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PreprintCited by 0Chromosomal and Genetic VariationsGenetic and Clinical Aspects of Sex Determination and Chromosomal AbnormalitiesPlant Reproductive Biology

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Sex chromosome pairing and multivalent associations during meiosis in diploid and polyploid Silene latifolia

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Bačovský, Václav, Novotná, Pavla, Phillips, Dylan, Horáková, Lucie, Kružlicová, Jana, Čížková, Jana, Janoušek, Bohuslav, Čegan, Radim·2025·PLANT PHYSIOLOGY
DOI 10.1101/2025.08.08.669263PMC PMC13017482

Preprint — published as 10.1093/plphys/kiaf599 · Paper page

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Abstract

Sex chromosomes undergo various modifications that affect their synapsis during meiosis. While most of the genome achieves full synapsis by the end of pachytene, the non-recombining regions of XY (or ZW) chromosomes often remain asynaptic, and fail to form physical associations at metaphase I. Despite significant progress in animal models, the meiotic behaviour dynamics of plant sex chromosomes remain largely unexplored. In this study, we employed super-resolution microscopy to analyse 3D chromosome organization and the localization of key meiotic proteins. Namely, we studied the dynamics of ASY1, ZYP1, and HEI10, across the leptotene to pachytene stages, and compared sex chromosome behaviour in dioecious Silene latifolia with related gynodioecious S. vulgaris . Our findings show that both exhibits a class I crossover (CO) frequency comparable to mammals, indicating moderate COs per bivalent and their similar genetic determinants. We document variation in sex chromosome configurations, from rod bivalents in diploids to open-ring tetravalents in autopolyploids, and characterize Y chromosome behaviour across XXY, XXXY, and XXYY karyotypes. These results reveal pronounced variation in pairing and synaptic patterns, even within a shared genetic background. We discuss how these patterns reflect the evolutionary trajectory of the non-recombining region and provide the most detailed cytogenetic analysis of sex chromosome pairing in a plant with evolutionary young sex chromosomes.

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Figure 1. Meiotic segregation and sex chromosome pairing during male metaphase I in Silene. In S. vulgaris, 3 autosomes differentiated by XY-PAR positioning, form 2 ring bivalents and rod bivalent configurations at the metaphase I plate. The 3 regions are orthologous to XY chromosomes (dashed line). In contrast, in S. latifolia, the X and Y chromosomes consistently form a rod bivalent at the metaphase I plate. In cases of multiple sex chromosomes (2n = 3x = 36, XXY; 2n = 4x = 48, XXXY/XXYY), the sex chromosomes form from left to right (the upper line): type A—a single rod bivalent and physically separated univalent (X-Y and X), type B—a Y-shaped trivalent (X-X-Y), type C—a chain-like (Y-X-X-X), and type D—an open-ring tetravalent with 3 Xs and a single Y. From left to right (bottom line): type E—an open-ring tetravalent, type F—a single bivalent (X-X) and rod bivalent structure (Y-Y), type G—a chain-like tetravalent (Y-X-X-Y), type H—an open-ring tetravalent in which 2 X chromosomes are connected through the q-arm (Y-Y-X-X), or type I—all 4 sex chromosomes connected via the PAR (YY-X-X). Type J consists of a chain tetravalent structure with a loosely associated Y chromosome (Y-X-X/Y). The formation of all displayed configurations was consistently observed in individual analyzed cells (at least 20 per slide) across 8 replicates. Sex chromosomes in S. latifolia and polyploid individuals were identified using a combination of subtelomeric (X43.1; green) and centromeric tandem repeat (STAR-C; magenta) markers. Arrows indicate PAR. Chromosomes were counterstained with DAPI (gray). Scale bar = 10 µm is applicable to all the images.
Figure 1. Meiotic segregation and sex chromosome pairing during male metaphase I in Silene. In S. vulgaris, 3 autosomes differentiated by XY-PAR positioning, form 2 ring bivalents and rod bivalent configurations at the metaphase I plate. The 3 regions are orthologous to XY chromosomes (dashed line). In contrast, in S. latifolia, the X and Y chromosomes consistently form a rod bivalent at the metaphase I plate. In cases of multiple sex chromosomes (2n = 3x = 36, XXY; 2n = 4x = 48, XXXY/XXYY), the sex chromosomes form from left to right (the upper line): type A—a single rod bivalent and physically separated univalent (X-Y and X), type B—a Y-shaped trivalent (X-X-Y), type C—a chain-like (Y-X-X-X), and type D—an open-ring tetravalent with 3 Xs and a single Y. From left to right (bottom line): type E—an open-ring tetravalent, type F—a single bivalent (X-X) and rod bivalent structure (Y-Y), type G—a chain-like tetravalent (Y-X-X-Y), type H—an open-ring tetravalent in which 2 X chromosomes are connected through the q-arm (Y-Y-X-X), or type I—all 4 sex chromosomes connected via the PAR (YY-X-X). Type J consists of a chain tetravalent structure with a loosely associated Y chromosome (Y-X-X/Y). The formation of all displayed configurations was consistently observed in individual analyzed cells (at least 20 per slide) across 8 replicates. Sex chromosomes in S. latifolia and polyploid individuals were identified using a combination of subtelomeric (X43.1; green) and centromeric tandem repeat (STAR-C; magenta) markers. Arrows indicate PAR. Chromosomes were counterstained with DAPI (gray). Scale bar = 10 µm is applicable to all the images.CC BY · PubMed Central
Figure 2. Formation of SCs and immunolocalization of meiotic proteins ASY1, ZYP1, and HEI10. A to F) The progression of prophase I in S. vulgaris (A, C, E) and S. latifolia (B, D, F) is visualized through the dynamic localization of ZYP1 along the axial elements. A, B) During leptotene ASY1 (cyan) labels the axial elements, and central elements (ZYP1, magenta) become increasingly distinct. HEI10 forms numerous small foci along the chromosomes. C, D) In zygotene, the ASY1 signal becomes fragmented as synapsis progresses, marked by the extension of ZYP1 along the central element, facilitating SC assembly. HEI10 foci subsequently coalesce into large foci. E, F) By pachytene, ASY1 (axial elements) was restricted to asynaptic regions of the nucleus, while fully assembled SCs were observed between homologous chromosome pairs. These are 3 autosome bivalents in S. vulgaris, and PAR in S. latifolia. HEI10 foci become fewer and larger, indicating a process of coarsening, marking future CO events. The behavior of ZYP1, ASY1, and HEI10 was consistent across all analyzed cells (n = 74; Supplementary Table S3). Scale bar = 4 µm is applicable to all the images.
Figure 2. Formation of SCs and immunolocalization of meiotic proteins ASY1, ZYP1, and HEI10. A to F) The progression of prophase I in S. vulgaris (A, C, E) and S. latifolia (B, D, F) is visualized through the dynamic localization of ZYP1 along the axial elements. A, B) During leptotene ASY1 (cyan) labels the axial elements, and central elements (ZYP1, magenta) become increasingly distinct. HEI10 forms numerous small foci along the chromosomes. C, D) In zygotene, the ASY1 signal becomes fragmented as synapsis progresses, marked by the extension of ZYP1 along the central element, facilitating SC assembly. HEI10 foci subsequently coalesce into large foci. E, F) By pachytene, ASY1 (axial elements) was restricted to asynaptic regions of the nucleus, while fully assembled SCs were observed between homologous chromosome pairs. These are 3 autosome bivalents in S. vulgaris, and PAR in S. latifolia. HEI10 foci become fewer and larger, indicating a process of coarsening, marking future CO events. The behavior of ZYP1, ASY1, and HEI10 was consistent across all analyzed cells (n = 74; Supplementary Table S3). Scale bar = 4 µm is applicable to all the images.CC BY · PubMed Central
