scholarly journals Recombination patterns in maize reveal limits to crossover homeostasis

2015 ◽  
Vol 112 (52) ◽  
pp. 15982-15987 ◽  
Author(s):  
Gaganpreet K. Sidhu ◽  
Celestia Fang ◽  
Mischa A. Olson ◽  
Matthieu Falque ◽  
Olivier C. Martin ◽  
...  

During meiotic recombination, double-strand breaks (DSBs) are formed in chromosomal DNA and then repaired as either crossovers (COs) or non–crossovers (NCOs). In most taxa, the number of DSBs vastly exceeds the number of COs. COs are required for generating genetic diversity in the progeny, as well as proper chromosome segregation. Their formation is tightly controlled so that there is at least one CO per pair of homologous chromosomes whereas the maximum number of COs per chromosome pair is fairly limited. One of the main mechanisms controlling the number of recombination events per meiosis is CO homeostasis, which maintains a stable CO number even when the DSB number is dramatically altered. The existence of CO homeostasis has been reported in several species, including mouse, yeast, and Caenorhabditis elegans. However, it is not known whether homeostasis exists in the same form in all species. In addition, the studies of homeostasis have been conducted using mutants and/or transgenic lines exhibiting fairly severe meiotic phenotypes, and it is unclear how important homeostasis is under normal physiological conditions. We found that, in maize, CO control is robust only to ensure one CO per chromosome pair. However, once this limit is reached, the CO number is linearly related to the DSB number. We propose that CO control is a multifaceted process whose different aspects have a varying degree of importance in different species.

2018 ◽  
Vol 156 (2) ◽  
pp. 106-116
Author(s):  
Kimberly M. Davenport ◽  
Stephanie McKay ◽  
Alan G. Fahey ◽  
Clare Gill ◽  
Brenda M. Murdoch

Meiotic recombination is an important contributor to genetic variation and ensures proper chromosome segregation during gametogenesis. Previous studies suggest that at least 1 crossover (CO) per chromosome arm is important to avoid mis-segregation. While the total number of COs per spermatocyte is known to differ in mice, this is only beginning to be evaluated in sheep. This study used a cytogenetic approach to quantify and compare the number of COs per spermatocyte in rams from 3 breeds of sheep: Suffolk, Icelandic, and Targhee. In total, 2,758 spermatocytes and over 170,000 COs were examined. Suffolk rams exhibited the lowest mean number of COs (61.1 ± 0.15) compared to Icelandic (63.5 ± 0.27) and Targhee (65.9 ± 0.26) rams. Significant differences in the number of COs per spermatocyte were observed between Suffolk, Icelandic, and Targhee breeds as well as within each breed. Additionally, the number and location of COs were characterized for homologous chromosomes in a subset of spermatocytes for each ram. A positive correlation was identified between the number of COs and the length of the homologous chromosome pair. Suffolk and Icelandic rams exhibited up to 7 COs per chromosome, while Targhee rams exhibited up to 9. Further, distinct CO location preferences on homologous chromosome pairs with 1, 2, 3, and 4 COs were observed in all 3 breeds. These data in sheep will aid in elucidating the mechanism of mammalian meiotic recombination, an important contributor to genetic diversity.


2006 ◽  
Vol 26 (10) ◽  
pp. 3683-3694 ◽  
Author(s):  
Hsin-Yen Wu ◽  
Sean M. Burgess

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.


2018 ◽  
Vol 115 (10) ◽  
pp. 2437-2442 ◽  
Author(s):  
Heïdi Serra ◽  
Christophe Lambing ◽  
Catherine H. Griffin ◽  
Stephanie D. Topp ◽  
Divyashree C. Nageswaran ◽  
...  

During meiosis, homologous chromosomes undergo reciprocal crossovers, which generate genetic diversity and underpin classical crop improvement. Meiotic recombination initiates from DNA double-strand breaks (DSBs), which are processed into single-stranded DNA that can invade a homologous chromosome. The resulting joint molecules can ultimately be resolved as crossovers. In Arabidopsis, competing pathways balance the repair of ∼100–200 meiotic DSBs into ∼10 crossovers per meiosis, with the excess DSBs repaired as noncrossovers. To bias DSB repair toward crossovers, we simultaneously increased dosage of the procrossover E3 ligase gene HEI10 and introduced mutations in the anticrossovers helicase genes RECQ4A and RECQ4B. As HEI10 and recq4a recq4b increase interfering and noninterfering crossover pathways, respectively, they combine additively to yield a massive meiotic recombination increase. Interestingly, we also show that increased HEI10 dosage increases crossover coincidence, which indicates an effect on interference. We also show that patterns of interhomolog polymorphism and heterochromatin drive recombination increases distally towards the subtelomeres in both HEI10 and recq4a recq4b backgrounds, while the centromeres remain crossover suppressed. These results provide a genetic framework for engineering meiotic recombination landscapes in plant genomes.


