Crossover Position Drives Chromosome Remodeling for Accurate Meiotic Chromosome Segregation

Altendorfer, Elisabeth; Lascarez-Lagunas, Laura I; Nadarajan, Saravanapriah; Mathieson, Iain; Colaiácovo, Mónica P.

doi:10.1016/j.cub.2020.01.079

Cited by 34 publications

(25 citation statements)

References 66 publications

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“…Moreover, a recent C . elegans study has found that the asymmentric placement of the crossover along the chromosome is important for proper chromosome remodeling and segregation [ 42 ]. Perhaps the acquisition of holocentric chromosomes requires extreme crossover interference in addition to asymmetric placement of a crossover along the chromosome length.…”

Section: Discussionmentioning

confidence: 99%

“…One way that C. elegans counteract this problem is the asymmetric positioning of a single crossover along the length of a chromosome; this generates a single point of organization along the length of each chromosome, which patterns the chromosome in a manner that facilitates chromosome biorientation, alignment, release of cohesion, and segregation [40,41]. Moreover, a recent C. elegans study has found that the asymmentric placement of the crossover along the chromosome is important for proper chromosome remodeling and segregation [42]. Perhaps the acquisition of holocentric chromosomes requires extreme crossover interference in addition to asymmetric placement of a crossover along the chromosome length.…”

Section: Crossover Interference and Holocentric Chromosomesmentioning

confidence: 99%

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Excess crossovers impede faithful meiotic chromosome segregation in C. elegans

et al. 2020

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During meiosis, diploid organisms reduce their chromosome number by half to generate haploid gametes. This process depends on the repair of double strand DNA breaks as crossover recombination events between homologous chromosomes, which hold homologs together to ensure their proper segregation to opposite spindle poles during the first meiotic division. Although most organisms are limited in the number of crossovers between homologs by a phenomenon called crossover interference, the consequences of excess interfering crossovers on meiotic chromosome segregation are not well known. Here we show that extra interfering crossovers lead to a range of meiotic defects and we uncover mechanisms that counteract these errors. Using chromosomes that exhibit a high frequency of supernumerary crossovers in Caenorhabditis elegans, we find that essential chromosomal structures are mispatterned in the presence of multiple crossovers, subjecting chromosomes to improper spindle forces and leading to defects in metaphase alignment. Additionally, the chromosomes with extra interfering crossovers often exhibited segregation defects in anaphase I, with a high incidence of chromatin bridges that sometimes created a tether between the chromosome and the first polar body. However, these anaphase I bridges were often able to resolve in a LEM-3 nuclease dependent manner, and chromosome tethers that persisted were frequently resolved during Meiosis II by a second mechanism that preferentially segregates the tethered sister chromatid into the polar body. Altogether these findings demonstrate that excess interfering crossovers can severely impact chromosome patterning and segregation, highlighting the importance of limiting the number of recombination events between homologous chromosomes for the proper execution of meiosis.

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Section: Discussionmentioning

confidence: 99%

Section: Crossover Interference and Holocentric Chromosomesmentioning

confidence: 99%

Excess crossovers impede faithful meiotic chromosome segregation in C. elegans

et al. 2020

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“…In the holocentric C. elegans, a single crossing-over event partitions the chromosome into the short and long arms and distributes key chromosome-associated proteins asymmetrically relative to the crossover site, eventually defining where cohesion will be released during meiosis I ( Altendorfer et al, 2020 ; Martinez-Perez et al, 2008 ; Nabeshima et al, 2005 ). While two axis components, HTP-3 and HIM-3, remain associated with all arms of chromosomes ( Zetka et al, 1999 ; Goodyer et al, 2008 ; Severson et al, 2009 ), the other axis-associated proteins, HTP-1/2 and LAB-1, become restricted to the long arm of a bivalent ( de Carvalho et al, 2008 ; Martinez-Perez et al, 2008 ).…”

Section: Introductionmentioning

confidence: 99%

Spatial and temporal control of targeting Polo-like kinase during meiotic prophase

Brandt

Hussey

Kim

2020

Journal of Cell Biology

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Polo-like kinases (PLKs) play widely conserved roles in orchestrating meiotic chromosome dynamics. However, how PLKs are targeted to distinct subcellular localizations during meiotic progression remains poorly understood. Here, we demonstrate that the cyclin-dependent kinase CDK-1 primes the recruitment of PLK-2 to the synaptonemal complex (SC) through phosphorylation of SYP-1 in C. elegans. SYP-1 phosphorylation by CDK-1 occurs just before meiotic onset. However, PLK-2 docking to the SC is prevented by the nucleoplasmic HAL-2/3 complex until crossover designation, which constrains PLK-2 to special chromosomal regions known as pairing centers to ensure proper homologue pairing and synapsis. PLK-2 is targeted to crossover sites primed by CDK-1 and spreads along the SC by reinforcing SYP-1 phosphorylation on one side of each crossover only when threshold levels of crossovers are generated. Thus, the integration of chromosome-autonomous signaling and a nucleus-wide crossover-counting mechanism partitions holocentric chromosomes relative to the crossover site, which ultimately defines the pattern of chromosome segregation during meiosis I.

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“…Meiotic recombination, which is necessary for proper chromosomal segregation, is tightly regulated by the intricate integration of programmed DSB induction, HR repair machinery and chromosomal remodelling resulting in the right proportions of CO and NCO recombinants ( Altendorfer et al, 2020 ). The frequency and distribution of COs are regulated by the still poorly understood phenomena of CO homeostasis and interference, respectively ( Wang et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

Downregulation of Barley Regulator of Telomere Elongation Helicase 1 Alters the Distribution of Meiotic Crossovers

et al. 2021

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Programmed meiotic DNA double-strand breaks (DSBs), necessary for proper chromosomal segregation and viable gamete formation, are repaired by homologous recombination (HR) as crossovers (COs) or non-crossovers (NCOs). The mechanisms regulating the number and distribution of COs are still poorly understood. The regulator of telomere elongation helicase 1 (RTEL1) DNA helicase was previously shown to enforce the number of meiotic COs in Caenorhabditis elegans but its function in plants has been studied only in the vegetative phase. Here, we characterised barley RTEL1 gene structure and expression using RNA-seq data previously obtained from vegetative and reproductive organs and tissues. Using RNAi, we downregulated RTEL1 expression specifically in reproductive tissues and analysed its impact on recombination using a barley 50k iSelect SNP Array. Unlike in C. elegans, in a population segregating for RTEL1 downregulated by RNAi, high resolution genome-wide genetic analysis revealed a significant increase of COs at distal chromosomal regions of barley without a change in their total number. Our data reveal the important role of RTEL1 helicase in plant meiosis and control of recombination.

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Crossover Position Drives Chromosome Remodeling for Accurate Meiotic Chromosome Segregation

Cited by 34 publications

References 66 publications

Excess crossovers impede faithful meiotic chromosome segregation in C. elegans

Excess crossovers impede faithful meiotic chromosome segregation in C. elegans

Spatial and temporal control of targeting Polo-like kinase during meiotic prophase

Downregulation of Barley Regulator of Telomere Elongation Helicase 1 Alters the Distribution of Meiotic Crossovers

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