scp>MSH</scp> 2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis

MSH 2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis DOI

et al.

The EMBO Journal, Journal Year: 2020, Volume and Issue: 39(21)

Published: Sept. 16, 2020

Article16 September 2020Open Access Transparent process MSH2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism Arabidopsis Alexander R Blackwell orcid.org/0000-0002-0369-4584 Department of Plant Sciences, University Cambridge, UK Search for more papers by this author Julia Dluzewska orcid.org/0000-0002-7419-5934 Laboratory Genome Biology, Institute Molecular Biology and Biotechnology, Adam Mickiewicz University, Poznan, Poland Maja Szymanska-Lejman orcid.org/0000-0003-4813-3278 Stuart Desjardins orcid.org/0000-0002-3749-1873 Genetics Leicester, Andrew J Tock orcid.org/0000-0002-6590-8314 Nadia Kbiri orcid.org/0000-0001-6816-8369 Christophe Lambing orcid.org/0000-0001-5218-4217 Emma Lawrence Tomasz Bieluszewski Beth Rowan orcid.org/0000-0001-7240-4889 Max Planck Developmental Tübingen, Germany James D Higgins Piotr A Ziolkowski Corresponding Author [email protected] orcid.org/0000-0001-7673-6565 Ian Henderson orcid.org/0000-0001-5066-1489 Information Blackwell1,‡, Dluzewska2,‡, Szymanska-Lejman2, Desjardins3, Tock1, Kbiri2, Lambing1, Lawrence1, Bieluszewski2, Rowan4,†, Higgins3, *,2 *,1 1Department 2Laboratory 3Department 4Department †Present address: Center California, Davis, CA, USA ‡These authors contributed equally work *Corresponding author. Tel: +48 61 8295966; E-mail: +44 01223 748 977; EMBO (2020)39:e104858https://doi.org/10.15252/embj.2020104858 PDFDownload PDF article text main figures. Peer ReviewDownload a summary editorial decision including letters, reviewer comments responses feedback. ToolsAdd favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures & Info Abstract During meiosis, DNA double-strand breaks undergo repair yield crossovers between homologous chromosomes. To investigate how sequence affects crossovers, we sequenced multiple recombinant populations model plant thaliana. Crossovers were elevated diverse pericentromeric regions, showing local preference polymorphic regions. We provide evidence that association with diversity is mediated via Class I formation pathway, although very high levels suppress crossovers. Interhomolog causes mismatches recombining molecules, which can be detected MutS homolog (MSH) mismatch protein heterodimers. Therefore, mapped msh2 mutant, defective recognition, using hybrid backgrounds. Although total numbers unchanged mutants, recombination was remodelled from pericentromeres towards less-polymorphic sub-telomeric Juxtaposition megabase heterozygous homozygous regions remodelling wild type Arabidopsis, but not mutants. Immunostaining showed accumulates on chromosomes during prophase I, consistent regulating recombination. Our results reveal pro-crossover role higher A. Synopsis Meiotic Sequencing polymorphisms wild-type mutant plants reveals an unexpected relative diversity. are positively associated both at chromosome level fine scales Arabidopsis. mediate – Total less sub-telomeres. megabase-scale remodeling MSH2-dependent. Introduction Meiosis creates genetic eukaryotic sexual reproduction widely conserved among plants, animals fungi (Villeneuve Hillers, 2001; Mercier et al, 2015). (DSBs) form may enter pathway create reciprocal or non-reciprocal gene conversions Together, these have profound effect variation genome evolution. SPO11 transesterases DSBs resected produce 3′-overhanging single-stranded (ssDNA) (Keeney Neale, 2006; Hunter, ssDNA bound RecA homologs DMC1 RAD51, strand invasion displacement loops (D-loops) D-loops dissolved repaired non-crossover protected further processed (Hunter, The "ZMM" provides major activity (Mercier 2015; Pyatnitskaya 2019). ZMM acts stabilize joint molecules promote resolution double Holliday junctions (dHJs) minority formed II involves structure-specific endonucleases, MUS81 An important distinction pathways only show interference, meaning events spaced along than expected chance Copenhaver 2002; Due chromosomes, meiosis likely experience base pair mismatches. Increased divergence been observed (HR) mitosis (Borts Haber, 1987; Datta 1997; Elliott 1998; Chen Jinks-Robertson, 1999; Opperman 2004; Emmanuel Li 2018; Do LaRocque, For example, hotspot budding yeast Saccharomyces cerevisiae cause decreased whilst increasing frequency other 1987). Furthermore, structural within hotspots, insertions deletions, has suppression (Dooner, 1986; Jeffreys Neumann, 2005; Baudat de Massy, 2007; Cole 2010). In many cases, inhibition HR dependent MutS-related heterodimers contain Jasin, complexes capable binding play key roles post-replicative mutation correction rejection heteroduplex (Modrich Lahue, 1996; Kunkel Erie, 2005). Msh2 as anti-recombinase recruitment Sgs1 helicase, human BLM, promotes disassembly mismatched (Myung Mazina 2004). Hence, machinery limit polymorphism-dependent manner. Despite inhibitory HR, data indicate positive relationship polymorphism. historical recombination, measured linkage disequilibrium, correlated species (Begun Aquadro, 1992; Nordborg Spencer Gore 2009; Paape 2012; Cutter Payseur, 2013). Direct measurements hybrids also shown compared inbred backgrounds, specific (Barth Finally, juxtaposition heterozygosity homozygosity increased expense (Ziolkowski case, require interfering vary across different contexts. sought explore polymorphism, forms MSH3, MSH6 MSH7 vitro, display varying affinities single short (1–3 bp) indel (Culligan Hays, 2000; Adé Wu 2003). Single rates deleterious phenotypes following inbreeding (Leonard 2003; Hoffman Watson 2016; Belfield 2018). Somatic split GUS (GU:US) transgenes (Emmanuel Increasing number GU US substrate repeats decreases type, Interestingly, previous demonstrated increase region hybrids, 2006). extend studies mapping distributions genome-wide examine relationships promoted associate scale. SNP density pathway. sensor 2015), test its Unexpectedly, found MSH2. This leads re-evaluation impact genomes, process. Results Crossover landscapes thaliana predominantly self-fertilizes occurs naturally accessions estimated outcross rate 0.3 2.5% (Bomblies 2010; 1001 Genomes Consortium 2016). interactions generated F2 five crosses Col-0 reference accession (hereafter Col) Ler-0 Ler) (Serra 2018b), Bur-0 Bur) (Lawrence 2019), Ws-4 Ws) Ct-1 Ct) accessions. population crossing Col CLC, mosaic Cvi-0, Ler (Fig 1). CLC composed Cvi-0 sequence, substituted 5 additional introgressions 1B). × larger set 2,182 individuals identified 17,077 2018b; These backgrounds range when Col. 413,830 (3.31 SNPs/kb) 562,423 (4.49 SNPs each accession, Col, 30–55% shared Ler, Bur, Ws Ct (Appendix Tables S1 S2). Figure 1. Histograms (blue) per individual indicated populations, Poisson expectation plotted red. Mean values black dotted lines. average SNPs/kb cross printed above plots. 