Sex-Linked Gene Expression And The Emergence Of Hermaphrodites In Carica Papaya

Premise One evolutionary path from hermaphroditism to dioecy is via a gynodioecious intermediate. The evolution of dioecy may also coincide with the formation of sex chromosomes that possess sex-determining loci that are physically linked in a region of suppressed recombination. Dioecious papaya (Carica papaya) has an XY chromosome system, where the presence of a Y chromosome determines maleness. However, in cultivation, papaya is gynodioecious, due to the conversion of the male Y chromosome to a hermaphroditic Y-h chromosome during its domestication. Methods We investigated gene expression linked to the X, Y, and Y-h chromosomes at different floral developmental stages to identify differentially expressed genes that may be involved in the sexual transition of males to hermaphrodites. Results We identified 309 sex-biased genes found on the sex chromosomes, most of which are found in the pseudoautosomal regions. Female (XX) expression in the sex-determining region was almost double that of X-linked expression in males (XY) and hermaphrodites (XYh), which rules out dosage compensation for most sex-linked genes; although, an analysis of hemizygous X-linked loci found evidence of partial dosage compensation. Furthermore, we identified a candidate gene associated with sex determination and the transition to hermaphroditism, a homolog of the MADS-box protein SHORT VEGETATIVE PHASE. Conclusions We identified a pattern of partial dosage compensation for hemizygous genes located in the papaya sex-determining region. Furthermore, we propose that loss-of-expression of the Y-linked SHORT VEGETATIVE PHASE homolog facilitated the transition from males to hermaphrodites in papaya.