Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A primitive Y chromosome in papaya marks incipient sex chromosome evolution


Many diverse systems for sex determination have evolved in plants and animals1,2,3. One involves physically distinct (heteromorphic) sex chromosomes (X and Y, or Z and W) that are homozygous in one sex (usually female) and heterozygous in the other (usually male). Sex chromosome evolution is thought to involve suppression of recombination around the sex determination genes, rendering permanently heterozygous a chromosomal region that may then accumulate deleterious recessive mutations by Muller's ratchet, and fix deleterious mutations by hitchhiking as nearby favourable mutations are selected on the Y chromosome4,5. Over time, these processes may cause the Y chromosome to degenerate and to diverge from the X chromosome over much of its length; for example, only 5% of the human Y chromosome still shows X–Y recombination6. Here we show that papaya contains a primitive Y chromosome, with a male-specific region that accounts for only about 10% of the chromosome but has undergone severe recombination suppression and DNA sequence degeneration. This finding provides direct evidence for the origin of sex chromosomes from autosomes.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Figure 1: AFLP map of papaya LG 1 and physical maps of BAC contigs in the MSY region.
Figure 2: Characterization of duplicated markers cpsm31 and cpsm90 in the MSY region.
Figure 3: Comparative organization of Y chromosomes in papaya (estimated as 41 Mb), S. latifolia (estimated as 570 Mb) and human (66 Mb).


  1. Westergaard, M. The mechanism of sex determination in flowering plants. Adv. Genet. 9, 217–281 (1958)

    Article  CAS  PubMed  Google Scholar 

  2. White, M. J. D. in Insect Reproduction (eds Leather, S. R. & Hardie, J.) 57–94 (Cambridge Univ. Press, Cambridge, 1973)

    Google Scholar 

  3. Ohno, S. Sex Chromosome and Sex-linked Genes (Springer, Berlin, 1967)

    Book  Google Scholar 

  4. Muller, M. The relation of recombination to mutational advance. Mutat. Res. 1, 2–9 (1964)

    Article  Google Scholar 

  5. Rice, W. R. Genetic hitch-hiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116, 161–167 (1987)

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Skaletsky, H. et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Hofmeyr, J. D. J. Genetical studies of Carica papaya L. S. Afr. Dept Agric. Sci. Bull. 187, 64 (1938)

    Google Scholar 

  8. Storey, W. B. Segregation of sex types in Solo papaya and their application to the selection of seed. Am. Soc. Horticult. Sci. Proc. 35, 83–85 (1938)

    Google Scholar 

  9. Hofmeyr, J. D. J. Some genetic and breeding aspects of Carica papaya. Agronomia Tropical 17, 345–351 (1967)

    Google Scholar 

  10. Storey, W. B. in The Evolution of Crop Plants (ed. Simmonds, N. W.) 21–24 (Longman, London, 1976)

    Google Scholar 

  11. Horovitz, S. & Jiminez, H. Cruzamientos interespecificos e intergenericos en Caricaceaes y sus implicationes fitotecnias. Agronomia Tropical 17, 353–359 (1967)

    Google Scholar 

  12. Sondur, S. N., Manshardt, R. M. & Stiles, J. I. A genetic linkage map of papaya based on randomly amplified polymorphic DNA markers. Theor. Appl. Genet. 93, 547–553 (1996)

    Article  CAS  PubMed  Google Scholar 

  13. Ma, H. et al. High-density linkage mapping revealed suppression of recombination at the sex determination locus in papaya. Genetics (in the press)

  14. Deputy, J. C. et al. Molecular marker for sex determination in papaya (Carica papaya L.). Theor. Appl. Genet. 106, 107–111 (2002)

    Article  CAS  PubMed  Google Scholar 

  15. Ming, R. et al. Construction and characterization of a papaya BAC library as a foundation for molecular dissection of a tree-fruit genome. Theor. Appl. Genet. 102, 892–899 (2001)