200 kb horizontal dashed shaded colour (Col (purple), Bur 2019) (dark green), (light blue), (red) 1,840 (pink/light green, where pink indicates Cvi green SNPs). positions telomeres (TEL) centromeres (CEN) indicated. analysed inset. Data B, analysing (lines) (shading) proportionally scaled arms, orientated telomere centromere (CEN). Download figure PowerPoint genomic 180 305 1,396 2,478 population, TIGER pipeline 1A Appendix Table S3) 2019; haplotype switches assigned pairs (Rowan define had mean distance 653 2,261 bp S3). stable crosses, 7.51 8.40 significantly assessed goodness-of-fit tests (P = 0.012–3.63 10−6; Fig 1A), action interference homeostasis (Jones Franklin, order spacing, cis-DCOs our genotyping data, filtering parental-heterozygous-parental genotype transitions (e.g. Col-Het-Col Ler-Het-Ler individuals; S1) (Drouaud 2020a). 2,000 sets matched randomly distances control case. random DCOs permutation tests. greater distances, all (all P < 0.005; S1). maintenance spacing tested analyse throughout genome, calculated after normalizing replicate maps (Spearman's correlation coefficient rs 0.904 scale; 1B S4), demonstrating reproducibility approach. Significant, yet weaker, correlations (rs 0.580–0.712; S4). Structural contribute differences highly reduced 45S rDNA copy NOR2 (Rabanal 2017), correlates Additionally, zone long arm 4 map reflect presence known inversion 1B) arms U-shaped distribution, extents 1C). Across maps, highest sub-telomeres patterns relate pairing (Armstrong Da Ines 2012). Using same analysis, progressive C). 0.545; Figs 2A). most divergent defined methylation, surround S2) (Choi It note chromatin strongly influences varies telomere-centromere axes (Yelina Choi Underwood 2020b). remained suppressed C), heterochromatic marks methylation H3K9me2, SPO11-1-oligo sequencing Walker 2. parabolic normalized 100 kilobase (kb) adjacent windows ranked into percentiles according density. Centromeric excluded analysis (Underwood Spearman's rank (r) Trend lines fitted ggplot generalized additive (GAM) formula y ˜ poly(x,2). Generalized linear (GLM) plots Col/Ler intervals grouped hexiles quintiles, (left right x-axis) given explanatory variable. modelled glm2 function R, binomial family logit link function. used (SPO11-1 + nucleosomes H3K4me3 width)2. Predicted group derived sampling distribution based probabilities overlapping crossover. box represent samples, central band represents median, interquartile (IQR), whiskers minimum maximum no 1.5 times IQR box. final stepAIC-selected follows:Crossovers SPO11-1 width SPO11-1:nucleosomes SPO11-1:DNA SPO11-1:width nucleosomes:H3K4me3 nucleosomes:DNA nucleosomes:SNPs/kb H3K4me3:DNA H3K4me3:width methylation:width SNPs/kb:width. Importantly, Initially, correlation, associates quantitatively effects parameters features, 3,320 2B S5) considered 534,780 it possible detect crossover, 224 bp. binary response variable whether least one interval. then variables intervals, SPO11-1-oligos, (MNase-seq), (ChIP-seq), (BS-seq) density, rolling step calculate formula, (SPO11-1-oligos selected lowest Akaike information criterion (AIC). shows negative SPO11-1-oligos again 2B). associating However, beyond certain threshold becomes causing 2018a; summary, see that, below critical threshold, attract addition strong DSB frequency. scale sites (kilobase) (SNPs/kb) physical size around midpoints, divided 3A). Analysis restricted resolved 10 apart. As control, significant enrichment random, window (Bonferroni-adjusted t-tests, 5.04 10−5; repeated separating those located versus similar trends majority sizes transversions separately, (n 16,175; 3B). class positions, over 1.85 10−4; analyses composition AT reported, locally nucleosome occupancy S4) 3. midpoints (red), chosen (grey). Printed plot circles coloured if 0.05), red > 0.05; Bonferroni-adjusted t-tests). Ws, Ct, CLC) plot, A, transition transversion HEI10-OE, recq4a recq4b HEI10-OE 2018b). All hybrids. beneath genotype, genotyping-by-sequencing 2017; Serra significance sets, mediates elevate

