Recent Origin of Dioecious and Gynodioecious Y Chromosomes in Papaya
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Sex of dioecious and gynodioecious papayas is controlled by two slightly different Y chromosomes, Y for males and Yh for hermaphrodites. All combinations of the Y and/or Yh 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 Yh-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 Yh 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 Yh chromosomes was approximately 73,000 years for Gene 5. Our findings indicate that Y and Yh chromosomes evolved from a common ancestral Y chromosome, possibly prior to the origin of agriculture. The existence of a hermaphrodite Yh chromosome is less likely to have resulted from human selection as once suggested.
KeywordsCarica papaya Chromosomal rearrangements Molecular evolution MSY male specific region of the Y chromosome Sex chromosomes
We thank Chris Saski for constructing the papaya male BAC library. This work was supported by a grant from NSF to R.M., Q.Y., P.H.M., J.J., and A.H.P. (DBI-0553417) and a USDA-ARS Cooperative Agreement (CA 58-3020-8-134) with the Hawaii Agriculture Research Center.
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