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ARS Home » Pacific West Area » Hilo, Hawaii » Daniel K. Inouye U.S. Pacific Basin Agricultural Research Center » Tropical Plant Genetic Resources and Disease Research » Research » Publications at this Location » Publication #355524

Title: Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep

Author
item VANBUREN, ROBERT - University Of Illinois
item MAN WAI, CHING - University Of Illinois
item ZHANG, JISEN - Fujian Agriculture And Forest University
item HAN, JENNIFER - University Of Illinois
item ARRO, JIE - University Of Illinois
item LIN, ZHICONG - Fujian Agriculture And Forest University
item LIAO, ZHENYANG - Fujian Agriculture And Forest University
item YU, QINGYI - Texas A&M University
item WANG, MING-LI - Hawaii Agricultural Research Center
item ZEE, FRANCIS - Retired ARS Employee
item MOORE, RICHARD - Miami University - Ohio
item CHARLESWORTH, DEBORAH - University Of Edinburgh
item MING, RAY - University Of Illinois

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/31/2016
Publication Date: 11/28/2016
Citation: Vanburen, R., Man Wai, C., Zhang, J., Han, J., Arro, J., Lin, Z., Liao, Z., Yu, Q., Wang, M., Zee, F., Moore, R.C., Charlesworth, D., Ming, R. 2016. Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep. Genome Biology. 17:230.

Interpretive Summary: Similar to humans, papayas have a sex chromosomes that contain Y linked genes for males and X linked genes for females. In previous studies, the genes in the Y region were similar when comparing different papayas suggesting they all shared a similar ancestor. The same population of plants were used in this current study to compare the X linked genes and they were found to be extremely similar. This is thought to be caused by recent selection to choose a trait that is either beneficial to the male papaya plant or a trait that benefits just the females or both sexes of papaya plants.

Technical Abstract: Background: The papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from. The same populations were used to study nucleotide diversity and population structure in the X-linked region. Results: Diversity is very low for all genes in the X-linked region in the wild dioecious population, with nucleotide diversity psyn = 0.00017, tenfold lower than the autosomal region (psyn = 0.0017) and 12-fold lower than the Y-linked region (psyn = 0.0021). Analysis of the X-linked sequences shows an undivided population, suggesting a geographically wide diversity-reducing event, whereas two subpopulations were observed in the autosomes separating gynodioecy and dioecy and three subpopulations in the Y-linked region separating three male populations. The extremely low diversity in the papaya X-linked region was probably caused by a recent, strong selective sweep before domestication, involving either the spread of a recessive mutation in an X-linked gene that is beneficial to males or a partially dominant mutation that benefitted females or both sexes. Nucleotide diversity in the domesticated X samples is about half that in the wild Xs, probably due to the bottleneck when hermaphrodites were selected during domestication. Conclusions: The extreme low nucleotide diversity in the papaya X-linked region is much greater than observed in humans, great apes, and the neo-X chromosome of Drosophila miranda, which show the expected pattern of Y-linked genes < X-linked genes < autosomal genes; papaya shows an unprecedented pattern of X-linked genes < autosomal genes < Y-linked genes.