Sex-linked gene expression and the emergence of hermaphrodites in Carica papaya

Am J Bot. 2021 Jun;108(6):1029-1041. doi: 10.1002/ajb2.1689. Epub 2021 Jun 22.

Abstract

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 Yh chromosome during its domestication.

Methods: We investigated gene expression linked to the X, Y, and Yh 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.

Keywords: Caricaceae; Dioecy; dosage compensation; plant sex chromosomes; sex determination.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Carica* / genetics
  • Chromosomes, Plant / genetics
  • Disorders of Sex Development*
  • Gene Expression
  • Sex Chromosomes / genetics