A conserved filamentous assembly underlies the structure of the meiotic chromosome axis
- University of California, San Diego, United States
- Ludwig-Maximilians-Universität München, Germany
- Institute of Molecular Biology of Barcelona, Spain
- Wesleyan University, United States
Abstract
The meiotic chromosome axis plays key roles in meiotic chromosome organization and recombination, yet the underlying protein components of this structure are highly diverged. Here, we show that 'axis core proteins' from budding yeast (Red1), mammals (SYCP2/SYCP3), and plants (ASY3/ASY4) are evolutionarily related and play equivalent roles in chromosome axis assembly. We first identify 'closure motifs' in each complex that recruit meiotic HORMADs, the master regulators of meiotic recombination. We next find that axis core proteins form homotetrameric (Red1) or heterotetrameric (SYCP2:SYCP3 and ASY3:ASY4) coiled-coil assemblies that further oligomerize into micron-length filaments. Thus, the meiotic chromosome axis core in fungi, mammals, and plants shares a common molecular architecture, and likely also plays conserved roles in meiotic chromosome axis assembly and recombination control.
Data availability
Primary diffraction data for M. musculus SYCP3 tetramer structures have been deposited with the SBGrid Data Bank (https://data.sbgrid.org) under dataset numbers 583 (P21 crystal form) and 584 (P1 form).Reduced diffraction data and refined structural models have been deposited with the Protein Data Bank (www.pdb.org) under accession numbers 6DD8 (P21 crystal form) and 6DD9 (P1 form)
Article and author information
Author details
Funding
National Institutes of Health (R01 GM104141)
- Alan M V West
- Scott C Rosenberg
- Madison K Lehmer
- Qiaozhen Ye
- Kevin D Corbett
Human Frontier Science Program (RGP0008/2015)
- Franz Herzog
- Kevin D Corbett
National Science Foundation (Graduate Research Fellowship)
- Sarah N Ur
Ludwig Institute for Cancer Research
- Kevin D Corbett
National Institutes of Health (R15 GM116109)
- Amy J MacQueen
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Bernard de Massy, Institute of Human Genetics, CNRS UPR 1142, France
Version history
- Received: July 24, 2018
- Accepted: January 18, 2019
- Accepted Manuscript published: January 18, 2019 (version 1)
- Version of Record published: January 28, 2019 (version 2)
Copyright
© 2019, West et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,435
- views
-
- 552
- downloads
-
- 90
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
A conserved filamentous assembly underlies the structure of the meiotic chromosome axis
eLife 8:e40372.
https://doi.org/10.7554/eLife.40372
Further reading
-
- Chromosomes and Gene Expression
- Immunology and Inflammation
Ikaros is a transcriptional factor required for conventional T cell development, differentiation, and anergy. While the related factors Helios and Eos have defined roles in regulatory T cells (Treg), a role for Ikaros has not been established. To determine the function of Ikaros in the Treg lineage, we generated mice with Treg-specific deletion of the Ikaros gene (Ikzf1). We find that Ikaros cooperates with Foxp3 to establish a major portion of the Treg epigenome and transcriptome. Ikaros-deficient Treg exhibit Th1-like gene expression with abnormal production of IL-2, IFNg, TNFa, and factors involved in Wnt and Notch signaling. While Ikzf1-Treg-cko mice do not develop spontaneous autoimmunity, Ikaros-deficient Treg are unable to control conventional T cell-mediated immune pathology in response to TCR and inflammatory stimuli in models of IBD and organ transplantation. These studies establish Ikaros as a core factor required in Treg for tolerance and the control of inflammatory immune responses.
-
- Cell Biology
- Chromosomes and Gene Expression
Heat stress is a major threat to global crop production, and understanding its impact on plant fertility is crucial for developing climate-resilient crops. Despite the known negative effects of heat stress on plant reproduction, the underlying molecular mechanisms remain poorly understood. Here, we investigated the impact of elevated temperature on centromere structure and chromosome segregation during meiosis in Arabidopsis thaliana. Consistent with previous studies, heat stress leads to a decline in fertility and micronuclei formation in pollen mother cells. Our results reveal that elevated temperature causes a decrease in the amount of centromeric histone and the kinetochore protein BMF1 at meiotic centromeres with increasing temperature. Furthermore, we show that heat stress increases the duration of meiotic divisions and prolongs the activity of the spindle assembly checkpoint during meiosis I, indicating an impaired efficiency of the kinetochore attachments to spindle microtubules. Our analysis of mutants with reduced levels of centromeric histone suggests that weakened centromeres sensitize plants to elevated temperature, resulting in meiotic defects and reduced fertility even at moderate temperatures. These results indicate that the structure and functionality of meiotic centromeres in Arabidopsis are highly sensitive to heat stress, and suggest that centromeres and kinetochores may represent a critical bottleneck in plant adaptation to increasing temperatures.