    Article  CAS  Google Scholar 

  16. Storey, W. B. The botany and sex relations of the papaya. Hawaii Agricult. Exp. Station Bull 87, 5–22 (1941)

    Google Scholar 

  17. Tanksley, S. D., Miller, J. C., Paterson, A. H. & Bernatzky, R. Proc. 18th Stadler Genet. Symp. 157–173 (Plenum, New York, 1988)

    Google Scholar 

  18. Charlesworth, B. The evolution of sex chromosomes. Science 251, 1030–1033 (1991)

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Lahn, B. T. & Page, D. C. Four evolutionary strata on the human X chromosome. Science 286, 964–967 (1999)

    Article  CAS  PubMed  Google Scholar 

  20. Iwase, M. et al. The amelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species. Proc. Natl Acad. Sci. USA 100, 5258–5263 (2003)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  21. Charlesworth, D. Plant sex determination and sex chromosomes. Heredity 88, 94–101 (2002)

    Article  PubMed  Google Scholar 

  22. Filatov, D. A., Moneger, F., Negrutiu, I. & Charlesworth, D. Low variability in a Y-linked plant gene and its implications for Y-chromosome evolution. Nature 404, 388–390 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Chiu, C. T. Study on Sex Inheritance and Horticultural Characteristics of Hermaphrodite Papaya Thesis, Nat. Pingtung Univ. Sci. Technol., Taiwan (2000)

    Google Scholar 

  24. Storey, W. B. Genetics of the papaya. J. Hered. 44, 70–78 (1953)

    Article  Google Scholar 

  25. Okada, S. et al. The Y chromosome in the liverwort Marchantia polymorpha has accumulated unique repeat sequences harboring a male-specific gene. Proc. Natl Acad. Sci. USA 98, 9454–9459 (2001)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Bachtrog, D. Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes in Drosophila. Nature Genet. 34, 215–219 (2003)

    Article  CAS  PubMed  Google Scholar 

  27. Charlesworth, B. & Charlesworth, D. A model for the evolution of dioecy and gynodioecy. Am. Nat. 112, 975–997 (1978)

    Article  Google Scholar 

  28. Yang, Z. N. & Mirkov, T. E. Isolation of large terminal sequences of BAC inserts based on double restriction enzyme digestion followed by anchored PCR. Genome 43, 412–415 (2000)

    Article  CAS  PubMed  Google Scholar 

  29. Siroky, J., Lysak, M. A., Dolezel, J., Kejnovsky, E. & Vyskot, B. Heterogeneity of rDNA distribution and genome size in Silene spp. Chromosome Res. 9, 387–393 (2001)

    Article  CAS  PubMed  Google Scholar 

  30. Lengerova, M., Moore, R. C., Grant, S. R. & Vyskot, B. The sex chromosomes of Silene latifolia revisited and revised. Genetics 165, 935–938 (2003)

    PubMed  PubMed Central  Google Scholar 

Download references


We thank D. Charlesworth for comments on the manuscript; R. Perl-Treves for discussions; S. Ancheta, G. Asmus and L. Poland for technical assistance; R. Manshardt for providing an F2 population for fine-mapping; and H. Albert, M. Moore, R. Osgood, B. Vyskot and S. Whalen for reviewing the manuscript. This work was supported by a United States Department of Agriculture Agricultural Research Service (USDA-ARS) Cooperative Agreement with the Hawaii Agriculture Research Center, and a subaward to R. M. and A.H.P. to produce and to characterize the BAC library.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Ray Ming.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1: PCR amplification of cpsm10 among four papaya cultivars and three sex types. (DOC 33 kb)


Supplementary Figure 2: PCR amplification of duplicated cpsm90 and cpsm31 on BACs mapped to the tandem duplication region in the papaya MSY. (DOC 39 kb)


Supplementary Figure 3: Precocious separation of one pair of papaya chromosomes at anaphase I in pollen mother cells. (DOC 683 kb)


Supplementary Table: Comparison of male-specific DNA sequences amplified from papaya hermaphrodite and male genomic DNA. (DOC 24 kb)

Supplementary Notes (DOC 23 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Z., Moore, P., Ma, H. et al. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427, 348–352 (2004).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing