Papaya sex chromosome evolution and domestication

Papaya is an economically important tropical fruit crop, and is a model species for studying early stages of sex chromosome evolution. Sex in papaya is genetically determined by three sex chromosomes, known as X, Y, and Y-h. These chromosomes contain sex-linked regions that were sequenced using a BAC-by-BAC approach, assembled in pseudomolecules, analyzed and compared in an effort to understand the events that led to the evolution of sex chromosomes in this species. The genomic sequences are substantially different between the X and Y chromosomes in their respective sex-specific regions. A major genomic feature is two inversions in the Y and Yh chromosomes that stopped recombination after their occurrence about 7 and 1.9 million years ago, respectively. DNA sequence expansion was detected in the male- and hermaphrodite-specific regions of the Y and Y-h chromosome (MSY and HSY) at 8.1 Mb compared with their X counterpart at 3.5 Mb. The X and Y chromosomes share 50 paired genes, whereas 22 genes are Y-specific and 34 genes are X-specific. MSY and HSY share 99.6% DNA sequence identity, and all gene content except one. Re-sequencing the genomes of papaya cultivars and wild accessions revealed that hermaphrodites were selected from a male population in northwest Costa Rica about 4000 years ago, coinciding with the rise of the Mayan civilization. Characterization of papaya sex chromosomes revealed early events of sex chromosome evolution and domestication of the Yh chromosome.