Language: Английский

The genetic and epigenetic landscape of the Arabidopsis centromeres DOI

Matthew Naish, Michael Alonge, Piotr Włodzimierz

et al.

Science, Journal Year: 2021, Volume and Issue: 374(6569)

Published: Nov. 11, 2021

A closer look at centromeres Centromeres are key for anchoring chromosomes to the mitotic spindle, but they have been difficult sequence because can contain many repeating DNA elements. These repeats, however, carry regularly spaced, distinctive markers of heterogeneity between mostly, not completely, identical repeats. Such differences aid assembly. Naish et al . used ultra-long-read sequencing establish a reference assembly that resolves all five in small mustard plant Arabidopsis Their view into subtly homogenized world reveals retrotransposons interrupt centromere organization and repressive methylation excludes from meiotic crossover repair. Thus, evolve under opposing forces homogenization retrotransposon disruption. —PJH

Language: Английский

Citations

305

Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions DOI

Kyuha Choi, Xiaohui Zhao, Andrew J. Tock

et al.

Genome Research, Journal Year: 2018, Volume and Issue: 28(4), P. 532 - 546

Published: March 12, 2018

Meiotic recombination initiates from DNA double-strand breaks (DSBs) generated by SPO11 topoisomerase-like complexes. DSB frequency varies extensively along eukaryotic chromosomes, with hotspots controlled chromatin and sequence. To map meiotic DSBs throughout a plant genome, we purified sequenced Arabidopsis thaliana SPO11-1-oligonucleotides. SPO11-1-oligos are elevated in gene promoters, terminators, introns, which is driven AT-sequence richness that excludes nucleosomes allows SPO11-1 access. A positive relationship was observed between crossovers genome-wide, although fine-scale correlations were weaker. This may reflect the influence of interhomolog polymorphism on crossover formation, downstream formation. Although H3K4me3 enriched proximity to SPO11-1-oligo at 5′ ends, levels do not correlate DSBs. Repetitive transposons thought be silenced during meiosis, prevent nonallelic interactions genome instability. Unexpectedly, found high nucleosome-depleted Helitron/Pogo/Tc1/Mariner transposons, whereas retrotransposons coldspots. High within regulatory regions immunity genes, suggesting role as enhancers. As transposon mobility genomes restricted methylation, used met1 methyltransferase mutant investigate heterochromatin distributions. Epigenetic activation centromeres occurred mutants, coincident reduced nucleosome occupancy, gain transcription, H3K4me3. Together, our work reveals complex A. genes significance for diversity evolution genomes.

Language: Английский

Citations

198

DNA methylation-free Arabidopsis reveals crucial roles of DNA methylation in regulating gene expression and development DOI

Li He, Huan Huang, Mariem Bradai

et al.

Nature Communications, Journal Year: 2022, Volume and Issue: 13(1)

Published: March 14, 2022

Abstract A contribution of DNA methylation to defense against invading nucleic acids and maintenance genome integrity is uncontested; however, our understanding the extent involvement this epigenetic mark in genome-wide gene regulation plant developmental control incomplete. Here, we knock out all five known methyltransferases Arabidopsis , generating methylation-free plants. This quintuple mutant exhibits a suite defects, unequivocally demonstrating that essential for multiple aspects development. We show CG non-CG are required plethora biological processes, including pavement cell shape, endoreduplication, death, flowering, trichome morphology, vasculature meristem development, root fate determination. Moreover, find has strong dose-dependent effect on expression repression transposable elements. Taken together, results demonstrate dispensable survival but proper processes.

Language: Английский

Citations

147

Addressing Research Bottlenecks to Crop Productivity DOI

Matthew Reynolds, Owen K. Atkin, Malcolm J. Bennett

et al.

Trends in Plant Science, Journal Year: 2021, Volume and Issue: 26(6), P. 607 - 630

