Nonparadoxical evolutionary stability of the recombination initiation landscape in yeast

Lam, Isabel; Keeney, Scott

doi:10.1126/science.aad0814

Cited by 123 publications

(175 citation statements)

References 57 publications

(81 reference statements)

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“…At the whole-genome level, similar results were found with 2/3 of COs overlapping genes, as this is the case for most COs in plants (reviewed in Mercier et al 2015). Our COs were found in the gene body and slightly more frequently in promoters and terminators, confirming the results observed in Arabidopsis (Choi et al 2013) as well as in avian (Singhal et al 2015;Smeds et al 2016) and in Saccharomyces species (Lam and Keeney 2015), where recombination pattern is highly conserved and localized to the promoter (TSS) and terminator (TTS) regions.…”

Section: Retrotransposons Associate With Reduced Recombination Ratesupporting

confidence: 89%

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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: Retrotransposons Associate With Reduced Recombination Ratesupporting

confidence: 89%

“…In avian (Singhal et al 2015;Smeds et al 2016) and in Saccharomyces species (Lam and Keeney 2015), recombination patterns are highly conserved during evolution. This led us to assay using another approach to reveal historical recombination using LD and coalescent theory (r-map) (Li and Stephens 2003;Crawford et al 2004) in wheat.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2017

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“…However, there is almost no overlap with hotspots that occur in mice with functional PRDM9, and these DSBs occur preferentially at promoters and CpG-rich regions of the genome (Brick et al 2012). This pattern is similar to that in other species lacking PRDM9 , including birds (Singhal et al 2015), and yeast (Lam and Keeney 2015). …”

supporting

confidence: 84%

A Pedigree-Based Map of Recombination in the Domestic Dog Genome

Campbell

Bhérer

Morrow

et al. 2016

G3 Genes|Genomes|Genetics

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Meiotic recombination in mammals has been shown to largely cluster into hotspots, which are targeted by the chromatin modifier PRDM9. The canid family, including wolves and dogs, has undergone a series of disrupting mutations in this gene, rendering PRDM9 inactive. Given the importance of PRDM9, it is of great interest to learn how its absence in the dog genome affects patterns of recombination placement. We have used genotypes from domestic dog pedigrees to generate sex-specific genetic maps of recombination in this species. On a broad scale, we find that placement of recombination events in dogs is consistent with that in mice and apes, in that the majority of recombination occurs toward the telomeres in males, while female crossing over is more frequent and evenly spread along chromosomes. It has been previously suggested that dog recombination is more uniform in distribution than that of humans; however, we found that recombination in dogs is less uniform than in humans. We examined the distribution of recombination within the genome, and found that recombination is elevated immediately upstream of the transcription start site and around CpG islands, in agreement with previous studies, but that this effect is stronger in male dogs. We also found evidence for positive crossover interference influencing the spacing between recombination events in dogs, as has been observed in other species including humans and mice. Overall our data suggests that dogs have similar broad scale properties of recombination to humans, while fine scale recombination is similar to other species lacking PRDM9.

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“…Some genomic regions, encompassing tens to hundreds of kb, experience more or less DSB formation than others, and within such DSB-"hot" and DSB-"cold" domains, DSBs are particularly enriched in small (typically <250 bp) regions known as "hotspots." In Saccharomyces cerevisiae, most hotspots correspond to evolutionarily conserved nucleosome-depleted promoters (Lam and Keeney 2015b). However, the factors shaping the DSB landscape at larger size scales remain poorly understood, particularly those factors related to the intersecting feedback mechanisms that regulate Spo11 activity Cooper et al 2016).…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1

2016

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The Spo11-generated double-strand breaks (DSBs) that initiate meiotic recombination are dangerous lesions that can disrupt genome integrity, so meiotic cells regulate their number, timing, and distribution. Mechanisms of this regulation remain poorly understood. Here, we use Spo11-oligonucleotide complexes, a byproduct of DSB formation, to reveal aspects of the contribution of the Saccharomyces cerevisiae DNA damage-responsive kinase Tel1 (ortholog of mammalian ATM). A tel1Δ mutant has globally increased amounts of Spo11-oligonucleotide complexes and altered Spo11-oligonucleotide lengths, consistent with conserved roles for Tel1 in control of DSB number and processing. A kinase-dead tel1 mutation similarly increases Spo11-oligonucleotide levels but mutating known Tel1 phosphotargets on Hop1 and Rec114 does not, implicating Tel1 kinase activity and clarifying roles of Tel1 phosphorylation substrates. Deep sequencing of Spo11 oligonucleotides demonstrates that Tel1 shapes the genome-wide DSB landscape in unexpected ways. Early in meiosis, Tel1 absence causes widespread changes in DSB distributions across large chromosomal domains. Many of these changes are erased as meiosis proceeds, however, illustrating homeostatic behavior of DSB regulatory systems. We further find that effects of Tel1 are distinct but partially overlapping with previously described contributions of the recombination regulator Cst9 (also known as Zip3). Finally, we provide evidence indicating that Tel1-dependent DSB interference influences the population-average DSB landscape but also demonstrate that locally inhibitory effects of an artificial hotspot insertion can be both Tel1-independent and chromosomal context-dependent. Our findings delineate Tel1 roles in regulating number and location of DSBs and illuminate the complex interplay between Tel1 and other pathways for DSB control.

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Nonparadoxical evolutionary stability of the recombination initiation landscape in yeast

Cited by 123 publications

References 57 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

A Pedigree-Based Map of Recombination in the Domestic Dog Genome

Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1

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