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A primitive Y chromosome in papaya marks incipient sex chromosome evolution

Nature volume 427, pages 348–352 (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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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.

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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

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  1. Zhiyong Liu
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Corresponding author

Correspondence to Ray Ming.

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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)

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)

Supplementary Notes (DOC 23 kb)

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Liu, Z., Moore, P., Ma, H. et al. A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427, 348–352 (2004). https://doi.org/10.1038/nature02228

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