Published: April 21, 2021

More symmetrical investment in crop research will create opportunities to improve models, combine new alleles through prebreeding, and suggest novel management practices.Consensus among public private sectors is that more needed understanding of hormone crosstalk, recombination rate, maintenance respiration, root structure function, source–sink balance.Greater these areas expected benefit a wide range crops across most environments.New phenomics, genomics, bioinformatics make it feasible explore the vast untapped collections genetic resources trait combinations.Filling knowledge gaps enable much integrated yield adaptation, improving breeding models. Asymmetry leads lost accelerate gain identifying sources combinations traits alleles. On basis consultation with scientists from major seed companies, we identified several three common features: (i) relatively underrepresented literature; (ii) high probability boosting productivity environments; (iii) could be researched 'precompetitive' space, leveraging previous knowledge, thereby models guide decisions. Areas included into hormones, recombination, roots, source–sink, which, along bioinformatics, strategies. Research growth adaptation under diverse cultivation scenarios has underpinned global food security, especially since Green Revolution, during which time population than doubled. During same time, area cultivated cereals, account for 70% total calories consumed by humans, barely changed while yields have tripled.i These two statistics alone clearly support impact on agronomy as well effective policy decisions agility farmers adopt technologies [1.Stewart B.A. Lal R. Increasing world average cereal crops: it's all about water.in: Sparks D.L. Advances Agronomy. 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Five challenging that, tackled systematically, likely open bottlenecks discussed herein, discussion used CGMs. exhaustive cannot presented here, nor bottlenecks, emerge improves. were broadly agreed authors colleagues sectors. complementary each existing 2). opinion colleagues, 'best bets' achieving step changes roles increasing sink strength carbon assimilation meiotic harness diversity. reviewed: exploration prebreeding Illuminating 'black boxes' simulation modelling. authorship represents stakeholders sectors, topics priorities 'precompetitive space' defined companies exercise; words, general neglected, potentially hold industry. aid foraging, responsive abiotic biotic signals local highly adaptable behavior, termed 'developmental plasticity', offers breeders 'customized' architecture (RSA) adapted forage heterogenous conditions [29.Hodge plastic plant: responses heterogeneous supplies nutrients.New Phytol. 2004; 162: 9-24Crossref (1052) (N) form nitrate (NO3–) particular challenge capture, mobile leaches deeper layers. 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Studying arguably relevant, poses Indirect approaches canopy measurements determining extraction profiles electrical electromagnetic inductance methods infer traits, currently coarse resolution [42.Whalley W.R. al.Methods estimate activity field.Plant 415: 407-422Crossref (22) Invasive coring 'shovelomics' greatly facilitated throughput [43.Trachsel al.Shovelomics: L.) 341: 75-87Crossref (338) destructive techniques result loss finer-scale features roots), give snapshot development. Nondestructive imaging techniques, agar plates, rhizotrons, paper-based hydro-/aeroponic systems, temporal observed throughout possible transparent gels [44.Clark R.T. al.Three-dimensional software platform.Plant 156: 455-465Crossref (274) non–soil-based helps decrease experimental reducing heterogeneity microbial populations, results difficult extrapolate conditions. experiments [45.Messina al.Reproductive resilience underpin L.).bioRxiv. 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U. 113: 8861-8866Crossref (43) Scholar,51.Gao Y.Z. acquisition L.).J. 67: 4545-4557Crossref (84) few long ideotype suggested stress, saved extend profiles. indeed tuned based fundamental [52.Cooper gap productivity.Crop 582-604Crossref (10) colonizing

Language: Английский

Citations

112

The integrated genomics of crop domestication and breeding DOI

Xuehui Huang, Sanwen Huang, Bin Han

et al.

Cell, Journal Year: 2022, Volume and Issue: 185(15), P. 2828 - 2839

Published: May 27, 2022

Language: Английский

Citations

103

Structural variation and DNA methylation shape the centromere-proximal meiotic crossover landscape in Arabidopsis DOI

Joiselle Blanche Fernandes, Matthew Naish, Qichao Lian

et al.

Genome biology, Journal Year: 2024, Volume and Issue: 25(1)

Published: Jan. 22, 2024

Centromeres load kinetochore complexes onto chromosomes, which mediate spindle attachment and allow segregation during cell division. Although centromeres perform a conserved cellular function, their underlying DNA sequences are highly divergent within between species. Despite variability in sequence, also universally suppressed for meiotic crossover recombination, across eukaryotes. However, the genetic epigenetic factors responsible suppression of centromeric crossovers remain to be completely defined.

Language: Английский

Citations

An Ultra High-Density Arabidopsis thaliana Crossover Map That Refines the Influences of Structural Variation and Epigenetic Features DOI

Beth A. Rowan, Darren Heavens, Tatiana R. Feuerborn

et al.

Genetics, Journal Year: 2019, Volume and Issue: 213(3), P. 771 - 787

Published: Sept. 16, 2019

Abstract Rowan et al. generated a dataset of over 17,000 meiotic crossovers (COs) from 2000 F2 individuals single Arabidopsis thaliana cross. The unprecedented density COs and the high-quality reference genomes two... Many environmental, genetic, epigenetic factors are known to affect frequency positioning (COs). Suppression by large, cytologically visible inversions translocations has long been recognized, but relatively little is about how smaller structural variants (SVs) COs. To examine fine-scale determinants CO landscape, including SVs, we used rapid, cost-effective method for high-throughput sequencing generate precise map >17,000 between Col-0 Ler-0 accessions thaliana. were generally suppressed in regions with this effect did not depend on size variant region, was only marginally affected type. suppression extend far beyond SV borders rates slightly elevated flanking regions. Disease resistance gene clusters, which often exist as exhibited high at some loci, there tendency toward depressed loci where large differences two parents. Our high-density also revealed fine detail relates genetic (DNA motifs) (chromatin structure) features genome. We conclude that occurs narrow region spanning large- small-scale representing an influence landscape addition sequence variation along chromosomes.