Figure 3. 3D analysis of meiotic pairing in pachytene chromosomes of S. vulgaris and S. latifolia. A) In S. vulgaris, 3 orthologous chromosome pairs, depicted by ZYP1 (magenta) axis (A1 to A3), link to 3 asynaptic regions (cyan) designated as A1asy, A2asy, and A3asy. B) In S. latifolia, a single large asynaptic region of 2 axes (X–Yasy) corresponds to the X and Y chromosomes. PAR is visualized by ZYP1 immunolocalization. White boxes in (A, B) represent the boundary of asynaptic region in both species. C, D, E) The insets (yellow boxes) of asynaptic regions in S. vulgaris (A), the boundaries between synapsed and asynaptic regions are sharply defined, as revealed in maximum intensity projections, marked by arrows. F) The inset (yellow box) of asynaptic region in S. latifolia (B), the asynaptic region displays a clear boundary at the PAB, extending into 2 protruding ASY1-marked axes representing the unsynapsed portions of the X and Y chromosomes. The whole 3D reconstruction and optical sectioning of pachytene chromosomes for both species are shown in Supplementary Videos S1 and S2. Scale bars in main panels (A, B) = 3 µm. Scale bar in insets (C to F) = 0.5 µm.
Figure 3. 3D analysis of meiotic pairing in pachytene chromosomes of S. vulgaris and S. latifolia. A) In S. vulgaris, 3 orthologous chromosome pairs, depicted by ZYP1 (magenta) axis (A1 to A3), link to 3 asynaptic regions (cyan) designated as A1asy, A2asy, and A3asy. B) In S. latifolia, a single large asynaptic region of 2 axes (X–Yasy) corresponds to the X and Y chromosomes. PAR is visualized by ZYP1 immunolocalization. White boxes in (A, B) represent the boundary of asynaptic region in both species. C, D, E) The insets (yellow boxes) of asynaptic regions in S. vulgaris (A), the boundaries between synapsed and asynaptic regions are sharply defined, as revealed in maximum intensity projections, marked by arrows. F) The inset (yellow box) of asynaptic region in S. latifolia (B), the asynaptic region displays a clear boundary at the PAB, extending into 2 protruding ASY1-marked axes representing the unsynapsed portions of the X and Y chromosomes. The whole 3D reconstruction and optical sectioning of pachytene chromosomes for both species are shown in Supplementary Videos S1 and S2. Scale bars in main panels (A, B) = 3 µm. Scale bar in insets (C to F) = 0.5 µm.CC BY · PubMed Central
Figure 4. Synaptonemal complex formation in male triploid and autotetraploid S. latifolia individuals. During pachytene, in triploid and autotetraploid plants with XXY, XXYY, and XXXY sex chromosome constitutions, ASY1 (cyan) is confined to asynaptic regions of the nucleus, while fully assembled SCs are present between homologous chromosome pairs (ZYP1; magenta). HEI10 (yellow) foci are observed exclusively on fully assembled SCs. Scale bar = 4 µm is applicable to all the images.
Figure 4. Synaptonemal complex formation in male triploid and autotetraploid S. latifolia individuals. During pachytene, in triploid and autotetraploid plants with XXY, XXYY, and XXXY sex chromosome constitutions, ASY1 (cyan) is confined to asynaptic regions of the nucleus, while fully assembled SCs are present between homologous chromosome pairs (ZYP1; magenta). HEI10 (yellow) foci are observed exclusively on fully assembled SCs. Scale bar = 4 µm is applicable to all the images.CC BY · PubMed Central
Figure 5. Dynamics of ASY1 and ZYP1 loading during meiotic pairing in prophase I. A) Quantification of ASY1 (cyan) and ZYP1 (magenta) signal volumes during leptotene (LEP), zygotene (ZYG), and pachytene (PACH) in S. vulgaris, S. latifolia, and polyploid individuals. A progressive increase in ZYP1 signal corresponds with a reduction in ASY1 as synapsis proceeds. Despite differences in ploidy and sex chromosome constitution, the overall ASY1-to-ZYP1 transition pattern is conserved. Each dot corresponds to an individual cell. Error bars represent standard deviation (SD). B) Schematic representation of ASY1 and ZYP1 loading during leptotene-to-pachytene progression in prophase I. In S. vulgaris, 3 autosomal pairs (Aasy) display asynaptic behavior while the rest of the autosomes are fully synapsed (A). In S. latifolia, as well as in XXY, XXXY, and XXYY individuals, the nonhomologous regions of the X and Y chromosomes (X–Yasy) are asynaptic, marked by strong ASY1 adjacent to short ZYP1-positive PAR segments. The autosomes are synapsed (A).
Figure 5. Dynamics of ASY1 and ZYP1 loading during meiotic pairing in prophase I. A) Quantification of ASY1 (cyan) and ZYP1 (magenta) signal volumes during leptotene (LEP), zygotene (ZYG), and pachytene (PACH) in S. vulgaris, S. latifolia, and polyploid individuals. A progressive increase in ZYP1 signal corresponds with a reduction in ASY1 as synapsis proceeds. Despite differences in ploidy and sex chromosome constitution, the overall ASY1-to-ZYP1 transition pattern is conserved. Each dot corresponds to an individual cell. Error bars represent standard deviation (SD). B) Schematic representation of ASY1 and ZYP1 loading during leptotene-to-pachytene progression in prophase I. In S. vulgaris, 3 autosomal pairs (Aasy) display asynaptic behavior while the rest of the autosomes are fully synapsed (A). In S. latifolia, as well as in XXY, XXXY, and XXYY individuals, the nonhomologous regions of the X and Y chromosomes (X–Yasy) are asynaptic, marked by strong ASY1 adjacent to short ZYP1-positive PAR segments. The autosomes are synapsed (A).CC BY · PubMed Central

