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

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 nonrecombining 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 behavior dynamics of plant sex chromosomes remain largely unexplored. In this study, we employed super-resolution microscopy to analyze 3D chromosome organization and the localization of key meiotic proteins. Namely, we studied the dynamics of Asynaptic1 (ASY1), Zip1 homolog (ZYP1), and HEI10 across the leptotene to pachytene stages, and compared sex chromosome behavior in dioecious white campion (Silene latifolia) with related gynodioecious species bladder campion (Silene vulgaris). Our findings show that both species exhibit 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 behavior 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 nonrecombining region and provide the most detailed cytogenetic analysis of sex chromosome pairing in a plant with evolutionarily young sex chromosomes.