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Research Article

Rapid divergence and expansion of the X chromosome in papaya

Andrea R. Gschwend, Qingyi Yu, Eric J. Tong, Fanchang Zeng, Jennifer Han, Robert VanBuren, Rishi Aryal, Deborah Charlesworth, Paul H. Moore, Andrew H. Paterson, and Ray Ming
  1. aDepartment of Plant Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
  2. bTexas AgriLife Research Center, Department of Plant Pathology and Microbiology, Texas A & M University, Weslaco, TX 78596;
  3. cHawaii Agriculture Research Center, Kunia, HI 96759;
  4. dInstitute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom; and
  5. ePlant Genome Mapping Laboratory, University of Georgia, Athens, GA 30606

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PNAS August 21, 2012 109 (34) 13716-13721; https://doi.org/10.1073/pnas.1121096109
Andrea R. Gschwend
aDepartment of Plant Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Qingyi Yu
bTexas AgriLife Research Center, Department of Plant Pathology and Microbiology, Texas A & M University, Weslaco, TX 78596;
cHawaii Agriculture Research Center, Kunia, HI 96759;
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  • For correspondence: QYu@ag.tamu.edu rming@life.illinois.edu
Eric J. Tong
cHawaii Agriculture Research Center, Kunia, HI 96759;
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Fanchang Zeng
aDepartment of Plant Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Jennifer Han
aDepartment of Plant Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Robert VanBuren
aDepartment of Plant Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Rishi Aryal
aDepartment of Plant Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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Deborah Charlesworth
dInstitute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom; and
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Paul H. Moore
cHawaii Agriculture Research Center, Kunia, HI 96759;
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Andrew H. Paterson
ePlant Genome Mapping Laboratory, University of Georgia, Athens, GA 30606
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Ray Ming
aDepartment of Plant Biology, University of Illinois at Urbana–Champaign, Urbana, IL 61801;
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  • For correspondence: QYu@ag.tamu.edu rming@life.illinois.edu
  1. Edited by Ralf G. Kynast, Royal Botanic Gardens, Kew, Richmond, United Kingdom, and accepted by the Editorial Board April 16, 2012 (received for review December 22, 2011)

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Abstract

X chromosomes have long been thought to conserve the structure and gene content of the ancestral autosome from which the sex chromosomes evolved. We compared the recently evolved papaya sex chromosomes with a homologous autosome of a close relative, the monoecious Vasconcellea monoica, to infer changes since recombination stopped between the papaya sex chromosomes. We sequenced 12 V. monoica bacterial artificial chromosomes, 11 corresponding to the papaya X-specific region, and 1 to a papaya autosomal region. The combined V. monoica X-orthologous sequences are much shorter (1.10 Mb) than the corresponding papaya region (2.56 Mb). Given that the V. monoica genome is 41% larger than that of papaya, this finding suggests considerable expansion of the papaya X; expansion is supported by a higher repetitive sequence content of the X compared with the papaya autosomal sequence. The alignable regions include 27 transcript-encoding sequences, only 6 of which are functional X/V. monoica gene pairs. Sequence divergence from the V. monoica orthologs is almost identical for papaya X and Y alleles; the Carica-Vasconcellea split therefore occurred before the papaya sex chromosomes stopped recombining, making V. monoica a suitable outgroup for inferring changes in papaya sex chromosomes. The papaya X and the hermaphrodite-specific region of the Yh chromosome and V. monoica have all gained and lost genes, including a surprising amount of changes in the X.

  • Carica papaya
  • gene gains and losses
  • sex chromosome evolution
  • suppression of recombination
  • centromere of X chromosome

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: QYu{at}ag.tamu.edu or rming{at}life.illinois.edu.
  • Author contributions: A.R.G., Q.Y., P.H.M., A.H.P., and R.M. designed research; A.R.G., Q.Y., E.J.T., F.Z., J.H., R.V., and R.A. performed research; A.R.G., Q.Y., F.Z., J.H., R.V., R.A., D.C., and R.M. analyzed data; and A.R.G., D.C., and R.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. R.G.K. is a guest editor invited by the Editorial Board.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession numbers are listed in SI Appendix, Table S11.)

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1121096109/-/DCSupplemental.

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Divergence and expansion of papaya X chromosome
Andrea R. Gschwend, Qingyi Yu, Eric J. Tong, Fanchang Zeng, Jennifer Han, Robert VanBuren, Rishi Aryal, Deborah Charlesworth, Paul H. Moore, Andrew H. Paterson, Ray Ming
Proceedings of the National Academy of Sciences Aug 2012, 109 (34) 13716-13721; DOI: 10.1073/pnas.1121096109

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Divergence and expansion of papaya X chromosome
Andrea R. Gschwend, Qingyi Yu, Eric J. Tong, Fanchang Zeng, Jennifer Han, Robert VanBuren, Rishi Aryal, Deborah Charlesworth, Paul H. Moore, Andrew H. Paterson, Ray Ming
Proceedings of the National Academy of Sciences Aug 2012, 109 (34) 13716-13721; DOI: 10.1073/pnas.1121096109
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