Skip to main content

Thank you for visiting nature.com. 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.

  • Letter
  • Published:

An X-linked gene with a degenerate Y-linked homologue in a dioecious plant

Abstract

Most flowering plants are hermaphroditic, having flowers with both male and female parts. Less than 4% of plant species are dioecious (with individuals of separate sexes), and many of these species have chromosome-mediated sex determination. The taxonomic distribution of separate sexes and chromosomal sex-determination systems in the flowering plants indicates that plant sex chromosomes have evolved recently through replicated, independent events1,2,3,4, contrasting with the ancient origins of mammalian and insect sex chromosomes. Plant sex chromosomes, therefore, offer opportunities to study the most interesting early stages of the evolution of sex chromosomes. Here we show that a gene encoding a male-specific protein is linked to the X chromosome in the dioecious plant Silene latifolia, and that it has a degenerate homologue in the non-pairing region of the Y chromosome. The Y-linked locus has degenerated as a result of nucleotide deletion and the accumulation of repetitive sequences. We have identified both the first X-linked gene and the first pair of homologous sex-linked loci to be found in plants. The homology between the active X-linked locus and the degenerate Y-linked locus supports a common ancestry for these two loci.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Sex linkage of MROS3.
Figure 2: Gel photograph of the products of anchored PCR of MROS3 from the mother and father of the family array used throughout the study.
Figure 3: Sequence comparison of MROS3-X (upper sequence) and MROS3-Y (lower sequence).

Similar content being viewed by others

References

  1. Charlesworth, D. in Essays in Honour of John Maynard Smith (eds Greenwood, P. J. & Slatkin, M.) 237–268 (Cambridge Univ. Press, (1985)).

    Google Scholar 

  2. Darwin, C. R. The Different forms of Flowers on Plants of the Same Species (John Murray, London, (1877)).

    Book  Google Scholar 

  3. Mayer, S. S. & Charlesworth, D. Genetic evidence for mutliple origins of dioecy in the Hawaiian shrub Wikstroemia (Thymelaeaceae). Evolution 46, 207–215 (1992).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Desfeux, C., Maurice, S., Henry, J.-P., Lejeune, B. & Gouyon, P.-H. Evolution of reproductive systems in the genus Silene. Proc. R. Soc. Lond. B 263, 409–414 (1996).

    Article  ADS  CAS  Google Scholar 

  6. van Nigtevecht, G. Genetic studies in dioecious Melandrium. II. Sex determination in Melandrium album and Melandrium dioicum. Genetica 37, 307–344 (1966).

    Article  Google Scholar 

  7. van Nigtevecht, G. Genetic studies in dioecious Melandrium. I. Sex-linked and sex-influenced inheritance in Melandrium album and Melandrium dioicum. Genetica 37, 281–306 (1966).

    Article  Google Scholar 

  8. Vyskot, B., Araya, A., Veuskens, J., Negrutiu, I. & Mouras, A. DNA methylation of sex chromosomes in a dioecious plant, Melandrium album. Mol. Gen. Genet. 239, 219–224 (1993).

    CAS  PubMed  Google Scholar 

  9. Grant, S. et al. Genetics of sex determination in flowering plants. Dev. Gen. 15, 214–230 (1994).

    Article  Google Scholar 

  10. Ye, D. et al. Sex determination in the dioecious Melandrium. I. First lessons from androgenic haploids. Sex. Plant Reprod. 3, 179–186 (1990).

    Article  Google Scholar 

  11. Donnison, I. S., Stroky, J., Vyskot, B., Saedler, H. & Grant, S. R. Isolation of Y chromosome-specific sequences from Silene latifolia and mapping of male sex determining genes using representational difference analysis. Genetics 144, 1893–1901 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  13. Charlesworth, B. Model for evolution of Y chromosomes and dosage compensation. Proc. Natl Acad. Sci. USA 75, 5618–5622 (1978).

    Article  ADS  CAS  Google Scholar 

  14. Charlesworth, B. The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 6, 149–162 (1996).

    Article  CAS  Google Scholar 

  15. Rejón, C. R., Jamilena, M., Ramos, M. G., Parker, J. S. & Rejón, M. R. Cytogenetic and molecular analysis of the multiple sex chromosome system of Rumex acetosa. Heredity 72, 209–215 (1994).

    Article  Google Scholar 

  16. Zuk, J. Autoradiographic studies in Rumex with special reference to sex chromosomes. Chromosomes Today 2, 183–188 (1969).

    Google Scholar 

  17. Guttman, D. S. et al. Multiple infections of Ixodes scapularis ticks by Borrelia burgdorferi as revealed by single-strand conformation polymorphism analysis. J. Clin. Microbiol. 34, 652–656 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Hongyo, T., Buzard, G. S., Calvert, R. J. & Weghorst, C. M. ‘Cold SSCP’: a simple, rapid and non-radioactive method for optimized single-stranded conformation polymorphism analyses. Nucleic Acids Res. 21, 3637–3642 (1993).

    Article  CAS  Google Scholar 

  19. Matsunaga, S. et al. Isolation and developmental expression of male reproductive organ-specific genes in a dioecious campion, Melandrium album (Silene latifolia). Plant J. 10, 679–689 (1996).

    Article  CAS  Google Scholar 

  20. Jukes, T. & Cantor, C. in Mammalian Protein Metabolism (ed. Munro, H. N.) 21–132 (Academic, New York, (1969)).

    Book  Google Scholar 

  21. Nei, M. Molecular Evolutionary Genetics 1–512 (Columbia Univ. Press, New York, (1987)).

    Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  23. Marshall Graves, J. A. The origin and function of the mammalian Y chromosome and Y-borne genes—an evolving understanding. BioEssays 17, 311–321 (1995).

    Article  Google Scholar 

  24. Pedersen, S., Simonsen, V. & Loeschcke, V. Overlap of gametophytic and sporophytic gene expression in barley. Theor. Appl. Genet. 75, 200–206 (1987).

    Article  Google Scholar 

  25. Stinson, J. R. et al. Genes expressed in the male gametophyte of flowering plants and their isolation. Plant Physiol. 83, 442–447 (1987).

    Article  CAS  Google Scholar 

  26. Tanksley, S. D., Zamir, D. & Rick, C. M. Evidence for extensive overlap of sporophytic and gametophytic gene expression in Lycopersicon esculentum. Science 213, 453–455 (1981).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank B. Charlesworth for input, counsel and support, and J. Greenberg, T.Morton and J. Mach for assistance with the manuscript. This work was supported by a grant from the NIH (to D.C. and B. Charlesworth).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David S. Guttman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guttman, D., Charlesworth, D. An X-linked gene with a degenerate Y-linked homologue in a dioecious plant. Nature 393, 263–266 (1998). https://doi.org/10.1038/30492

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/30492

This article is cited by

Comments

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.

Search

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