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Metadata

Authors
Bačovský, V., Novotná, P., Phillips, D., Horáková, L., Kružlicová, J., Čížková, J., Janoušek, B., & Čegan, R.
Affiliations
  • Czech Academy of Sciences, Institute of Biophysics (CZ)
  • Masaryk University (CZ)
  • Aberystwyth University (GB)
  • Czech Academy of Sciences, Institute of Experimental Botany (CZ)
Corresponding author
  • Bačovský, Václav
  • Čegan, Radim
ORCID
Venue
PLANT PHYSIOLOGY
Publisher
openRxiv
Published
2025-08-11
Volume
200
Issue
3
ISSN
0032-0889 (ISSN-L)
DOI
10.1101/2025.08.08.669263
PMC
PMC13017482
OpenAlex
W4416438670
Cited by
0
References
1
FWCI
0.00
Type
journal article
Language
en
Open access
Licence
Locations
  • PLANT PHYSIOLOGY (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Veřejné služby Informačního systému (Masarykiana Brunensis Universitas) (submittedVersion, cc-by)
Funders
Ministry of Education Youth and Sports
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Reproductive Biology
Keywords
sex chromosome pairing, meiotic synapsis, non-recombining region, Silene latifolia, Silene vulgaris, autopolyploidy, crossover frequency, HEI10, karyotype variation, gynodioecy, dioecy
MeSH terms
Diploidy, Meiosis, Plant Proteins, Polyploidy, Sex Chromosomes, Chromosome Pairing, Silene, Chromosomes, Plant

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Bačovský, V., Novotná, P., Phillips, D., Horáková, L., Kružlicová, J., Čížková, J., Janoušek, B., & Čegan, R. (2025). Sex chromosome pairing and multivalent associations during meiosis in diploid and polyploid Silene latifolia. PLANT PHYSIOLOGY. https://doi.org/10.1101/2025.08.08.669263

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