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Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution.

ABSTRACT: Sex determination in papaya is controlled by a recently evolved XY chromosome pair, with two slightly different Y chromosomes controlling the development of males (Y) and hermaphrodites (Y(h)). To study the events of early sex chromosome evolution, we sequenced the hermaphrodite-specific region of the Y(h) chromosome (HSY) and its X counterpart, yielding an 8.1-megabase (Mb) HSY pseudomolecule, and a 3.5-Mb sequence for the corresponding X region. The HSY is larger than the X region, mostly due to retrotransposon insertions. The papaya HSY differs from the X region by two large-scale inversions, the first of which likely caused the recombination suppression between the X and Y(h) chromosomes, followed by numerous additional chromosomal rearrangements. Altogether, including the X and/or HSY regions, 124 transcription units were annotated, including 50 functional pairs present in both the X and HSY. Ten HSY genes had functional homologs elsewhere in the papaya autosomal regions, suggesting movement of genes onto the HSY, whereas the X region had none. Sequence divergence between 70 transcripts shared by the X and HSY revealed two evolutionary strata in the X chromosome, corresponding to the two inversions on the HSY, the older of which evolved about 7.0 million years ago. Gene content differences between the HSY and X are greatest in the older stratum, whereas the gene content and order of the collinear regions are identical. Our findings support theoretical models of early sex chromosome evolution.

SUBMITTER: Wang J

PROVIDER: S-EPMC3427123 | biostudies-literature | 2012 Aug

REPOSITORIES: biostudies-literature

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Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution.

Wang Jianping J Na Jong-Kuk JK Yu Qingyi Q Gschwend Andrea R AR Han Jennifer J Zeng Fanchang F Aryal Rishi R VanBuren Robert R Murray Jan E JE Zhang Wenli W Navajas-Pérez Rafael R Feltus F Alex FA Lemke Cornelia C Tong Eric J EJ Chen Cuixia C Wai Ching Man CM Singh Ratnesh R Wang Ming-Li ML Min Xiang Jia XJ Alam Maqsudul M Charlesworth Deborah D Moore Paul H PH Jiang Jiming J Paterson Andrew H AH Ming Ray R

Proceedings of the National Academy of Sciences of the United States of America 20120806 34

Sex determination in papaya is controlled by a recently evolved XY chromosome pair, with two slightly different Y chromosomes controlling the development of males (Y) and hermaphrodites (Y(h)). To study the events of early sex chromosome evolution, we sequenced the hermaphrodite-specific region of the Y(h) chromosome (HSY) and its X counterpart, yielding an 8.1-megabase (Mb) HSY pseudomolecule, and a 3.5-Mb sequence for the corresponding X region. The HSY is larger than the X region, mostly due ...[more]

PMID: 22869747

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Project description:BACKGROUND: Papaya is a major fruit crop in tropical and subtropical regions worldwide. It is trioecious with three sex forms: male, female, and hermaphrodite. Sex determination is controlled by a pair of nascent sex chromosomes with two slightly different Y chromosomes, Y for male and Yh for hermaphrodite. The sex chromosome genotypes are XY (male), XYh (hermaphrodite), and XX (female). The papaya hermaphrodite-specific Yh chromosome region (HSY) is pericentromeric and heterochromatic. Physical mapping of HSY and its X counterpart is essential for sequencing these regions and uncovering the early events of sex chromosome evolution and to identify the sex determination genes for crop improvement. RESULTS: A reiterate chromosome walking strategy was applied to construct the two physical maps with three bacterial artificial chromosome (BAC) libraries. The HSY physical map consists of 68 overlapped BACs on the minimum tiling path, and covers all four HSY-specific Knobs. One gap remained in the region of Knob 1, the only knob structure shared between HSY and X, due to the lack of HSY-specific sequences. This gap was filled on the physical map of the HSY corresponding region in the X chromosome. The X physical map consists of 44 BACs on the minimum tiling path with one gap remaining in the middle, due to the nature of highly repetitive sequences. This gap was filled on the HSY physical map. The borders of the non-recombining HSY were defined genetically by fine mapping using 1460?F2 individuals. The genetically defined HSY spanned approximately 8.5?Mb, whereas its X counterpart extended about 5.4?Mb including a 900 Kb region containing the Knob 1 shared by the HSY and X. The 8.5?Mb HSY corresponds to 4.5?Mb of its X counterpart, showing 4?Mb (89%) DNA sequence expansion. CONCLUSION: The 89% increase of DNA sequence in HSY indicates rapid expansion of the Yh chromosome after genetic recombination was suppressed 2-3 million years ago. The genetically defined borders coincide with the common BACs on the minimum tiling paths of HSY and X. The minimum tiling paths of HSY and its X counterpart are being used for sequencing these X and Yh-specific regions.

Dataset Information

Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution.

Publications

Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution.

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