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Genomics of Papaya Sex Chromosomes

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Genetics and Genomics of Papaya

Part of the book series: Plant Genetics and Genomics: Crops and Models ((PGG,volume 10))

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Abstract

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.

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References

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218

    Article  CAS  Google Scholar 

  • Bachtrog D (2003) Adaptation shapes patterns of genome evolution on sexual and asexual chromosomes in Drosophila. Nat Genet 34:215–219

    Article  PubMed  CAS  Google Scholar 

  • Bachtrog D, Charlesworth B (2002) Reduced adaptation of a non-recombining neo-Y chromosome. Nature 416:323–326

    Article  PubMed  CAS  Google Scholar 

  • 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 466:612–616

    Article  PubMed  CAS  Google Scholar 

  • Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24:94–102

    Article  PubMed  Google Scholar 

  • 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 175:1945–1954

    Article  PubMed  CAS  Google Scholar 

  • 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 52:716–725

    Article  PubMed  CAS  Google Scholar 

  • 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 237–268

    Google Scholar 

  • Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997

    Article  Google Scholar 

  • Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303

    PubMed  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128

    Article  PubMed  CAS  Google Scholar 

  • Delph LF, Arntz AM, Scotti-Saintagne C, Scotti I (2010) The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64:2873–2886

    PubMed  Google Scholar 

  • Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78:737–756

    PubMed  CAS  Google Scholar 

  • Graves JAM, Shetty S (2001) Sex from W to Z: evolution of vertebrate sex chromosomes and sex determining genes. J Exp Zool 290:449–462

    Article  Google Scholar 

  • 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 109:13716–13721

    Article  PubMed  CAS  Google Scholar 

  • Havecker ER, Gao X, Voytas DF (2004) The diversity of LTR retrotransposons. Genome Biol 5:225

    Article  PubMed  Google Scholar 

  • 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 463:536–539

    Article  PubMed  CAS  Google Scholar 

  • 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 427:348–352

    Article  PubMed  CAS  Google Scholar 

  • Meuller HJ (1964) The relation of recombination to mutational advance. Mutat Res 106:2–9

    Google Scholar 

  • Ming R, Yu Q, Moore PH (2007) Sex determination in papaya. Semin Cell Dev Biol 18:401–408

    Article  PubMed  CAS  Google Scholar 

  • 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 452:991–996

    Article  PubMed  CAS  Google Scholar 

  • Ming R, Bendahmane A, Renner SS (2011) Sex chromosomes in land plants. Annu Rev Plant Biol 62:485–514

    Article  PubMed  CAS  Google Scholar 

  • 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 13:176

    Article  PubMed  CAS  Google Scholar 

  • Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606

    Article  Google Scholar 

  • Rice WR (1987) Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116:161–167

    PubMed  CAS  Google Scholar 

  • Ross MT, Grafham DV, Coffey AJ, Scherer S et al (2005) The DNA sequence of the human X chromosome. Nature 434:325–337

    Article  PubMed  CAS  Google Scholar 

  • 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 423:873–876

    Article  PubMed  CAS  Google Scholar 

  • 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 423:825–837

    Article  PubMed  CAS  Google Scholar 

  • 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 101:507–517

    Article  PubMed  CAS  Google Scholar 

  • Spigler RB, Lewers KS, Johnson AL, Ashman TL (2010) Comparative mapping reveals autosomal origin of sex chromosome in octoploid Fragaria virginiana. J Hered 101:107–117

    Article  Google Scholar 

  • Steinemann S, Steinemann M (2005) Y chromosomes: born to be destroyed. Bioessays 27: 1076–1083

    Article  PubMed  CAS  Google Scholar 

  • Storey WB (1938) Segregations of sex types in Solo papaya and their application to the selection of seed. Proc Am Soc Hortic Sci 35:83–85

    Google Scholar 

  • Storey WB (1941) The botany and sex relations of the papaya. Hawaii Agric Exp Sta Bul 87:5–22

    Google Scholar 

  • Tanurdzic M, Banks JA (2004) Sex-determining mechanisms in land plants. Plant Cell 16:61–71

    Article  Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Genet Rev 5:123–135

    Article  CAS  Google Scholar 

  • 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 116:159–173

    Article  PubMed  Google Scholar 

  • 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 109:13710–13715

    Article  PubMed  CAS  Google Scholar 

  • Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 15:1314–1326

    Google Scholar 

  • Westergaard M (1958) The mechanism of sex determination in dioecious flowering plants. Adv Genet 9:217–281

    Article  PubMed  CAS  Google Scholar 

  • 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 63:801–810

    Article  PubMed  CAS  Google Scholar 

  • 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 53:124–132

    Article  PubMed  CAS  Google Scholar 

  • 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 18:1938–1943

    Article  PubMed  CAS  Google Scholar 

  • 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 3:166–170

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Plant Biology, University of Illinois at Urbana-Champaign, 1201 W. Gregory Drive, 148 ERML, MC-051, Urbana, IL, 61801, USA

    Robert VanBuren & Ray Ming

Authors
  1. Robert VanBuren
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  2. Ray Ming
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Correspondence to Ray Ming .

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Editors and Affiliations

  1. Department of Plant Biology, University of Illinois at Urbana-Champai, Urbana, Illinois, USA

    Ray Ming

  2. Hawaii Agriculture Research Center, Kaneohe, Hawaii, USA

    Paul H. Moore

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VanBuren, R., Ming, R. (2014). Genomics of Papaya Sex Chromosomes. In: Ming, R., Moore, P. (eds) Genetics and Genomics of Papaya. Plant Genetics and Genomics: Crops and Models, vol 10. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8087-7_16

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