Abstract
A central feature of meiosis is the pairing of homologous maternal and paternal chromosomes (‘homologues’) along their lengths1,2,3. Recognition between homologues and their juxtaposition in space is mediated by axis-associated recombination complexes. Also, pairing must occur without entanglements among unrelated chromosomes. Here we examine homologue juxtaposition in real time by four-dimensional fluorescence imaging of tagged chromosomal loci at high spatio-temporal resolution in budding yeast. We discover that corresponding loci come together from a substantial distance (1.8 µm) and complete pairing in a very short time, about 6 min (thus, rapid homologue juxtaposition or RHJ). Homologue loci first move rapidly together (in 30 s, at speeds of roughly 60 nm s−1) into an intermediate stage corresponding to canonical 400 nm axis coalignment. After a short pause, crossover/non-crossover differentiation (crossover interference) mediates a second short, rapid transition that ultimately gives close pairing of axes at 100 nm by means of synaptonemal complex formation. Furthermore, RHJ (1) occurs after chromosomes acquire prophase chromosome organization, (2) is nearly synchronous over thirds of chromosome lengths, but (3) is asynchronous throughout the genome. Finally, cytoskeleton-mediated movement is important for the timing and distance of RHJ onset and for ensuring its normal progression. General implications for local and global aspects of pairing are discussed.
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Data availability
Primary datasets are available at Harvard Dataverse (https://dataverse.harvard.edu/dataverse/TadasuNozaki_RHJ_2024). Source data are provided with this paper.
Code availability
Custom code for low-SNR microscopy system has been previously published and is available online (https://github.com/frdchang/fcMatlabTools)12,51.
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Acknowledgements
We thank members of the Kleckner laboratory and D. Zickler for advice and discussions, and D. Zickler for help with Extended Data Fig. 10. This research, T.N., B.W. and N.K. were supported by a grant to N.K. from the National Institutes of Health (grant no. R35 GM136322). T.N. was supported by fellowships from Japan Society for the Promotion of Science and Charles A. King Trust.
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T.N. and N.K. conceived and designed the experiments. T.N. and B.W. constructed the strains. T.N. performed imaging and data analysis. All authors contributed to writing the article and approved the submitted version.
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Extended data figures and tables
Extended Data Fig. 1 Long-timescale imaging of homologous loci during meiosis.
a. An example of image processing of low SNR wide field fluorescence signals. The left figure is the raw data (after cell segmentation), and the right figure is the same image processed with the “A1” algorithm51, shown at the same Z-position. The scale bar is 2 µm. b-g. Trajectories of homolog loci through meiosis. b, e. Two representative kymographs of lys2 homolog loci based on the imaging data at 1-min intervals. The meiosis I division and meiosis II division time points are indicated by the white lines. c, f. Plots of 3D distances between homologous loci throughout meiosis until the MI division. d, g. The motion of the green spot in 3D at 1 min intervals was plotted. The orange line indicates the time point of the onset of rapid chromosome motion and the blue triangle indicates the time point of RHJ onset as defined in panels c, f. This comparison illustrates the fact that motion initiates well before RHJ onset (~30 and ~60 min in these two examples). h. The cumulative percentage of cells that have undergone RHJ onset and MI as a function of time after initiation of meiosis by transfer of cells to SPM, defined at 1 min resolution (n = 18 cells). Times at which 50% of cells achieve RHJ onset and MI are indicated.
Extended Data Fig. 2 RHJ is a general process in meiotic budding yeast.
a. The list of the fluorescent spot labeling used in this study with genomic and physical length. The physical length was estimated from the imaging of spread chromosomes in our previous paper47. The data of 3D spot distances from 60 cells were derived from 6 locus pairs: lys2-lys2 (n = 14 cells), hmr-hmr (n = 10 cells), tma16-tma16 (n = 11 cells), his4leu2-his4leu2 (n = 8 cells), scp1-scp1 (n = 9 cells), and cen15-cen15 (n = 8 cells). b. The representative 3D distance plots exhibit RHJ at each locus. Each line indicates the average value at the far apart stage (before RHJ, cyan), intermediate stage (orange), and close pairing stage (purple). c. The example of RHJ skipping the intermediate stage (2 stages and single step RHJ). This type of RHJ was quite rare in the wild type (4/61 cells, 6 locus pairs). d. An example of RHJ with an extra stage is shown by a green line. This cell was excluded from the general analysis in Fig. 2 (data of n = 60 cells). However, this cell was included in the analysis to compare to the ndj1Δ and csm4Δ mutant cells and LatB-treated cells in Fig. 5. Such an extra stage is rarely observed in the wild type cells (1/61 cells, 6 locus pairs). e. The example of RHJ with temporary recoiling to the intermediate after the close pairing. Cells with the homologous loci close to CenXV sometimes showed this pattern. However, this pattern could not be observed in other strains (5/61 cells, 6 locus pair but all of five cells were cen15 loci).
Extended Data Fig. 3 Analysis process of 3D distance changes.
a. The step detection process with 2 stages (left) and 3 stages (right). b. Stages detected by the algorithm, RHJ onset/end, total pairing time, max speed of distance change, and transitions are summarized. The detailed process to detect the onset timing of the RHJ (local maximum, peak) and RHJ endpoint (local minimum, valley) is described in Materials and Methods (local maximum/minimum search). The 3D distance plot was created with a slight modification of real data to allow a clear outline of the process.
Extended Data Fig. 4 Total pairing time and RHJ onset distance for each locus.
a, b. Distributions of the total pairing time (a) and the RHJ onset distance (b) for each locus are shown with average values among cells.
Extended Data Fig. 5 The detail of distance change analysis of lys2 homologous loci.
a. The distribution of distance change of homologous loci at G1/G0 (top), before RHJ (middle) and the maximum change in distances between homologous loci at the transitions from the far apart to the intermediate (brown) and from the intermediate to the close pairing (light green). Triangles indicate the average. Averages ± standard deviations are indicated. b. The lines of mean square change in distance (MSCD) at G1/G0 (black) and before RHJ (cyan) were shown with 95 % confidence intervals. The lines of square change in distance for each trajectory from the RHJ onset to the start of intermediate (brown) and from the end of intermediate to close pairing (light green) were also plotted. All lines of square change in distance from the RHJ onset to the start of intermediate exceeded the MSCD for the time points before RHJ (14/14 trajectories, brown). Most of the lines of square change in distance from the end of intermediate to the close pairing exceeded the MSCD for the time points before RHJ (9/14 trajectories, light green). The analysis shown here strongly implies the active process underlying the RHJ. Every data shown here was based on lys2 homologous loci.
Extended Data Fig. 6 Comparison of the distribution of inter-spot distances at the local maxima that immediately precede pairing with those at local maxima that occur earlier in the time series.
a. Analysis. (left) Example of primary data with times preceding the intermediate stage (“far apart stage”) in cyan; times defining the intermediate stage in orange; and the time of RHJ onset, defined as the local maximum of inter-spot distance immediately preceding the intermediate stage (asterisk). To define this local maximum, distances were scanned from the time the intermediate stage begins (t = 0 in the left panel) “backwards” through earlier time points until the first local maximum is encountered (details in Materials and Methods). Onset distances defined in this way for all cells at all analyzed loci are shown in Extended Data Fig. 4b. (right) Other local maxima in the same time series, at times earlier than the one that defines RHJ onset, were identified analogously. In effect, each position along the curve for the far apart stage was used at the starting point for a scan of immediately preceding points, analogously to the approach used to define the RHJ onset local maximum. In many cases, adjacent start points give the same preceding local maximum (indicated for several examples by horizontal blue lines). Local maxima for the illustrated example are circled and the start points that give each local maximum are indicated by horizontal lines. To ensure that fluctuations at the very beginning of the time series were detected, the data for the far apart stage was duplicated (blue horizontal arrows). b. The distribution of inter-spot distances defined at 6 loci (n = 60 cells) for (i) the local maximum that defines RHJ onset in each cell (orange); and (ii) all local maxima at time points preceding RHJ in the same cells (blue). (Analogous to data for lys2 in text Fig. 2i). P-value for the difference in variances = 0.02 (two-sided F-test).
Extended Data Fig. 7 Analysis of the distance between chromosome axes in electron microscopy image of zip1Δ mutant cell.
Data was based on the paper of ref. 25. The white lines in the left figure and the green lines in the right figure are at the same position and these lines are used to measure the distance between chromosome axes. The scale bar in the left figure is 1 µm (original) and the scale bars in the right figure are 500 nm (added by this study). Figure adapted with permission from ref. 25, Elsevier.
Extended Data Fig. 8 Multiple spots imaging for RHJ onset timing and chromosome shortening.
a. The procedure of the longitudinal distance analysis for fluorescent loci along the chromosomes. There are two combinations of green and magenta spots (blue lines and orange dotted lines) when every four spots are separately observed. The combination of the spots along the same chromosomes is estimated by the minimization of the maximum distance between spots (e.g., 1.9 µm vs 0.7 µm -> 0.7 µm in the figure). b. The longitudinal spots analysis on the single chromosome labeling. The red line is the average in 10 min. The chromosome shortening timing is indicated by a blue dotted line. The average distance after the chromosome shortening was 0.46 µm and plotted by cyan line. After the chromosome shortening, the distance between spots along the chromosome was maintained stably until the MI division with a small fluctuation. c-h. The representative examples of pairing at multiple spots along the chromosomes. c. hmr-his4leu2 pairing along chromosome IIIs. d. gsp2-scp1 pairing along chromosome XVs. e. gsp2-cen15 pairing along chromosome XVs. f. The unsynchronized case of ade2-tma16 pairing. g, h. The unsynchronized cases of pairing at different chromosomes.
