Genomics of Papaya Sex Chromosomes

  • Robert VanBuren
  • Ray Ming
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 10)


Unlike most flowering plants, papaya is trioecious with separate male, female, and hermaphrodite trees. Sex determination in papaya is controlled by a pair of nascent sex chromosomes. Female papaya plants have two X chromosomes, and male and hermaphrodite papayas have an XY chromosome pair. There are two slightly different Y chromosomes: Y controlling male and Yh controlling hermaphrodite sex. Sequencing of the papaya sex chromosomes was recently completed, shedding light on the early events in sex chromosome evolution. The hermaphrodite-specific region of the Y chromosome (HSY) has expanded drastically in comparison to its X counterpart, mostly due to retrotransposons and other repetitive elements. Gene trafficking, loss, and degradation are a prominent feature of the HSY, despite its young evolutionary age. Two large-scale inversions were detected in the HSY, resulting in suppression of recombination and subsequent fixation of sex chromosomes. In this chapter, the genetics and genomics of the papaya sex chromosomes are discussed, as well as the major findings from the recently completed X and HSY sequences.


Simple Sequence Repeat Marker Collinear Region Papaya Genome Repeat Accumulation Knob Structure 
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  1. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218CrossRefGoogle Scholar
  2. Bachtrog D (2003) Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes in Drosophila. Nat Genet 34:215–219PubMedCrossRefGoogle Scholar
  3. Bachtrog D, Charlesworth B (2002) Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416:323–326PubMedCrossRefGoogle Scholar
  4. Bellott DW, Skaletsky H, Pynitkova T, Mardis ER et al (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466:612–616PubMedCrossRefGoogle Scholar
  5. Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24:94–102PubMedCrossRefGoogle Scholar
  6. Bergero R, Forrest A, Kamau E, Charlesworth D (2007) Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes. Genetics 175:1945–1954PubMedCrossRefGoogle Scholar
  7. Blas AL, Yu Q, Chen C, Veatch O, Moore PH, Paull RE, Ming R (2009) Enrichment of a papaya high-density genetic map with AFLP markers. Genome 52:716–725PubMedCrossRefGoogle Scholar
  8. Charlesworth D (1985) Distribution of dioecy and self-incompatibility in angiosperms. In: Greenwood PJ, Slatkin M (eds) Evolution—essays in honour of John Maynard Smith. Cambridge University Press, Cambridge, pp 237–268Google Scholar
  9. Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997CrossRefGoogle Scholar
  10. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303PubMedGoogle Scholar
  11. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128PubMedCrossRefGoogle Scholar
  12. Delph LF, Arntz AM, Scotti-Saintagne C, Scotti I (2010) The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64:2873–2886PubMedGoogle Scholar
  13. Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78:737–756PubMedGoogle Scholar
  14. Graves JAM, Shetty S (2001) Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes. J Exp Zool 290:449–462CrossRefGoogle Scholar
  15. Gschwend AR, Yu Q, Tong EJ, Zeng F, Han J, VanBuren R et al (2012) Rapid divergence and expansion of the X chromosome in papaya. Proc Natl Acad Sci USA 109:13716–13721PubMedCrossRefGoogle Scholar
  16. Havecker ER, Gao X, Voytas DF (2004) The diversity of LTR retrotransposons. Genome Biol 5:225PubMedCrossRefGoogle Scholar
  17. Hughes JF, Skaletsky H, Pyntikova T, Graves TA et al (2010) Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463:536–539PubMedCrossRefGoogle Scholar
  18. Liu Z, Moore PH, Ma H, Ackerman CM, Makandar R, Yu Q, Pearl HM, Kim MS, Charlton JW, Stiles JI, Zee FT, Paterson AH, Ming R (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427:348–352PubMedCrossRefGoogle Scholar
  19. Meuller HJ (1964) The relation of recombination to mutational advance. Mutat Res 106:2–9Google Scholar
