Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation

Sato-Carlton, Aya; Tabuchi, Chihiro; Chartrand, Stephane Kazuki; Uchino, Tomoki; Carlton, Peter M.

doi:10.1083/jcb.201707161

Cited by 44 publications

(56 citation statements)

References 68 publications

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“…While we were preparing this paper, phosphorylation of SYP-1 with a role in meiosis progression was described ( Sato-Carlton et al., 2018 ). This prompted us to test if this modification is altered in our strains.…”

Section: Resultsmentioning

confidence: 99%

“…The SC is a dynamic structure that operates during meiosis to ensure the formation of crossovers while at the same time limiting their numbers ( Colaiácovo et al., 2003 , Saito and Colaiácovo, 2017 ). Phosphorylation of SC components has been recently reported to influence changes in SC dynamics and meiotic recombination during unperturbed meiosis ( Nadarajan et al., 2017 , Sato-Carlton et al., 2018 ). Intriguingly, a previous study reported that the SC undergoes localized disassembly during the repair of IR-induced DSBs to favor rapid repair through the sister chromatid as template ( Couteau and Zetka, 2011 ).…”

Section: Discussionmentioning

confidence: 99%

“…, 2008 Rabbit SYP-1-ph Antibody The P. Carlton lab. Sato-Carlton et al., 2018 Guinea Pig ZHP-3 The S. Boulton lab Bhalla et al., 2008 Bacterial Strains Escherichia coli DH5a chemically competent cells N/A N/A One Shot ccdB Survival 2T1 chemically competent cells Invitrogen # A10460 Chemicals, Peptides, and Recombinant Proteins Alkaline Phosphatase Roche 713 023 Caffeine Sigma C0750 Vectashield Vector Laboratories H-1000 4,6-Diamidino-2-phenylindole dihydrochloride (DAPI) Sigma D9542 Peptide array (19-mer peptides on cellulose membrane) N/A N/A Phusion High-Fidelity DNA polymerase NEB M0530S MyTaq BIOLINE BIO-21107 MaeIII Roche 10822230001 BstAPI NEB R0654S Hpy188 NEB R0617S Experimental Models: Organisms/Strains C. elegans : Strain N2: wild-type Bristol CGC WB Strain: N2 C. elegans : Strain AV307: syp -1(me17) V/nT1[ unc -? (n754) let -?…”

Section: Methodsmentioning

confidence: 99%

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A Meiotic Checkpoint Alters Repair Partner Bias to Permit Inter-sister Repair of Persistent DSBs

et al. 2019

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SummaryAccurate meiotic chromosome segregation critically depends on the formation of inter-homolog crossovers initiated by double-strand breaks (DSBs). Inaccuracies in this process can drive aneuploidy and developmental defects, but how meiotic cells are protected from unscheduled DNA breaks remains unexplored. Here we define a checkpoint response to persistent meiotic DSBs in C. elegans that phosphorylates the synaptonemal complex (SC) to switch repair partner from the homolog to the sister chromatid. A key target of this response is the core SC component SYP-1, which is phosphorylated in response to ionizing radiation (IR) or unrepaired meiotic DSBs. Failure to phosphorylate (syp-16A) or dephosphorylate (syp-16D) SYP-1 in response to DNA damage results in chromosome non-dysjunction, hyper-sensitivity to IR-induced DSBs, and synthetic lethality with loss of brc-1BRCA1. Since BRC-1 is required for inter-sister repair, these observations reveal that checkpoint-dependent SYP-1 phosphorylation safeguards the germline against persistent meiotic DSBs by channelling repair to the sister chromatid.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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A Meiotic Checkpoint Alters Repair Partner Bias to Permit Inter-sister Repair of Persistent DSBs

et al. 2019

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“…During late meiotic prophase, SC components were found to remain associated with chromosome subdomains in diverse organisms ( Bisig et al, 2012 ; Gladstone et al, 2009 ; Nabeshima et al, 2005 ; Newnham et al, 2010 ; Qiao et al, 2012 ; Takeo et al, 2011 ); however, the molecular consequences for such retention are not clear. In Caenorhabditis elegans , although asymmetric SC disassembly accompanies chromosome remodeling and the establishment of bivalent asymmetry required for their accurate segregation ( de Carvalho et al, 2008 ; Martinez-Perez et al, 2008 ; Sato-Carlton et al, 2018 ; Tzur et al, 2012 ), the requirement for the maintenance of SC components during this process is not known.…”

