Sequencing papaya X and Yʰ chromosomes reveals molecular basis of incipient sex chromosome evolution
2012
Wang, Jianping | Na, Jong-Kuk | Yu, Qingyi | Gschwend, Andrea R. | Han, Jennifer | Zeng, Fanchang | Aryal, Rishi | VanBuren, Robert | Murray, Jan E. | Zhang, Wenli | Navajas-Pérez, Rafael | Feltus, F Alex | Lemke, Cornelia | Tong, Eric J. | Chen, Cuixia | Man Wai, Ching | Singh, Ratnesh | Wang, Mingli | Min, Xiang Jia | Alam, Maqsudul | Charlesworth, Deborah | Moore, Paul H. | Jiang, Jiming | Paterson, Andrew H. | Ming, Ray
Sex determination in papaya is controlled by a recently evolved XY chromosome pair, with two slightly different Y chromosomes controlling the development of males (Y) and hermaphrodites (Y ʰ). To study the events of early sex chromosome evolution, we sequenced the hermaphrodite-specific region of the Y ʰ chromosome (HSY) and its X counterpart, yielding an 8.1-megabase (Mb) HSY pseudomolecule, and a 3.5-Mb sequence for the corresponding X region. The HSY is larger than the X region, mostly due to retrotransposon insertions. The papaya HSY differs from the X region by two large-scale inversions, the first of which likely caused the recombination suppression between the X and Y ʰ chromosomes, followed by numerous additional chromosomal rearrangements. Altogether, including the X and/or HSY regions, 124 transcription units were annotated, including 50 functional pairs present in both the X and HSY. Ten HSY genes had functional homologs elsewhere in the papaya autosomal regions, suggesting movement of genes onto the HSY, whereas the X region had none. Sequence divergence between 70 transcripts shared by the X and HSY revealed two evolutionary strata in the X chromosome, corresponding to the two inversions on the HSY, the older of which evolved about 7.0 million years ago. Gene content differences between the HSY and X are greatest in the older stratum, whereas the gene content and order of the collinear regions are identical. Our findings support theoretical models of early sex chromosome evolution.
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