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A primitive Y chromosome in papaya marks incipient sex chromosome evolution

Naturevolume 427, pages348–352 (2004)Cite this article

Abstract

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.

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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).

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References

  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. inInsect 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.Genetics116, 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.Nature423, 825–837 (2003)

    Article ADS CAS PubMed  Google Scholar 

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

    Google Scholar 

  8. Storey, W. B. Segregation of sex types inSolo 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 ofCarica papaya.Agronomia Tropical17, 345–351 (1967)

    Google Scholar 

  10. Storey, W. B. inThe 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 Tropical17, 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 Bull87, 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.Science251, 1030–1033 (1991)

    Article ADS CAS PubMed  Google Scholar 

  19. Lahn, B. T. & Page, D. C. Four evolutionary strata on the human X chromosome.Science286, 964–967 (1999)

    Article CAS PubMed  Google Scholar 

  20. Iwase, M. et al. Theamelogenin loci span an ancient pseudoautosomal boundary in diverse mammalian species.Proc. Natl Acad. Sci. USA100, 5258–5263 (2003)

    Article ADS CAS PubMed PubMed Central  Google Scholar 

  21. Charlesworth, D. Plant sex determination and sex chromosomes.Heredity88, 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.Nature404, 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 liverwortMarchantia polymorpha has accumulated unique repeat sequences harboring a male-specific gene.Proc. Natl Acad. Sci. USA98, 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 inDrosophila.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.Genome43, 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 inSilene 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 ofSilene latifolia revisited and revised.Genetics165, 935–938 (2003)

    PubMed PubMed Central  Google Scholar 

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Acknowledgements

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

  1. Hawaii Agriculture Research Center, Aiea, Hawaii, 96701, USA

    Zhiyong Liu, Hao Ma, Christine M. Ackerman, Makandar Ragiba, Qingyi Yu, Heather M. Pearl, Minna S. Kim, Joseph W. Charlton & Ray Ming

  2. USDA-ARS, Pacific Basin Agricultural Research Center, Hilo, Hawaii, 96720, USA

    Paul H. Moore & Francis T. Zee

  3. Department of Molecular Biosciences and Bioengineering, University of Hawaii, Honolulu, Hawaii, 96822, USA

    Hao Ma & Qingyi Yu

  4. Integrated Coffee Technologies Incorporated, Waialua, Hawaii, 96791, USA

    John I. Stiles

  5. Plant Genome Mapping Laboratory, University of Georgia, Athens, Georgia, 30602, USA

    Andrew H. Paterson

Authors
  1. Zhiyong Liu
  2. Paul H. Moore
  3. Hao Ma
  4. Christine M. Ackerman
  5. Makandar Ragiba
  6. Qingyi Yu
  7. Heather M. Pearl
  8. Minna S. Kim
  9. Joseph W. Charlton
  10. John I. Stiles
  11. Francis T. Zee
  12. Andrew H. Paterson
  13. Ray Ming

Corresponding author

Correspondence toRay Ming.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

41586_2004_BFnature02228_MOESM2_ESM.doc

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)

41586_2004_BFnature02228_MOESM3_ESM.doc

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

41586_2004_BFnature02228_MOESM4_ESM.doc

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

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Liu, Z., Moore, P., Ma, H.et al. A primitive Y chromosome in papaya marks incipient sex chromosome evolution.Nature427, 348–352 (2004). https://doi.org/10.1038/nature02228

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