1997 ◽  
Vol 139 (2) ◽  
pp. 459-467 ◽  
Author(s):  
Carol A. Bascom-Slack ◽  
Dean S. Dawson

The recognition and alignment of homologous chromosomes early in meiosis is essential for their subsequent segregation at anaphase I; however, the mechanism by which this occurs is unknown. We demonstrate here that, in the absence of the molecular motor, Kar3p, meiotic cells are blocked with prophase monopolar microtubule arrays and incomplete synaptonemal complex (SC) formation. kar3 mutants exhibit very low levels of heteroallelic recombination. kar3 mutants do produce double-strand breaks that act as initiation sites for meiotic recombination in yeast, but at levels severalfold reduced from wild-type. These data are consistent with a meiotic role for Kar3p in the events that culminate in synapsis of homologues.


2021 ◽  
Vol 134 (4) ◽  
pp. jcs253518 ◽  
Author(s):  
Mélody Wintrebert ◽  
Mai-Chi Nguyen ◽  
Gerald R. Smith

ABSTRACTMeiotic recombination forms crossovers important for proper chromosome segregation and offspring viability. This complex process involves many proteins acting at each of the multiple steps of recombination. Recombination initiates by formation of DNA double-strand breaks (DSBs), which in the several species examined occur with high frequency at special sites (DSB hotspots). In Schizosaccharomyces pombe, DSB hotspots are bound with high specificity and strongly activated by linear element (LinE) proteins Rec25, Rec27 and Mug20, which form colocalized nuclear foci with Rec10, essential for all DSB formation and recombination. Here, we test the hypothesis that the nuclear localization signal (NLS) of Rec10 is crucial for coordinated nuclear entry after forming a complex with other LinE proteins. In NLS mutants, all LinE proteins were abundant in the cytoplasm, not the nucleus; DSB formation and recombination were much reduced but not eliminated. Nuclear entry of limited amounts of Rec10, apparently small enough for passive nuclear entry, can account for residual recombination. LinE proteins are related to synaptonemal complex proteins of other species, suggesting that they also share an NLS, not yet identified, and undergo protein complex formation before nuclear entry.This article has an associated First Person interview with Mélody Wintrebert, joint first author of the paper.


2021 ◽  
Author(s):  
Nataliya E. Yelina ◽  
Sabrina Gonzalez-Jorge ◽  
Dominique Hirsz ◽  
Ziyi Yang ◽  
Ian R. Henderson

AbstractDuring meiosis, homologous chromosomes pair and recombine, which can result in reciprocal crossovers that increase genetic diversity. Crossovers are unevenly distributed along eukaryote chromosomes and show repression in heterochromatin and the centromeres. Within the chromosome arms crossovers are often concentrated in hotspots, which are typically in the kilobase range. The uneven distribution of crossovers along chromosomes, together with their low number per meiosis, creates a limitation during crop breeding, where recombination can be beneficial. Therefore, targeting crossovers to specific genome locations has the potential to accelerate crop improvement. In plants, meiotic crossovers are initiated by DNA double strand breaks (DSBs) that are catalysed by SPO11 complexes, which consist of two catalytic (SPO11-1 and SPO11-2) and two non-catalytic subunits (MTOPVIB). We used the model plant Arabidopsis thaliana to target a dCas9-MTOPVIB fusion protein to the 3a crossover hotspot via CRISPR. We observed that this was insufficient to significantly change meiotic crossover frequency or pattern within 3a. We discuss the implications of our findings for targeting meiotic recombination within plant genomes.


2006 ◽  
Vol 26 (8) ◽  
pp. 2913-2923 ◽  
Author(s):  
Jill M. Henry ◽  
Raymond Camahort ◽  
Douglas A. Rice ◽  
Laurence Florens ◽  
Selene K. Swanson ◽  
...  