Extended Data Fig. 9 Details of RHJ in conditions where chromosome motion is compromised.
a. Treatment of cells with LatB stops the progression of meiosis and/or leads to death of cells during long timescale imaging. Thus, for this condition, instead of the long timescale imaging used for ndj1Δ, and csm4Δ mutants (from 1.5 h to 8 h after initiation of meiosis), we evaluated the progression of the pairing in LatB-treated cells by short timescale imaging (from 3 h to 5 h after initiation of meiosis). A representative example of a LatB-treated nucleus in which homologous lys2 loci remain unpaired until 5 h in meiosis is shown. ~50% of LatB-treated cells show this pattern, implying that RHJ onset is significantly delayed (or, possibly, never occurred). b. Distribution of RHJ onset distances between homolog lys2 loci in wild-type cells, ndj1Δ, and csm4Δ mutant cells, and LatB-treated cells (as in Fig. 5d) but with cells exhibiting more than one intermediate stage (an extra stage) indicated as gray filled circles. Bar indicates average value. The detailed descriptions about Fig. 5a,b analysis: Motion in ndj1Δ resembles that in mitotic cells, in accord with complete abrogation of the entire meiotic apparatus due to absence of meiosis-specific telomere/nuclear envelope association (Fig. 5a). csm4Δ exhibits less motion than ndj1Δ; and motion in LatB is most severely reduced (Fig. 5a,b). In these latter cases, telomere/nuclear envelope associations are still intact but are, apparently, less mobile in csm4Δ. In the presence of LatB, chromosomes and their ends are virtually motionless (see also ref. 12).
Extended Data Fig. 10 Unique 3D reconstruction of homolog pairs in an early zygotene lily nucleus exhibit two types of regions.
Two chromosomes among 12 from a 3D electron microscopy reconstruction of lily nucleus with partial synapsis (SC)44. Data was based on the paper of ref. 44. Only two types of pairing configurations occur: (I) Regions in which segments of SC alternate with homolog segments in close proximity (magenta). (II) Regions in which homologs are widely separated and, often, in unrelated parts of the nucleus (blue). We propose that Type I regions are created by nucleation and progression of RHJ, with RHJ in one region enabling RHJ in nearby regions and that continuation of this process into Type II regions “reels homologs together” to complete pairing/synapsis such that “pairing promotes pairing”. Figure adapted from ref. 44, Springer Nature.
Supplementary information
Supplementary Information
This file contains legends of Supplementary Videos 1–8 and Table 1.
Supplementary Video 1
The long-timescale imaging of lys2 homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic prophase (2 h in SPM to MI/MII divisions). The 3D-stack images were taken once per 1 min.
Supplementary Video 2
The short-timescale imaging of lys2 homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic prophase (2.5–4.5 h in SPM). The 3D-stack images were taken once per 10 s.
Supplementary Video 3
The short-timescale imaging of hmr homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic prophase (2.5–4.5 h in SPM). The 3D-stack images were taken once per 10 s.
Supplementary Video 4
The short-timescale imaging of lys2 homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic pachytene stage in the ndt80Δ mutant cell (8–8.5 h in SPM). The 3D-stack images were taken once per 10 s.
Supplementary Video 5
The long-timescale imaging of ade2-tma16 homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic prophase (2 h in SPM to MI division). The 3D-stack images were taken once per 1 min.
Supplementary Video 6
The long-timescale imaging of hmr-his4leu2 homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic prophase (2 h in SPM to MI division). The 3D-stack images were taken once per 1 min.
Supplementary Video 7
The long-timescale imaging of lys2/lys2 and hmr/hmr homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic prophase (1.5 h in SPM to MI division). The 3D-stack images were taken once per 1 min.
Supplementary Video 8
The short-timescale imaging of lys2 homologous loci labelled by lacO array/LacI–mEGFP (green) and tetO array/TetR–mCherry (magenta) at meiotic prophase in the ndj1 mutant cell (4–5 h in SPM). The 3D-stack images were taken once per 10 s.
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Nozaki, T., Weiner, B. & Kleckner, N. Rapid homologue juxtaposition during meiotic chromosome pairing. Nature (2024). https://doi.org/10.1038/s41586-024-07999-5
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DOI: https://doi.org/10.1038/s41586-024-07999-5
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