DNA Crossover Motifs Associated with Epigenetic Modifications Delineate Open Chromatin Regions in Arabidopsis

Shilo, Shay; Melamed-Bessudo, Cathy; Dorone, Yanniv; Barkai, Naama; Levy, Avraham A.

doi:10.1105/tpc.15.00391

Cited by 104 publications

(181 citation statements)

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“…These two different categories (specific TE-associated motif and simple repeats) were found in previous analyses in other species (Comeron et al 2012;Auton et al 2013;Choi et al 2013;Wijnker et al 2013;Shilo et al 2015). The A-stretch motif was already found in Arabidopsis, human, and Drosophila to be associated with recombination in 2-kb areas around CO events, suggesting that A-stretches do not directly induce recombination but that they contribute to its occurrence as a result of DNA decompaction (Myers et al 2008;Comeron et al 2012;Shilo et al 2015).…”

Section: Te-related Motifs Are Thus Present In Recombinogenic Windowssupporting

confidence: 55%

“…New wheat-genomic tools allow more resolute analysis of recombination pattern Whole-genome, fine-scale recombination studies in plants have only been conducted in species for which the genome sequence was available (Wu et al 2003;Liu et al 2009;Paape et al 2012;Rodgers-Melnick et al 2015;Shilo et al 2015). However, this mainly restricted such analyses to species with small and compact genomes with low rates of TEs.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies in Arabidopsis, Drosophila, and dogs discovered recombination-associated motifs like A-stretch motif, CCT, CCN repeats, and CpG (Comeron et al 2012;Auton et al 2013;Wijnker et al 2013;Shilo et al 2015;Choi et al 2016). To evaluate the existence of recombinationassociated motifs in wheat, we searched for DNA motifs overrepresented in Rec intervals without a priori using MEME Suite and the base frequency of the chromosome (see Materials and Methods for details).…”

Section: Recombinogenic Regions Have Different Composition In Tes Andmentioning

confidence: 99%

“…In plants, no homolog to PRDM9 subfamily was found (Zhang and Ma 2012). However, most H3K4me3-methylase encoding genes are expressed in meiotic cells in Arabidopsis and rice (Zhang and Ma 2012), and this mark is associated with recombinogenic regions in Arabidopsis and barley (Choi et al 2013;Aliyeva-Schnorr et al 2015;Shilo et al 2015). This may even be a general eukaryotic regulatory mechanism and may have originated in the ancestor of eukaryotes (Zhang and Ma 2012;Mercier et al 2015).…”

mentioning

confidence: 99%

“…Significant associations were found between hotspots and poly-A stretches (Choi et al 2013;Wijnker et al 2013;Shilo et al 2015) which are known to preferentially locate upstream of TSSs, resulting in reduced nucleosome occupancy that facilitates accessibility of the recombination machinery (Wu and Lichten 1994;Berchowitz et al 2009;Segal and Widom 2009;Pan et al 2011). Similarly, CCN-and CTT-repeat sequence motifs were also detected to be associated to recombination hotspots (Choi et al 2013;Shilo et al 2015;Wijnker et al 2013). These motifs are also located close to the TSSs and are similar to the motif targeted by the PRDM9 protein in humans and mouse, which may suggest a similar recognition by the recombination machinery.…”

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confidence: 99%

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High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

et al. 2017

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During meiosis, crossovers (COs) create new allele associations by reciprocal exchange of DNA. In bread wheat (Triticum aestivum L.), COs are mostly limited to subtelomeric regions of chromosomes, resulting in a substantial loss of breeding efficiency in the proximal regions, though these regions carry 60-70% of the genes. Identifying sequence and/or chromosome features affecting recombination occurrence is thus relevant to improve and drive recombination. Using the recent release of a reference sequence of chromosome 3B and of the draft assemblies of the 20 other wheat chromosomes, we performed fine-scale mapping of COs and revealed that 82% of COs located in the distal ends of chromosome 3B representing 19% of the chromosome length. We used 774 SNPs to genotype 180 varieties representative of the Asian and European genetic pools and a segregating population of 1270 F 6 lines. We observed a common location for ancestral COs (predicted through linkage disequilibrium) and the COs derived from the segregating population. We delineated 73 small intervals (,26 kb) on chromosome 3B that contained 252 COs. We observed a significant association of COs with genic features (73 and 54% in recombinant and nonrecombinant intervals, respectively) and with those expressed during meiosis (67% in recombinant intervals and 48% in nonrecombinant intervals). Moreover, while the recombinant intervals contained similar amounts of retrotransposons and DNA transposons (42 and 53%), nonrecombinant intervals had a higher level of retrotransposons (63%) and lower levels of DNA transposons (28%). Consistent with this, we observed a higher frequency of a DNA motif specific to the TIR-Mariner DNA transposon in recombinant intervals. KEYWORDS recombination; meiosis; bread wheat; linkage disequilibrium; transposon; hotspot; sequence motif M EIOTIC recombination is a process that allows reshuffling of diversity by the reciprocal exchange of DNA called a crossover (CO). This phenomenon is conserved in most eukaryotes (for a review see Mercier et al. 2015) and follows the formation of a double-strand break (DSB) of DNA generated by the topoisomerase SPO11 complex. However, the number of DSBs is at least 10-to 50-fold greater than the number of COs which rarely exceeds three per bivalent chromosome per meiosis (Mercier et al. 2015). This paucity of COs per meiosis with regards to the number of DSBs suggests the existence of a tight control and regulation of recombination in plants that promote DSB repair in a manner that does not lead to COs. For example, the study of the two helicases AtFANCM and RECQ4 (AtRECQ4A and AtRECQ4B) (Crismani et al. 2012;Knoll et al. 2012;Girard et al. 2014;Séguéla-Arnaud et al. 2015) revealed three-and sixfold CO frequency increases in the Atfancm single mutant and the Atrecq4a/Atrecq4b double mutant, respectively, compared to the wild type. These increases result from additional COs from the class-II pathway which suggests that FANCM and RECQ4 prevent CO formation and direct recombination intermediates towar...