  20. Ming R, Yu Q, Moore PH (2007) Sex determination in papaya. Semin Cell Dev Biol 18:401–408PubMedCrossRefGoogle Scholar
  21. Ming R, Hou S, Feng Y, Yu Q et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996PubMedCrossRefGoogle Scholar
  22. Ming R, Bendahmane A, Renner SS (2011) Sex chromosomes in land plants. Annu Rev Plant Biol 62:485–514PubMedCrossRefGoogle Scholar
  23. Na JK, Wang J, Murray JE, Gschwend AR, Zhang W, Yu Q et al (2012) Construction of physical maps for the sex-specific regions of papaya sex chromosomes. BMC Genomics 13:176PubMedCrossRefGoogle Scholar
  24. Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606CrossRefGoogle Scholar
  25. Rice WR (1987) Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116:161–167PubMedGoogle Scholar
  26. Ross MT, Grafham DV, Coffey AJ, Scherer S et al (2005) The DNA sequence of the human X chromosome. Nature 434:325–337PubMedCrossRefGoogle Scholar
  27. Rozen S, Skaletsky H, Marszalek JD, Minx PJ et al (2003) Abundant gene conversion between arms of massive palindromes in human and ape Y chromosomes. Nature 423:873–876PubMedCrossRefGoogle Scholar
  28. Skaletsky H, Kuroda-kawaguchi T, Minx PJ, Cordum HS et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837PubMedCrossRefGoogle Scholar
  29. Spigler RB, Lewers KS, Main DS, Ashman TL (2008) Genetic mapping of sex determination in a wild strawberry, Fragaria virginiana, reveals earliest form of sex chromosome. Heredity 101:507–517PubMedCrossRefGoogle Scholar
  30. Spigler RB, Lewers KS, Johnson AL, Ashman TL (2010) Comparative mapping reveals autosomal origin of sex chromosome in octoploid Fragaria virginiana. J Hered 101:107–117CrossRefGoogle Scholar
  31. Steinemann S, Steinemann M (2005) Y chromosomes: born to be destroyed. Bioessays 27: 1076–1083PubMedCrossRefGoogle Scholar
  32. Storey WB (1938) Segregations of sex types in Solo papaya and their application to the selection of seed. Proc Am Soc Hortic Sci 35:83–85Google Scholar
  33. Storey WB (1941) The botany and sex relations of the papaya. Hawaii Agric Exp Sta Bul 87:5–22Google Scholar
  34. Tanurdzic M, Banks JA (2004) Sex-determining mechanisms in land plants. Plant Cell 16:61–71CrossRefGoogle Scholar
  35. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  36. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Genet Rev 5:123–135CrossRefGoogle Scholar
  37. Tsuda Y, Nishida-Umehara C, Ishijima J, Yamada K, Matsuda Y (2007) Comparison of the Z and W sex chromosomal architectures in elegant crested tinamou (Eudromia elegans) and ostrich (Struthio camelus) and the process of sex chromosome differentiation in palaeognathous birds. Chromosoma 116:159–173PubMedCrossRefGoogle Scholar
  38. Wang J, Na JK, Yu Q, Gschwend AR, Han J et al (2012) Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci USA 109:13710–13715PubMedCrossRefGoogle Scholar
  39. Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 15:1314–1326Google Scholar
  40. Westergaard M (1958) The mechanism of sex determination in dioecious flowering plants. Adv Genet 9:217–281PubMedCrossRefGoogle Scholar
  41. Wu X, Wang J, Na JK, Yu Q, Moore RC, Zee F, Huber SC, Ming R (2010) The origin of the non-recombining region of sex chromosomes in Carica and Vasconcellea. Plant J 63:801–810PubMedCrossRefGoogle Scholar
  42. Yu Q, Hou S, Feltus FA, Jones MR et al (2008) Low X/Y divergence in four pairs of papaya sex-linked genes. Plant J 53:124–132PubMedCrossRefGoogle Scholar
  43. Zhang W, Wang X, Yu Q, Ming R, Jiang J (2008) DNA methylation and heterochromatinization in the male-specific region of the primitive Y chromosome of papaya. Genome Res 18:1938–1943PubMedCrossRefGoogle Scholar
  44. Zhang W, Wai CM, Ming R, Yu Q, Jiang J (2010) Integration of genetic and cytological maps and development of a pachytene chromosome-based karyotype in papaya. Trop Plant Biol 3:166–170CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Plant BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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