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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 #332373

Research Project: Pacific Tropical/Subtropical Fruit and Nut Genetic Resource Management and Sustainable Production Systems

Location: Tropical Plant Genetic Resources and Disease Research

Title: Origin and domestication of papaya Yh chromosome

Author
item Vanburen, Robert - University Of Illinois
item Zeng, Fanchang - University Of Illinois
item Chen, Cuixia - University Of Illinois
item Zhang, Jisen - Fujian Agricultural & Forestry University
item Wai, Ching Man - University Of Illinois
item Han, Jennifer - University Of Illinois
item Aryal, Rishi - University Of Illinois
item Gschwend, Andrea - University Of Illinois
item Wang, Jianping - University Of Illinois
item Na, Jong-kuk - University Of Illinois
item Huang, Lixian - Fujian Agricultural & Forestry University
item Zhang, Lingmao - Fujian Agricultural & Forestry University
item Miao, Wengjing - Fujian Agricultural & Forestry University
item Gou, Jiqing - Texas A&M Agrilife
item Arro, Jie - University Of Illinois
item Guyot, Romain - Institute For Research And Development (IRD)
item Moore, Richard - Miami University - Ohio
item Wang, Ming-li - Hawaii Agricultural Research Center
item Zee, Francis
item Charlesworth, Deborah - University Of Edinburgh
item Moore, Paul - Hawaii Agricultural Research Center
item Yu, Qingyi - Texas A&M Agrilife
item Ming, Ray - University Of Illinois

Submitted to: Genome Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/9/2015
Publication Date: 3/11/2015
Citation: Vanburen, R., Zeng, F., Chen, C., Zhang, J., Wai, C., Han, J., Aryal, R., Gschwend, A., Wang, J., Na, J., Huang, L., Zhang, L., Miao, W., Guo, J., Arro, J., Guyot, R., Moore, R., Wang, M., Zee, F.T., Charlesworth, D., Moore, P., Yu, Q., Ming, R. 2015. Origin and domestication of papaya Yh chromosome. Genome Research. 25:524-533.

Interpretive Summary: Similar to human gender, sex in papaya is controlled by sex chromosomes. Females are XX, but in papayas two slightly different Y chromosomes distinguish males (XY) and hermaphrodites (XYh). Wild papaya populations are dioecious, with one-half male and one-half female plants, whereas cultivated papaya is predominantly gynodioecious, with two-thirds hermaphrodite and one-third female plants. Fruits from hermaphrodite plants are commonly consumed as the commercial papaya. Here we describe the sequence of the entire male-specific region of the Y (MSY) to add to previous data on the hermaphrodite-specific region of the Yh chromosome (HSY) and its X chromosome counterpart. These data combined revealed that MSY and HSY regions are very similar with only 0.4% differences in the sequences and support the hypothesis that hermaphrodite papaya is a product of human domestication.

Technical Abstract: Sex in papaya is controlled by a pair of nascent sex chromosomes. Females are XX, and two slightly different Y chromosomes distinguish males (XY) and hermaphrodites (XYh). The hermaphrodite-specific region of the Yh chromosome (HSY) and its X chromosome counterpart were sequenced and analyzed previously. We now report the sequence of the entire male-specific region of the Y (MSY). We used a BAC-by-BAC approach to sequence the MSY and resequence the Y regions of 24 wild males and the Yh regions of 12 cultivated hermaphrodites. The MSY and HSY regions have highly similar gene content and structure, and only 0.4% sequence divergence. The MSY sequences from wild males include three distinct haplotypes, associated with the populations’ geographic locations, but gene flow is detected for other genomic regions. The Yh sequence is highly similar to one Y haplotype (MSY3) found only in wild dioecious populations from the north Pacific region of Costa Rica. The low MSY3-Yh divergence supports the hypothesis that hermaphrodite papaya is a product of human domestication. We estimate that Yh arose only ~4000 yr ago, well after crop plant domestication in Mesoamerica >6200 yr ago but coinciding with the rise of the Maya civilization. The Yh chromosome has lower nucleotide diversity than the Y, or the genome regions that are not fully sex-linked, consistent with a domestication bottleneck. The identification of the ancestral MSY3 haplotype will expedite investigation of the mutation leading to the domestication of the hermaphrodite Yh chromosome. In turn, this mutation should identify the gene that was affected by the carpel-suppressing mutation that was involved in the evolution of males.