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Section: Te-related Motifs Are Thus Present In Recombinogenic Windowssupporting

confidence: 55%

Section: Discussionmentioning

confidence: 99%

Section: Recombinogenic Regions Have Different Composition In Tes Andmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

et al. 2017

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Protocol for Chromatin Immunoprecipitation of Meiotic‐Stage‐Specific Tomato Anthers

et al. 2018

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Interactions occurring between DNA and proteins across the nuclear genome regulate numerous processes, including meiosis. Meiosis ensures genetic variation and balanced segregation of homologous chromosomes. It involves complex DNA-protein interactions across the entire genome to regulate a broad range of processes, including formation and repair of double-strand DNA breaks (DSBs), chromosome compaction, homolog pairing, synapsis, and homologous recombination. The latter meiotic event, meiotic recombination, often occurs at discrete locations in a genome, within a tight time window. The identification of genomic binding sites of meiotic proteins is a major step toward understanding the molecular mechanisms underlying meiotic recombination and provides important information for plant breeding. Collecting meiotic cells from plants is challenging, tedious, and time consuming, since the meiocyte-producing organs, the anthers, are generally small and limited to certain developmental stages of plants. Here we provide a protocol to isolate meiotic-stage-specific anthers and perform ChIP on this material. We have developed a ChIP protocol specifically suited to (1) small amounts of input material and (2) proteins that bind transiently to chromatin and at very low frequency. © 2018 by John Wiley & Sons, Inc.

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Balanced spatiotemporal arrangements of histone H3 and H4 posttranslational modifications are necessary for meiotic prophase I chromosome organization

Kumar,

Mohanty,

Kumari

et al. 2024

Journal Cellular Physiology

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Dynamic nuclear architecture and chromatin organizations are the key features of the mid‐prophase I in mammalian meiosis. The chromatin undergoes major changes, including meiosis‐specific spatiotemporal arrangements and remodeling, the establishment of chromatin loop–axis structure, pairing, and crossing over between homologous chromosomes, any deficiencies in these events may induce genome instability, subsequently leading to failure to produce gametes and infertility. Despite the significance of chromatin structure, little is known about the location of chromatin marks and the necessity of their balance during meiosis prophase I. Here, we show a thorough cytological study of the surface‐spread meiotic chromosomes of mouse spermatocytes for H3K9,14,18,23,27,36, H4K12,16 acetylation, and H3K4,9,27,36 methylation. Active acetylation and methylation marks on H3 and H4, such as H3K9ac, H3K14ac, H3K18ac, H3K36ac, H3K56ac, H4K12ac, H4K16ac, and H3K36me3 exhibited pan‐nuclear localization away from heterochromatin. In comparison, repressive marks like H3K9me3 and H3K27me3 are localized to heterochromatin. Further, taking advantage of the delivery of small‐molecule chemical inhibitors methotrexate (heterochromatin enhancer), heterochromatin inhibitor, anacardic acid (histone acetyltransferase inhibitor), trichostatin A (histone deacetylase inhibitor), IOX1 (JmjC demethylases inhibitor), and AZ505 (methyltransferase inhibitor) in seminiferous tubules through the rete testis route, revealed that alteration in histone modifications enhanced the centromere mislocalization, chromosome breakage, altered meiotic recombination and reduced sperm count. Specifically, IOX1 and AZ505 treatment shows severe meiotic phenotypes, including altering chromosome axis length and chromatin loop size via transcriptional regulation of meiosis‐specific genes. Our findings highlight the importance of balanced chromatin modifications in meiotic prophase I chromosome organization and instability.

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DNA Crossover Motifs Associated with Epigenetic Modifications Delineate Open Chromatin Regions in Arabidopsis

Cited by 104 publications

References 53 publications

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

Protocol for Chromatin Immunoprecipitation of Meiotic‐Stage‐Specific Tomato Anthers

Balanced spatiotemporal arrangements of histone H3 and H4 posttranslational modifications are necessary for meiotic prophase I chromosome organization

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