Sequencing papaya X and Y h chromosomes reveals molecular basis of incipient sex chromosome evolution

Jianping Wang, Jong Kuk Na, Qingyi Yu, Andrea R. Gschwend, Jennifer Han, Fanchang Zeng, Rishi Aryal, Robert VanBuren, Jan E. Murray, Wenli Zhang, Rafael Navajas-Pérez, F. Alex Feltus, Cornelia Lemke, Eric J. Tong, Cuixia Chen, Ching Man Wai, Ratnesh Singh, Ming Li Wang, Xiang Jia Min, Maqsudul AlamDeborah Charlesworth, Paul H. Moore, Jiming Jiang, Andrew H. Paterson, Ray Ming*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

151 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)13710-13715
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number34
DOIs
StatePublished - Aug 21 2012

Keywords

  • Carica papaya
  • DNA sequencing
  • Molecular evolution
  • Sex chromosomes

ASJC Scopus subject areas

  • General

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