Morphological, genic and epigenetic differences often exist in separate sexes of dioecious and trioecious plants. However, the connections and relationships among them in different breeding systems are still unclear. Papaya has three sex types, which is genetically determined and epigenetically regulated, and was chosen as a model to study sex differentiation. Bisulfite sequencing of genomic DNA extracted from early-stage flowers revealed sex-specific genomic methylation landscapes and seasonally methylome reprogramming processes in dioecious and gynodioecious papaya grown in spring and summer. Extensive methylation of sex-determining region (SDR) was the distinguishing epigenetic characteristics of nascent XY sex chromosomes in papaya. Seasonal methylome reprogramming of early-stage flowers in both dioecy and gynodioecy systems were detected, resulting from transcriptional expression pattern alterations of methylation-modification-related and chromatin-remodeling-related genes, particularly from those genes involved in active demethylation. Genes involved in phytohormone signal transduction pathway in male flowers have played an important role in the formation of male-specific characteristics. These findings enhanced the understanding of the genetic and epigenetic contributions to sex differentiation and the complexity of sex chromosome evolution in trioecious plants.

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