Abstract
The synaptonemal complex (SC) is a proteinaceous structure that forms between homologous chromosomes during meiosis prophase. The SC is widely conserved across species, but its structure and roles during meiotic recombination are still debated. While the SC central region is made up of transverse filaments and central element proteins in mammals and fungi, few central element proteins have been identified in other species. Here we report the identification of two coiled-coil proteins, SCEP1 and SCEP2, that form a complex and localize at the centre of the Arabidopsis thaliana SC. In scep1 and scep2 mutants, chromosomes are aligned but not synapsed (the ZYP1 transverse filament protein is not loaded), crossovers are increased compared with the wild type, interference is lost and heterochiasmy is strongly reduced. We thus report the identification of two plant SC central elements, and homologues of these are found in all major angiosperm clades.
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Data availability
The raw read data for Fig. 7 can be found in the EBI ArrayExpress database under accession number E-MTAB-12985 (https://www.ebi.ac.uk/biostudies/studies/E-MTAB-12985).
Code availability
The in-house R (4.2.2) scripts used in this work are available at https://github.com/mapeuch/SCEP1_SCEP2_paper.
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Acknowledgements
We thank L. Iguertsira and Z. Klising for technical help with plasmid construct and fertility characterization, and D. Charif for bioinformatic guidance in the analysis of transcriptomic data. This work has benefited from the support of the Institut Jean-Pierre Bourgin’s Plant Observatory technological platforms. This research was funded by ANR (COPATT ANR-20-CE12-0006), by core funding from the Max Planck Society and an Alexander von Humboldt Fellowship to Q.L. The Institut Jean-Pierre Bourgin benefits from the support of Saclay Plant Sciences (ANR-17-EUR-0007).
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N.V. produced all the genetic material, analysed the fertility data, produced and analysed the scep1−/− plants, produced the SCPE1 and SCEP2 proteins to obtain antibodies, and produced and analysed the immunocytology data at standard resolution. M.P. analysed the localization and distances between SC components, analysed the AlphaFold2 data and produced and analysed the SCEP1 and SCEP2 orthologue data. S.D. produced and analysed the STED immunocytology data. Q.L. analysed the sequencing data and performed the recombination, interference and aneuploidy analyses. A.C., A.H. and J.G. produced the MLH1 and HEI10 immunocytology data. R.G. produced the analysis of the SCEP1–SCEP2 complex with AlphaFold2. M.G. and R.M. contributed to the supervision and analysis of the cytological and genetic data. C.M. led the project, produced the bioinformatic analysis of the transcriptomic data and wrote the paper with input from all co-authors.
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Extended data
Extended Data Fig. 1 Description of SCEP1 and SCEP2 protein sequences in the wt and mutants.
a. SCEP1 (AT1G33500). The exon intron structure of the gene is obtained from the TAIR. The positions of the 3 gRNAs used for CRISPR-Cas9 are shown in green above the gene structure. The positions of the primers used to sequence the 3′ part of the cDNA are shown in black. b. DNA sequence of the 7 mutations obtained by CRISPR-Cas9. The sequence of each guide is presented and the PAM is underlined. scep1-1 in the Columbia background and scep1-7 in the Landsberg background are identical with an insertion of a C that creates a BamH1 restriction site (italicize). c. Protein sequence expected from the mutants obtained by CRISPR-Cas9. Amino acids in red are identical to the wt protein sequence, amino acids in grey differ from the wt due to the frame shift created by the mutations in the open reading frame. * marks the position of the STOP codon. d. SCEP2 (AT3G28370). The exon intron structure of the gene is obtained from the TAIR. The positions of the T-DNA insertions are presented below the gene structure with magenta arrows. Among the 4 T-DNA insertions, only the line N663933 (scep2-1) exhibits a meiotic phenotype. The positions of the two couple of primers used to sequence the 3′ part of the cDNA are drawn above the gene structure. e. The theoretical DNA sequence of the 3′ part of the genomic DNA between the nucleotides 10619881 and 10610599 obtained from the TAIR is written in black with exons in upper case letters. After PCR amplification and sequencing of the cDNA with either the F1-R7 or F4-R8 primers, two cDNA sequences (a short one with the primers F1-R7 and a long one with the primers F4-R8) were obtained producing two isoforms of SCEP2. f. The SCEP2 protein sequence with the two isoforms that differ in their 3′ sequence. The position of the N663933 insertion is highlighted in yellow in the coding sequence. The last 5 amino acids removed by the N525173 and N508352 insertions are highlighted in green.
Extended Data Fig. 2 Test of the specificity of the SCEP1 and SCEP2 antibodies.
a. Double immunolocalization ASY1 (Magenta) and SCEP1 (Green) in scep1-1 male meiocytes. b. Double immunolocalization ASY1 (Magenta) and SCEP2 (Green) in scep2-1 male meiocytes.
Extended Data Fig. 3 The distribution of COs along the five chromosomes.
The distribution of COs along chromosomes in female (A) and male (B) wild type, zyp1 and scep1-1. The centromere and pericentromeric regions are indicated by gray and blue shading, respectively. Analysis is done with 1-Mb windows and 50-kb sliding steps. For pericentromeric regions and each non-overlapping 1-Mb window along chromosome arms, two-sided Pearson′s Chi-squared test was used to examine the difference between wild type and scep1-1, zyp1 and scep1-1 in female and male populations separately. Windows with p-value (corrected with the FDR method) < 0.05 were marked by stars.
Extended Data Fig. 4 AlphaFold2 prediction of the complex formed by SCEP1 and SCEP2 orthologs in Selaginella moellendorffii, Amborella, Jatropha curcas, Solanum lycopersicum and Gossypium raimondii.
For each species, the top complex represents the SCEP1 homolog in pink and the SCEP2 homolog in blue. The bottom complex is colored by per-residue pLDDT. High pLDDT values indicate strong confidence in the predicted structure, and low values indicate low confidence. Predicted Aligned Error values of the SCEP1-SCEP2 dimer. Low PAE values indicate strong confidence in the relative position of the two amino acids, and high values indicate low confidence.
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Vrielynck, N., Peuch, M., Durand, S. et al. SCEP1 and SCEP2 are two new components of the synaptonemal complex central element. Nat. Plants 9, 2016–2030 (2023). https://doi.org/10.1038/s41477-023-01558-y
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DOI: https://doi.org/10.1038/s41477-023-01558-y