Dynamic rearrangements and gene trafficking in nascent Yh chromosome of papaya

Sex determination in papaya is controlled by a recently evolved XY chromosome pair, with two slightly different Y chromosomes, Y and Y^h, respectively controlling development of males and hermaphrodites. The sequencing of the hermaphrodite-specific region of the Y^h chromosome (HSY) and its X counterpart yielded an HSY pseudo-molecule of 8.1 megabases (Mb), and 3.5 Mb for the corresponding X region. The 131% expansion of the HSY is mostly due to retrotransposon insertions. The X region carries 81 genes, including 47 X/HSY gene pairs, and 34 genes present only in the X, which were apparently lost in the HSY. The HSY sequence includes 72 genes, of which 25 are HSY-specific. Ten HSY-specific genes were acquired from autosomes of which 3 were lost again, while the X region has acquired one. Sequence divergence between the alleles of retained X-HSY gene pairs reveals two evolutionary strata in the X chromosome, and the HSY differs from the X region by two large-scale inversions corresponding to the strata, causing recombination suppression. Numerous chromosomal rearrangements were detected within these inversions, and must have occurred later. The HSY’s expansion, rearrangements, and gene gains and losses, have occurred remarkably rapidly since this papaya chromosome region stopped recombining.