Evolution of a Flexible Sex Determination System in Polyploid Persimmon

Epigenetic regulation adds a flexible layer to genetic variation, potentially enabling long term, but reversible cis-regulatory changes of an allele while maintaining DNA sequence. Here we present evidence for the establishment of an epigenetic switch regulating sex determination in persimmon. Specifically, we are documenting the role of DNA methylation in sex-determination in Oriental persimmon (Diospyros kaki). This regulation leads to the formation of both male and female flowers (monoeocy), in genetically male individuals. In these Y-chromosome carrying hexaploid persimmon trees, the gene encoding the female-determining factor MeGI exhibits 5' methylation and repression in buds that form male flowers but not in developing female flowers or any other tissue. Treatment with a demethylating agent could result in the reversion of male developing buds to form semi-feminized flowers, while it did not affect female flowers. This epigenetic control of flower development in hexaploid persimmon differs from the genetic determination observed in the closely related diploid persimmon. There, male flower development is based on the repression of MeGI by the Y-encoded male-determining factor OGI. In hexaploid persimmon, OGI expression is undetectable, possibly due to the insertion of a transposon in the 5' region of its promoter. This transposon insertion is conserved in all Y-carrying D. kaki cultivars, suggesting either natural selection or a strong bottleneck for the silenced OGI gene during the establishment of this species. Adaptive scenarios involving the relationship between this epigenetic plasticity and polyploid evolution will be discussed.