Language: Английский

Citations

129

Double-edged sword: The evolutionary consequences of the epigenetic silencing of transposable elements DOI

Jae Young Choi, Yuh Chwen G. Lee

PLoS Genetics, Journal Year: 2020, Volume and Issue: 16(7), P. e1008872 - e1008872

Published: July 16, 2020

Transposable elements (TEs) are genomic parasites that selfishly replicate at the expense of host fitness. Fifty years evolutionary studies TEs have concentrated on deleterious genetic effects TEs, such as their disrupting genes and regulatory sequences. However, a flurry recent work suggests there is another important source TEs’ harmful effects—epigenetic silencing. Host genomes typically silence by deposition repressive epigenetic marks. While this silencing reduces selfish replication should benefit hosts, picture emerging triggers inadvertent spreading marks to otherwise expressed neighboring genes, ultimately jeopardizing In Review, we provide long-overdue overview genome-wide evidence for presence prevalence effects, highlighting both similarities differences across mammals, insects, plants. We lay out current understanding functional fitness consequences propose possible influences evolution hosts themselves. These unique indicate effect not only crucial component TE biology but could also be significant contributor genome function evolution.

Language: Английский

Citations

114

Speciation Success of Polyploid Plants Closely Relates to the Regulation of Meiotic Recombination DOI

Alexandre Pelé, Mathieu Rousseau‐Gueutin, Anne‐Marie Chèvre

et al.

Frontiers in Plant Science, Journal Year: 2018, Volume and Issue: 9

Published: June 28, 2018

Polyploidization is a widespread phenomenon, especially in flowering plants that have all undergone at least one event of whole genome duplication during their evolutionary history. Consequently, large range plants, including many the world's crops, combines more than two sets chromosomes originating from same (autopolyploids) or related species (allopolyploids). Depending on polyploid formation pathway, different patterns recombination will be promoted, conditioning level heterozygosity. A population harboring high heterozygosity produce genetically diverse progenies. Some these individuals may show better adaptability to ecological niches, increasing chance for successful establishment through natural selection. Another condition young polyploids survive corresponds well-balanced gametes, assuring sufficient fertility. In this review, we discuss consequences pathways, meiotic behavior and regulation speciation success maintenance species.

Language: Английский

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Destabilization of chromosome structure by histone H3 lysine 27 methylation DOI

Mareike Möller, Klaas Schotanus, Jessica L. Soyer

et al.

PLoS Genetics, Journal Year: 2019, Volume and Issue: 15(4), P. e1008093 - e1008093

Published: April 22, 2019

Chromosome and genome stability are important for normal cell function as instability often correlates with disease dysfunction of DNA repair mechanisms. Many organisms maintain supernumerary or accessory chromosomes that deviate from standard chromosomes. The pathogenic fungus Zymoseptoria tritici has many eight chromosomes, which highly unstable during meiosis mitosis, transcriptionally repressed, show enrichment repetitive elements, heterochromatic histone methylation marks, e.g., trimethylation H3 lysine 9 27 (H3K9me3, H3K27me3). To elucidate the role heterochromatin on in Z. tritici, we deleted genes encoding methyltransferases responsible H3K9me3 H3K27me3, kmt1 kmt6, respectively, generated a double mutant. We combined experimental evolution genomic analyses to determine impact these deletions chromosome stability, both vitro planta. used whole sequencing, ChIP-seq, RNA-seq compare changes chromatin structure, differences gene expression between mutant wildtype strains. Analyses ChIP-seq data H3K9me3-deficient strains revealed dramatic reorganization, where H3K27me3 is mostly relocalized into regions enriched wild type. rearrangements formation new were found absence H3K9me3, accompanied by activation transposable elements. In stark contrast, loss actually increased under growth conditions vitro, even without large scale activity. conclude maintenance because it disallows considered constitutive heterochromatin. this system, reduces overall generating "metastable" state quasi-essential genome.

Language: Английский

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