Section: Introductionmentioning

confidence: 99%

Multivalent weak interactions between assembly units drive synaptonemal complex formation

Zhang

Xie

Wang

et al. 2020

Journal of Cell Biology

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The synaptonemal complex (SC) is an ordered but highly dynamic structure assembled between homologous chromosomes to control interhomologous crossover formation, ensuring accurate meiotic chromosome segregation. However, the mechanisms regulating SC assembly and dynamics remain unclear. Here, we identified two new SC components, SYP-5 and SYP-6, in Caenorhabditis elegans that have distinct expression patterns and form distinct SC assembly units with other SYPs through stable interactions. SYP-5 and SYP-6 exhibit diverse in vivo SC regulatory functions and distinct phase separation properties in cells. Charge-interacting elements (CIEs) are enriched in SC intrinsically disordered regions (IDRs), and IDR deletion or CIE removal confirmed a requirement for these elements in SC regulation. Our data support the theory that multivalent weak interactions between the SC units drive SC formation and that CIEs confer multivalency to the assembly units.

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“…Those involved in histone modifications (Sasaki et al, 2008; Xu et al, 2009; Kota et al, 2010; Greer et al, 2011; Yelina et al, 2014; Székvölyi et al, 2015; Termolino et al, 2016) are frequently associated with changes in transcription, which is one of the reasons why we expected to detect larger changes in the meiotic transcription profile. However, several PTM are also involved in the modification of other meiotic proteins (Watanabe et al, 1997; Carballo et al, 2008; Fukuda et al, 2012; Sato-Carlton et al, 2017). Most of these meiotic PTMs have been reported in yeast and mammals, where synaptonemal complex formation and recombination are regulated through PTMs such as ubiquitination and phosphorylation.…”

Section: Discussionmentioning

confidence: 99%

Genome-wide transcription during early wheat meiosis is independent of synapsis, ploidy level and thePh1locus

Martín

Borrill

Higgins

et al. 2018

Preprint

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Polyploidization is a fundamental process in plant evolution. One of the biggest challenges faced by a new polyploid is meiosis, particularly discriminating between multiple related chromosomes so that only homologous chromosomes synapse and recombine to ensure regular chromosome segregation and balanced gametes. Despite its large genome size, high DNA repetitive content and similarity between homoeologous chromosomes, hexaploid wheat completes meiosis in a shorter period than diploid species with a much smaller genome. Therefore, during wheat meiosis, mechanisms additional to the classical model based on DNA sequence homology, must facilitate more efficient homologous recognition. One such mechanism could involve exploitation of differences in chromosome structure between homologues and homoeologues at the onset of meiosis. In turn, these chromatin changes, can be expected to be linked to transcriptional gene activity. In this study, we present an extensive analysis of a large RNA-Seq data derived from six different genotypes: wheat, wheat-rye hybrids and newly synthesized octoploid triticale, both in the presence and absence of the Ph1 locus. Plant material was collected at early prophase, at the transition leptotene-zygotene, when the telomere bouquet is forming and synapsis between homologues is beginning. The six genotypes exhibit different levels of synapsis and chromatin structure at this stage; therefore, recombination and consequently segregation, are also different. Unexpectedly, our study reveals that neither synapsis, whole genome duplication nor the absence of the Ph1 locus are associated with major changes in gene expression levels during early meiotic prophase. Overall wheat transcription at this meiotic stage is therefore highly resilient to such alterations, even in the presence of major chromatin structural changes. This suggests that post-transcriptional and post-translational processes are likely to be more important. Thus, further studies will be required to reveal whether these observations are specific to wheat meiosis, and whether there are significant changes in post-transcriptional and post-translational modifications in wheat and other polyploid species associated with their polyploidisation.

show abstract

Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation

Cited by 44 publications

References 68 publications

A Meiotic Checkpoint Alters Repair Partner Bias to Permit Inter-sister Repair of Persistent DSBs

A Meiotic Checkpoint Alters Repair Partner Bias to Permit Inter-sister Repair of Persistent DSBs

Multivalent weak interactions between assembly units drive synaptonemal complex formation

Genome-wide transcription during early wheat meiosis is independent of synapsis, ploidy level and thePh1locus

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