A primitive Y chromosome in papaya marks incipient sex chromosome evolution

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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Correspondence to Ray Ming.

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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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