Recent Origin of Dioecious and Gynodioecious Y Chromosomes in Papaya

Sex of dioecious and gynodioecious papayas is controlled by two slightly different Y chromosomes, Y for males and Y^h for hermaphrodites. All combinations of the Y and/or Y^h chromosomes are lethal. We investigated the features of paired dioecious X- and Y-specific bacterial artificial chromosomes (BACs) and compared their sequences to corresponding gynodioecious X- and Y-specific BACs. Numerous chromosomal rearrangements were detected between the X- and Y-specific BACs, including inversions, deletions, insertions, and duplications. DNA sequence expansion was documented on the Y BAC. Dioecious and gynodioecious X-specific BACs were virtually identical. The Y- and Y^h-specific BACs shared high degree of DNA sequence identity, but local chromosomal rearrangements were detected, as the consequence of suppression of recombination in the male specific region and the isolation of Y and Y^h chromosomes enforced by the lethal effect. Analysis of sequence divergence between three dioecious X and Y gene pairs resulted in the estimated ages of divergence from 0.6 to 2.5 million years, reinforcing the hypothesis of a recent origin of the papaya sex chromosomes. The estimated age of divergence between Y and Y^h chromosomes was approximately 73,000 years for Gene 5. Our findings indicate that Y and Y^h chromosomes evolved from a common ancestral Y chromosome, possibly prior to the origin of agriculture. The existence of a hermaphrodite Y^h chromosome is less likely to have resulted from human selection as once suggested.