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Decoding the giant Y of Silene latifolia: Evolutionary insights into an unusually large sex chromosome

A high-quality genome assembly of Silene latifolia was generated by researchers at CNRS/Université Claude Bernard Lyon 1 and collaborating institutions. The team identified extensive recombination suppression, large-scale repeat accumulation, and gene loss on the Y chromosome, providing insights into the evolution of this unusually large sex chromosome.

Silene latifolia, also known as White Campion, is a dioecious plant with an XY sex-determination system. It has a Y chromosome of approximately 550 megabases (Mb), much larger than typical Y chromosomes in many species. The Y chromosome has remained unassembled due to its repeat-rich structure.

Previous genetic maps indicated extensive recombination suppression between X and Y, leading to a single pseudoautosomal region (PAR) and multiple evolutionary strata. The Y chromosome has undergone significant rearrangements and degeneration, but candidate sex-determining genes had not been fully identified.

In the study, "The Silene latifolia genome and its giant Y chromosome," in Science, Oxford Nanopore sequencing was used to assemble the S. latifolia genome, integrating long- and short-read data with a new genetic map.

To infer evolutionary history, the genomes of latifolia assembly were compared with those of related single-sexed Silene species (S. conica and S. vulgaris). Epigenetic analyses included DNA methylation and small RNA profiling. Mutants with Y chromosome deletions affecting sex phenotypes were sequenced to identify candidate sex-determining genes.

The assembled Y chromosome spans 485 Mb (excluding the PAR), while the X chromosome is 346 Mb. Based on X-Y divergence, three evolutionary strata were identified: S1 (~11.8 million years ago), S2 (~5.4 million years ago), and S3 (~4.4 million years ago).

Stratum S1 likely formed through inversions on both X and Y. Stratum S2 is the largest and includes the centromere, while S3 resulted from a more recent translocation of X to Y fragments. The Y chromosome has undergone extensive rearrangements and transposable element accumulation, making it highly degenerated compared with the X.

Gene loss on the Y chromosome was widespread, with 53% to 62% of ancestral genes absent. Remaining Y-linked genes exhibited reduced expression, likely due to epigenetic silencing via transposable element accumulation, small RNA interference, and increased DNA methylation.

Mutant analysis identified candidate genes in sex-determining regions. The Clavata3 (slCLV3-Y) gene was confirmed as a candidate for female sterility. The male fertility factor region contained slCyp704B1-Y and slTHI1-Y, both involved in pollen development.

Despite being noncoding, the Scarecrow-like 4/7 (slSCL4-Y) pseudogene was implicated in male function. The researchers suspect there is an RNA-based mechanism at work.

Recombination suppression in S. latifolia has led to a complex, repeat-rich Y chromosome with progressive degeneration. Findings suggest that the Y originated ~11 million years ago, with early inversions establishing sex determination, followed by later expansions of repeat accumulation. The research team provides new insights into the structural and functional evolution of the world's largest known plant sex chromosomes.