ABSTRACT During meiosis, each chromosome must pair with its homolog and undergo meiotic crossover recombination in order to segregate properly at the first meiotic division. Recombination in meiosis in Saccharomyces cerevisiae relies on two Escherichia coli recA homologs, Rad51 and Dmc1, as well as the more recently discovered heterodimer Mnd1/Hop2. Meiotic recombination in S. cerevisiae mnd1 and hop2 single mutants is initiated via double-strand breaks (DSBs) but does not progress beyond this stage; heteroduplex DNA, joint molecules, and crossovers are not detected. Whereas hop2 and mnd1 single mutants are profoundly recombination defective, we show that mnd1 rad51, hop2 rad51, and mnd1 rad17 double mutants are able to carry out crossover recombination. Interestingly, noncrossover recombination is absent, indicating a role for Mnd1/Hop2 in the designation of DSBs for noncrossover recombination. We demonstrate that in the rad51 mnd1 double mutant, recombination is more likely to occur between repetitive sequences on nonhomologous chromosomes. Our results support a model in which Mnd1/Hop2 is required for DNA-DNA interactions that help ensure Dmc1-mediated stable strand invasion between homologous chromosomes, thereby preserving genomic integrity.


2019 ◽  
Vol 5 (1) ◽  
pp. eaau9780 ◽  
Author(s):  
Qianting Zhang ◽  
Shu-Yan Ji ◽  
Kiran Busayavalasa ◽  
Chao Yu

Segregation of homologous chromosomes in meiosis I is tightly regulated by their physical links, or crossovers (COs), generated from DNA double-strand breaks (DSBs) through meiotic homologous recombination. In budding yeast, three ZMM (Zip1/2/3/4, Mer3, Msh4/5) proteins, Zip2, Zip4, and Spo16, form a “ZZS” complex, functioning to promote meiotic recombination via a DSB repair pathway. Here, we identified the mammalian ortholog of Spo16, termed SPO16, which interacts with the mammalian ortholog of Zip2 (SHOC1/MZIP2), and whose functions are evolutionarily conserved to promote the formation of COs. SPO16 localizes to the recombination nodules, as SHOC1 and TEX11 do. SPO16 is required for stabilization of SHOC1 and proper localization of other ZMM proteins. The DSBs formed in SPO16-deleted meiocytes were repaired without COs formation, although synapsis is less affected. Therefore, formation of SPO16-SHOC1 complex–associated recombination intermediates is a key step facilitating meiotic recombination that produces COs from yeast to mammals.


2008 ◽  
Vol 180 (4) ◽  
pp. 673-679 ◽  
Author(s):  
Fang Yang ◽  
Sigrid Eckardt ◽  
N. Adrian Leu ◽  
K. John McLaughlin ◽  
Peijing Jeremy Wang

During meiosis, homologous chromosomes undergo synapsis and recombination. We identify TEX15 as a novel protein that is required for chromosomal synapsis and meiotic recombination. Loss of TEX15 function in mice causes early meiotic arrest in males but not in females. Specifically, TEX15-deficient spermatocytes exhibit a failure in chromosomal synapsis. In mutant spermatocytes, DNA double-strand breaks (DSBs) are formed, but localization of the recombination proteins RAD51 and DMC1 to meiotic chromosomes is severely impaired. Based on these data, we propose that TEX15 regulates the loading of DNA repair proteins onto sites of DSBs and, thus, its absence causes a failure in meiotic recombination.


2014 ◽  
Vol 205 (5) ◽  
pp. 633-641 ◽  
Author(s):  
J. Kim Holloway ◽  
Xianfei Sun ◽  
Rayka Yokoo ◽  
Anne M. Villeneuve ◽  
Paula E. Cohen

Meiotic crossovers (COs) are crucial for ensuring accurate homologous chromosome segregation during meiosis I. Because the double-strand breaks (DSBs) that initiate meiotic recombination greatly outnumber eventual COs, this process requires exquisite regulation to narrow down the pool of DSB intermediates that may form COs. In this paper, we identify a cyclin-related protein, CNTD1, as a critical mediator of this process. Disruption of Cntd1 results in failure to localize CO-specific factors MutLγ and HEI10 at designated CO sites and also leads to prolonged high levels of pre-CO intermediates marked by MutSγ and RNF212. These data show that maturation of COs is intimately coupled to deselection of excess pre-CO sites to yield a limited number of COs and that CNTD1 coordinates these processes by regulating the association between the RING finger proteins HEI10 and RNF212 and components of the CO machinery.


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