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

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.

Dosage compensation evolution in plants: theories, controversies and mechanisms

“…For instance, Carica papaya (Caricaceae) is a dioecious tree with XY homomorphic sex chromosomes that evolved approximately 7 Ma [92]. Evidence for DC was only found for a few non-recombining X/Y genes (7 out of 50) [93], and partial DC was found for some X-hemizygous genes (electronic supplementary material, table S2) [94].…”

Some thoughts about the words we use for thinking about sex chromosome evolution

“…If they do, the initial sterility factors should be within the oldest non-recombining region, or stratum, and other such factors might be found in younger strata, consistent with being associated with recombination suppression. In papaya, however, even though a young stratum has evolved, neither the sex chromosome as a whole, nor its fully Y-linked part, is enriched with genes whose expression in males is higher than in females [31]. However, this study found one Y-linked gene with lower expression in hermaphrodites than males, making it a good candidate for the active female-suppressing factor.…”

“…For example, in several fish, crossovers in male meiosis are strongly localized to the chromosome ends [16,28]; the centromere locations must then correspond to the non-crossover ends. Combined genetic and physical maps are still scarce for plants, but the small Y-linked region in Carica papaya is near the genetic centromere location of the metacentric chromosome 1 [29–31] (figure 3), though part stopped recombining more recently [32].

Figure 3Example of a completely sex-linked region close to a plant centromeric region with a low recombination rate.

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Identifying Genes Associated with Female Flower Development of Phellodendron amurense Rupr. Using a Transcriptomics Approach

“…Additionally, FMO3 , ATPD , WRKY21 , and exostosin are located in the sex-determined region of plants with unknown specific functions [ 148 , 176 , 214 ]. Their specific functions need further study.…”