Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM

Anderson, Carol M.; Oke, Ashwini; Yam, Phoebe; Zhuge, Tangna; Fung, Jennifer C.

doi:10.1371/journal.pgen.1005478

Cited by 53 publications

(74 citation statements)

References 78 publications

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“…Quantification of Spo11-oligo complexes reinforces the conclusion that more DSBs form when Tel1 is missing in S. cerevisiae, which was indicated by many studies (Zhang et al 2011;Carballo et al 2013;Anderson et al 2015;Garcia et al 2015) but not all (Argunhan et al 2013;Blitzblau and Hochwagen 2013). However, although it is now clear that Tel1/ATM has an evolutionarily conserved function in regulating DSB numbers, the mechanism remains poorly understood.…”

Section: Discussionsupporting

confidence: 63%

“…1C), indicating that the increased Spo11-oligo levels are not a consequence of either increased DSBs or altered Spo11-oligo-complex lifespan caused by delayed meiotic progression. Thus, quantification of Spo11-oligo complexes, combined with prior analyses of recombination products (Zhang et al 2011;Anderson et al 2015) and some physical analyses of broken genomic DNA (Carballo et al 2013;Garcia et al 2015), supports the conclusion that loss of Tel1 increases DSBs globally. Furthermore, the kinetics of accumulation of Spo11-oligo complexes (Fig.…”

Section: Resultssupporting

confidence: 56%

“…Analysis of recombination products (Anderson et al 2015) supported an earlier hypothesis that Tel1 shapes the DSB landscape (Lange et al 2011), but recombination maps are indirect and low-spatial-resolution indicators of DSB positions. We deep-sequenced Spo11 oligos purified from wild-type and tel1Δ cultures at 4 h in sporulation conditions, when DSBs are maximal in wild type and the tel1Δ mutant has only slightly elevated total Spo11-oligo levels, and at 5 h and 6 h, when the tel1Δ mutant has substantially elevated Spo11 oligos ( Fig.…”

Section: Altered Spo11-oligo Sizes In Tel1 Mutantsmentioning

confidence: 53%

“…Furthermore, over smaller distances (less than ∼10-15 kb), multiple cutting occurs in the absence of Tel1 at substantially elevated frequency compared to expectation from random, indicating that Tel1 normally restrains a tendency for Spo11 to generate clusters of DSBs (Garcia et al 2015). ATM/Tel1 action may also ensure that DSBs rarely form at the same location on both sister chromatids (Lange et al 2011;Anderson et al 2015;Garcia et al 2015).…”

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

confidence: 97%

“…Testes from Atm −/− mice display a large increase in DSB numbers, as indicated by a >10-fold rise in the amount of covalent SPO11-oligonucleotide (oligo) complexes, a quantitative by-product of meiotic DSB formation (Lange et al 2011). In Drosophila melanogaster oocytes, mutation of ATM elevates numbers of DSB-associated γ-H2AV foci (Joyce et al 2011), and in S. cerevisiae, Tel1 loss increases recombination at the HIS4LEU2 hotspot (Zhang et al 2011) and genome-wide (Anderson et al 2015). In a rad50S background, in which unrepaired DSBs accumulate, more DSBs are observed at HIS4LEU2 and on at least one whole chromosome (Carballo et al 2013;Garcia et al 2015), although such increases were not apparent on all chromosomes (Argunhan et al 2013;Blitzblau and Hochwagen 2013;Garcia et al 2015).…”

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

confidence: 99%

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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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Section: Discussionsupporting

confidence: 63%

Section: Resultssupporting

confidence: 56%

Section: Altered Spo11-oligo Sizes In Tel1 Mutantsmentioning

confidence: 53%

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

confidence: 97%

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

confidence: 99%

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Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1

2016

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Genome wide analysis of meiotic recombination in yeast: For a few SNPs more

et al. 2018

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Diploid organisms undergo meiosis to produce haploid germ cells. Crossover events during meiosis promote genetic diversity and facilitate accurate chromosome segregation. The baker's yeast Saccharomyces cerevisiae is extensively used as a model for analysis of meiotic recombination. Conventional methods for measuring recombination events in S. cerevisiae have been limited by the number and density of genetic markers. Next generation sequencing (NGS)‐based analysis of hybrid yeast genomes bearing thousands of heterozygous single nucleotide polymorphism (SNP) markers has revolutionized analysis of meiotic recombination. By facilitating analysis of marker segregation in the whole genome with unprecedented resolution, this method has resulted in the generation of high‐resolution recombination maps in wild‐type and meiotic mutants. These studies have provided novel insights into the mechanism of meiotic recombination. In this review, we discuss the methodology, challenges, insights and future prospects of using NGS‐based methods for whole genome analysis of meiotic recombination. The objective is to facilitate the use of these high through‐put sequencing methods for the analysis of meiotic recombination given their power to provide significant new insights into the process. © 2018 The Authors. IUBMB Life published by Wiley Periodicals, Inc. on behalf of International Union of Biochemistry and Molecular Biology, 70(8):743–752, 2018

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Meiosis and male fertility in F1 interspecific hybrids (Passiflora vitifolia vs. Passiflora hatschbachii)

Souza

Silva

et al. 2022

Euphytica

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Interspeci c hybrids can be studied using methodologies in which the male gamete with high reproduction potential, viability, and fertility is prioritized. Passi ora species, with lush, showy, and exotic colors, have great potential for the ornamental plant market. In addition, arti cial Passi ora hybrids were developed without many di culties because of weak reproductive barriers. Thus, meiotic and post-meiotic behaviors were analyzed with 2% acetic carmine staining. Con rmation of interspeci c hybridization was performed using SSR markers and GISH technique was used to detect genomic differentiation. The pollen viability of the parental and hybrids genotypes was tested using Alexander solution, uorescein diacetate and in vitro germination tests were performed using culture medium. The meiotic behavior was regular and displayed haploid number n = 9 with nine bivalent (II) chromosomal, pairing in 90% of the cells in diakinesis. There was a signi cant difference (p < 0.05) in terminal and interstitial chiasma frequencies. Meiotic irregularities observed were as follows: early and/or delayed chromosomes, disorientation of spindle bers, transverse spindles, tripolar spindles, and asynchrony; and consequently irregular post-meiotic products were observed: monads, dyads, triads, and polyads. GISH was used in the interspeci c hybrids and pairing between homeologous chromosomes, and bivalent and tetravalent formation were observed. From this study, we could conclude that hybrid genotypes are fertile and pollen grains are viable and can be used in breeding programs. We also hypothesize that interspeci c hybrid genotypes of Passi ora can be obtained with regular meiosis, which could be viable and fertile.

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Reduced Crossover Interference and Increased ZMM-Independent Recombination in the Absence of Tel1/ATM

Cited by 53 publications

References 78 publications

Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1

Numerical and spatial patterning of yeast meiotic DNA breaks by Tel1

Genome wide analysis of meiotic recombination in yeast: For a few SNPs more

Meiosis and male fertility in F1 interspecific hybrids (Passiflora vitifolia vs. Passiflora hatschbachii)

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