Advertisement

Physical Mapping of Papaya Sex Chromosomes

  • Jianping WangEmail author
  • Jong-Kuk Na
  • Ray Ming
Chapter
Part of the Plant Genetics and Genomics: Crops and Models book series (PGG, volume 10)

Abstract

Papaya sex chromosomes have recently evolved and suitable for studying the early events of sex chromosome evolution that are not detectable in ancient sex chromosomes like those of humans. The papaya hermaphrodite-specific Y chromosome region (HSY) is pericentromeric, heterochromatic, and suppressed for recombination. Complete sequencing and analysis of the papaya sex chromosomes will advance our knowledge of sex determination mechanism(s) in plants and the evolutionary process of young sex chromosomes. Physical mapping of HSY and its X counterpart is essential for complete sequencing of the papaya sex chromosomes. The maps of bacterial artificial chromosome (BAC) in minimal tiling path for both HSY and the corresponding X region were constructed in papaya through chromosome walking. The HSY map contained 68 anchored overlapped BAC clones and spanned approximately 8.5 Mb, while the physical map for the corresponding X region had 44 BAC clones and extended about 5.4 Mb with a small gap in the middle of the map unfilled. The borders of the MSY/X region were defined by fine mapping with a large F2 population. The HSY exhibited about 89 % expansion of DNA sequence compared to the corresponding X region, indicating expansion of the Y chromosome at an early evolutionary stage. These physical maps of HSY and X corresponding region in papaya provide the foundation for sequencing and analysis of the heterochromatic young sex chromosomes in papaya.

