Advertisement

Tropical Plant Biology

, Volume 1, Issue 1, pp 49–57 | Cite as

Recent Origin of Dioecious and Gynodioecious Y Chromosomes in Papaya

  • Qingyi Yu
  • Rafael Navajas-Pérez
  • Eric Tong
  • Jon Robertson
  • Paul H. Moore
  • Andrew H. Paterson
  • Ray Ming
Article

Abstract

Sex of dioecious and gynodioecious papayas is controlled by two slightly different Y chromosomes, Y for males and Yh for hermaphrodites. All combinations of the Y and/or Yh chromosomes are lethal. We investigated the features of paired dioecious X- and Y-specific bacterial artificial chromosomes (BACs) and compared their sequences to corresponding gynodioecious X- and Y-specific BACs. Numerous chromosomal rearrangements were detected between the X- and Y-specific BACs, including inversions, deletions, insertions, and duplications. DNA sequence expansion was documented on the Y BAC. Dioecious and gynodioecious X-specific BACs were virtually identical. The Y- and Yh-specific BACs shared high degree of DNA sequence identity, but local chromosomal rearrangements were detected, as the consequence of suppression of recombination in the male specific region and the isolation of Y and Yh chromosomes enforced by the lethal effect. Analysis of sequence divergence between three dioecious X and Y gene pairs resulted in the estimated ages of divergence from 0.6 to 2.5 million years, reinforcing the hypothesis of a recent origin of the papaya sex chromosomes. The estimated age of divergence between Y and Yh chromosomes was approximately 73,000 years for Gene 5. Our findings indicate that Y and Yh chromosomes evolved from a common ancestral Y chromosome, possibly prior to the origin of agriculture. The existence of a hermaphrodite Yh chromosome is less likely to have resulted from human selection as once suggested.

Keywords

Carica papaya Chromosomal rearrangements Molecular evolution MSY male specific region of the Y chromosome Sex chromosomes 

Notes

Acknowledgments

We thank Chris Saski for constructing the papaya male BAC library. This work was supported by a grant from NSF to R.M., Q.Y., P.H.M., J.J., and A.H.P. (DBI-0553417) and a USDA-ARS Cooperative Agreement (CA 58-3020-8-134) with the Hawaii Agriculture Research Center.

References

  1. 1.
    Atanassov I, Delichère C, Filatov DA, Charlesworth D, Negrutiu I, Monéger F (2001) Analysis and evolution of two functional Y-linked loci in a plant sex chromosome system. Mol Biol Evol 18:2162–2168PubMedGoogle Scholar
  2. 2.
    Bachtrog D (2006) Expression profile of a degenerating neo-Y chromosome in Drosophila. Curr Biol 16:1694–1699PubMedCrossRefGoogle Scholar
  3. 3.
    Bachtrog D (2005) Sex chromosome evolution: molecular aspects of Y-chromosome degeneration in Drosophila. Genome Res 15:1393–1401PubMedCrossRefGoogle Scholar
  4. 4.
    Badillo VM (2000) Carica L. vs. Vasconcella. St. Hil. (Caricaceae): con la rehabilitación de este último. Ernstia 10:74–79Google Scholar
  5. 5.
    Badillo VM (1971) Monografia de la familia Caricaceae. Publicada por la Associacion de Profesores, Venezuela, Univ. Centr. Venez, p 220Google Scholar
  6. 6.
    Badillo VM (2001) Nota correctiva Vasconcellea St. Hil y no Vasconcella (Caricaceae). Ernstia 11:75–76Google Scholar
  7. 7.
    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
  8. 8.
    Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG, Parkhill J (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21:3422–3423PubMedCrossRefGoogle Scholar
  9. 9.
    Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997CrossRefGoogle Scholar
  10. 10.
    Delichère C, Veuskens J, Hernould M, Barbacar N, Mouras A, Negrutiu I, Monéger F (1999) SlY1, the first active gene cloned from a plant Y chromosome, encodes a WD-repeat protein. EMBO J 18:4169–4179PubMedCrossRefGoogle Scholar
  11. 11.
    Filatov DA (2005) Substitution rates in a new Silene latifolia sex linked gene, SlssX/Y. Mol Biol Evol 22:402–408PubMedCrossRefGoogle Scholar
  12. 12.
    Gupta AK (2004) Origin of agriculture and domestication of plants and animals linked to early Holocene climate amelioration. Current Sci 87:54–59Google Scholar
  13. 13.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids SYp Ser 41:95–98Google Scholar
  14. 14.
    International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  15. 15.
    Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498PubMedGoogle Scholar
  16. 16.
    Li W-H (1997) Molecular evolution. Sinauer, SunderlandGoogle Scholar
  17. 17.
    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
  18. 18.
    Ming R, Yu Q, Moore PH (2007) Sex determination in papaya. Semin Cell Dev Biol 18:401–408PubMedCrossRefGoogle Scholar
  19. 19.
    Ming R, Van Droogenbroeck B, Moore PH, Zee FT, Kyndt T, Scheldeman X, Sekioka T, Gheysen G (2005) Molecular diversity of Carica papaya and related species. In: Sharma AK, Sharma A (eds) Plant genome: biodiversity and evolution, vol. vol 1B. Science Publishers, New Hampshire, pp 229–254Google Scholar
  20. 20.
    Ming R, Moore PH, Zee F, Abbey CA, Ma H, Paterson AH (2001) Construction and characterization of a papaya BAC library as a foundation for molecular dissection of a tree-fruit genome. Theor Appl Genet 102:892–899CrossRefGoogle Scholar
  21. 21.
    Moore RC, Kozyreva O, Lebel-Hardenack S, Siroky J, Hobza R, Vyskot B, Grant SR (2003) Genetic and functional analysis of DD44, a sex-linked gene from the dioecious plant Silene latifolia provides clues to early events in sex chromosome evolution. Genetics 163:321–334PubMedGoogle Scholar
  22. 22.
    Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 106:2–9PubMedGoogle Scholar
  23. 23.
    Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  24. 24.
    Nicolas M, Marais G, Hykelova V, Janousek B, Laporte V, Vyskot B, Mouchiroud D, Neqrutiu I, Charlesworth D, Moneqer F (2005) A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biology 3:47–56CrossRefGoogle Scholar
  25. 25.
    Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  26. 26.
    Storey WB (1976) Papaya. In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 21–24Google Scholar
  27. 27.
    The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  28. 28.
    Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperm: calibrating the family tree. Proc R Soc Lond B 268:2211–2220CrossRefGoogle Scholar
  29. 29.
    Yu Q, Hou S, Feltus FA, Jones MR, Murray J, 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-liked genes. Plant J 53:124–132PubMedCrossRefGoogle Scholar
  30. 30.
    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

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Qingyi Yu
    • 1
  • Rafael Navajas-Pérez
    • 2
  • Eric Tong
    • 1
  • Jon Robertson
    • 2
  • Paul H. Moore
    • 3
  • Andrew H. Paterson
    • 2
  • Ray Ming
    • 4
  1. 1.Hawaii Agriculture Research CenterAieaUSA
  2. 2.Plant Genome Mapping LaboratoryUniversity of GeorgiaAthensUSA
  3. 3.USDA-ARSPacific Basin Agricultural Research CenterHiloUSA
  4. 4.Department of Plant BiologyUniversity of Illinois at Urbana–ChampaignUrbanaUSA

Personalised recommendations