Subfunctionalization of CpSVP-Y Paralog Contributes to Male Reproductive Fitness in Papaya

Papayas possess three sex genotypes: female XX, male XY, and hermaphrodite XY^h. Only male plants produce long peduncles with numerous flowers, a trait that improves reproductive success. The gene SHORT VEGETATIVE PHASE (CpSVP) is located on the Y chromosome, absent from the X chromosome, and disrupted in the Y^h chromosome, making it a key candidate gene for long peduncles in male plants. An autosomal CpSVP allele (CpSVP-A) was also annotated in a papaya genome. The overexpression of the male allele in Arabidopsis increases pedicel length, which supports its role in pedicel elongation. Unexpectedly, the autosomal allele CpSVP-A produced a similar phenotype as the male one, while the hermaphroditic allele (CpSVP-Y^h) did not cause any significant change in pedicel length. Additionally, only the male allele rescued early flowering in an Atsvp mutant, indicating that it regulates both pedicel length and flowering time. In contrast, the autosomal allele only affected pedicel elongation and had no effect on flowering time. Together, these results demonstrate that CpSVP-Y underwent subfunctionalization, retaining both peduncle elongation and flowering time functions, while CpSVP-A likely lost the latter. Thus, CpSVP-Y contributes to male reproductive fitness through enhanced peduncle development without affecting sex determination, potentially regulated by Y chromosome-specific cis-elements. This study provides new insights into the genetic basis of sexually dimorphic traits in papayas.