Keywords

Bacterial Artificial Chromosome Bacterial Artificial Chromosome Clone Bacterial Artificial Chromosome Library Chromosome Walking Minimum Tiling Path 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Adam H, Collin M, Richaud F, Beule T, Cros D, Omore A, Nodichao L, Nouy B, Tregear JW (2011) Environmental regulation of sex determination in oil palm: current knowledge and insights from other species. Ann Bot 108:1529–1537PubMedCrossRefGoogle Scholar
  2. Bull J (1983) Evolution of sex determining mechanisms. Benjamin-Cummings, Menlo ParkGoogle Scholar
  3. Chailakhyan MKH (1979) Genetic and hormonal regulation of growth, flowering, and sex expression on plants. Am J Bot 66:717–736CrossRefGoogle Scholar
  4. Charlesworth D (2002) Plant sex determination and sex chromosomes. Heredity 88:94–101PubMedCrossRefGoogle Scholar
  5. Chen C, Yu Q, Hou S, Li Y, Eustice M, Skelton RL, Veatch O, Herdes RE, Diebold L, Saw J, Feng Y, Qian W, Bynum L, Wang L, Moore PH, Paull RE, Alam M, Ming R (2007) Construction of a sequence-tagged high-density genetic map of papaya for comparative structural and evolutionary genomics in brassicales. Genetics 177:2481–2491PubMedCrossRefGoogle Scholar
  6. Chiu CT (2000) Study on sex inheritance and horticultural characteristics of hermaphrodite papaya. Master thesis, National Pingtung University of Science and technology, Pingtung, p 61Google Scholar
  7. Chiu CT, Yen CR, Chang LS, Hsiao CH, Ko TS (2003) All hermaphrodite progeny are derived by self-pollinating the sunrise papaya mutant. Plant Breeding 122:431–434CrossRefGoogle Scholar
  8. Deputy JC, Ming R, Ma H, Liu Z, Fitch MM, Wang M, Manshardt R, Stiles JI (2002) Molecular markers for sex determination in papaya (Carica papaya L.). Theor Appl Genet 106:107–111PubMedGoogle Scholar
  9. Frankel R, Galun E (1977) Pollination mechanisms, reproduction and plant breeding. In: Frankel R, Gall GAE, Grossman M, Linskens HF, de Zeeuw D (eds) Mono-graphs on theoretical and applied genetics. Springer, New York. pp 141–157Google Scholar
  10. Gschwend AR, Yu Q, Moore P, Saski C, Chen C, Wang J, Na JK, Ming R (2011) Construction of papaya male and female BAC libraries and application in physical mapping of the sex chromosomes. J Biomed Biotechnol 2011:929472PubMedCrossRefGoogle Scholar
  11. Gschwend AR et al (2012) Rapid divergence and expansion of the X chromosome in papaya. Proc Natl Acad Sci USA 109:13716–13721PubMedCrossRefGoogle Scholar
  12. Hofmeyr JDJ (1938) Genetical studies of Carica papaya L. S Afr Dept Agric Sci Bull 187:64Google Scholar
  13. Hofmeyr JDJ (1939) Sex-linked inheritance in Carica papaya L. S Afr J Sci 36:283–285Google Scholar
  14. Hofmeyr JDJ (1967) Some genetic and breeding aspects of Carica papaya. Agron Trop 17:345–351Google Scholar
  15. Horovitz S, Jiménez H (1967) Cruzamientosinterespecificos e intergenericos en caricaceas y susimplicacionesfitotechicas. Agron Trop 17:323–343Google Scholar
  16. Irish EE, Nelson T (1989) Sex determination in monoecious and dioecious plants. Plant Cell 1:737–744PubMedGoogle Scholar
  17. Kumar LSS, Abraham A, Srinivasan VK (1945) The cytology of Carica papaya Linn. Indian J Agric Sci 15:242–253Google Scholar
  18. Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba M, 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. Ma H, Moore PH, Liu Z, Kim MS, Yu Q, Fitch MM, Sekioka T, Paterson AH, Ming R (2004) High-density linkage mapping revealed suppression of recombination at the sex determination locus in papaya. Genetics 166:419–436PubMedCrossRefGoogle Scholar
  20. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, Senin P, Wang W, Ly BV, Lewis KL et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–996PubMedCrossRefGoogle Scholar
  21. Ming R, Bendahmane A, Renner SS (2011) Sex chromosomes in land plants. Annu Rev Plant Biol 62:485–514PubMedCrossRefGoogle Scholar
  22. Na JK, Wang J, Murray JE, Gschwend AR, Zhang W, Yu Q, Pérez RN, Feltus FA, Chen C, Kubat Z, Moore PH, Jiang J, Paterson AH, Ming R (2012) Construction of physical maps for the sex-specific regions of papaya sex chromosomes. BMC Genomics 13:176PubMedCrossRefGoogle Scholar
  23. Nicolas M, Marais G, Hykelova V, Janousek B, Laporte V, Vyskot B, Mouchiroud D, Negrutiu I, Charlesworth D, Moneger F (2005) A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol 3:e4PubMedCrossRefGoogle Scholar
  24. Perl-Treves R (1999) Male to female conversion along the cucumber shoot: approaches to studying sex genes and floral development in Cucumis sativus. In: Ainsworth CC (ed) Sex determination in plants. Bios Scientific Publishers, Oxford, pp 189–216Google Scholar
  25. Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606CrossRefGoogle Scholar
  26. 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(6):507–517PubMedCrossRefGoogle Scholar
  27. Spigler RB, Lewers KS, Johnson AL, Ashman TL (2010) Comparative mapping reveals autosomal origin of sex chromosome in octoploid Fragaria virginiana. J Hered 101(Suppl 1):S107–S117PubMedCrossRefGoogle Scholar
  28. Spray CR, Kobayashi M, Suzuki Y, Phinney BO, Gaskin P, MacMillan J (1996) The dwarf-1 (dt) Mutant of Zea mays blocks three steps in the gibberellin-biosynthetic pathway. Proc Natl Acad Sci USA 93:10515–10518PubMedCrossRefGoogle Scholar
  29. Storey WB (1953) Genetics of the papaya. J Hered 44:70–78Google Scholar
  30. Tanurdzic M, Banks JA (2004) Sex-determining mechanisms in land plants. Plant Cell 16(Suppl):S61–S71PubMedGoogle Scholar
  31. Wang J, Na J-K, Yu Q, Gschwend AR, Han J, Zeng F, Aryal R, VanBuren R, Murray JE, Zhang W, Pérez RN, Feltus FA, Lemke C, Tong EJ, Chen C, Wai CM, Singh R, Wang M-L, Min X, Alam M, Charlesworth D, Moore PH, Jiang J, Paterson AH, Ming R (2012) Sequencing papaya X and Yh chromosomes revealed molecular basis of incipient sex chromosome evolution. PNAS 109:13710–13715PubMedCrossRefGoogle Scholar
  32. Yampolsky C, Yampolsky H (1922) Distribution of the sex forms in the phanerogamic flora. Bibl Genet 3:1–62Google Scholar
  33. Yu Q, Hou S, Hobza R, Feltus FA, Wang X, Jin W, Skelton RL, Blas A, Lemke C, Saw JH, Moore PH, Alam M, Jiang J, Paterson AH, Vyskot B, Ming R (2007) Chromosomal location and gene paucity of the male specific region on papaya Y chromosome. Mol Genet Genomics 278: 177–185PubMedCrossRefGoogle Scholar
  34. Yu Q, Hou S, Feltus FA, Jones MR, Murray JE, Veatch O, Lemke C, Saw JH, Moore RC, Thimmapuram J, Liu L, Moore PH, Alam M, Jiang J, Paterson AH, Ming R (2008) Low X/Y divergence in four pairs of papaya sex-linked genes. Plant J 53:124–132PubMedCrossRefGoogle Scholar
  35. Yu Q, Tong E, Skelton RL, Bowers JE, Jones MR, Murray JE, Hou S, Guan P, Acob RA, Luo MC, Moore PH, Alam M, Paterson AH, Ming R (2009) A physical map of the papaya genome with integrated genetic map and genome sequence. BMC Genomics 10:371PubMedCrossRefGoogle Scholar
  36. Zhang X, Feng B, Zhang Q, Zhang D, Altman N, Ma H (2005) Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol Biol 58:401–419PubMedCrossRefGoogle Scholar
  37. 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

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of Agronomy, Genetics Institute, Plant Molecular and Cellular Biology ProgramUniversity of FloridaGainesvilleUSA
  2. 2.Department of Agricultural Bio-ResourcesNational Academy of Agricultural Science, RDASuwonRepublic of Korea
  3. 3.Department of Plant BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations