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.
Similar content being viewed by others
References
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 18:2162–2168
Bachtrog D (2006) Expression profile of a degenerating neo-Y chromosome in Drosophila. Curr Biol 16:1694–1699
Bachtrog D (2005) Sex chromosome evolution: molecular aspects of Y-chromosome degeneration in Drosophila. Genome Res 15:1393–1401
Badillo VM (2000) Carica L. vs. Vasconcella. St. Hil. (Caricaceae): con la rehabilitación de este último. Ernstia 10:74–79
Badillo VM (1971) Monografia de la familia Caricaceae. Publicada por la Associacion de Profesores, Venezuela, Univ. Centr. Venez, p 220
Badillo VM (2001) Nota correctiva Vasconcellea St. Hil y no Vasconcella (Caricaceae). Ernstia 11:75–76
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
Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG, Parkhill J (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21:3422–3423
Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997
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 18:4169–4179
Filatov DA (2005) Substitution rates in a new Silene latifolia sex linked gene, SlssX/Y. Mol Biol Evol 22:402–408
Gupta AK (2004) Origin of agriculture and domestication of plants and animals linked to early Holocene climate amelioration. Current Sci 87:54–59
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids SYp Ser 41:95–98
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
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 17:1483–1498
Li W-H (1997) Molecular evolution. Sinauer, Sunderland
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 427:348–352
Ming R, Yu Q, Moore PH (2007) Sex determination in papaya. Semin Cell Dev Biol 18:401–408
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 229–254
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 102:892–899
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 163:321–334
Muller HJ (1964) The relation of recombination to mutational advance. Mutat Res 106:2–9
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
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 3:47–56
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Storey WB (1976) Papaya. In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 21–24
The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperm: calibrating the family tree. Proc R Soc Lond B 268:2211–2220
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 53:124–132
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 278:177–185
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by
Appendix
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplemental Figure 1
Multiple sequence alignment of Gene 6 alleles from Yh- (PH95B12), Y-(DM62K05), and X- (DM10G24) chromosomes of trioecious papaya (DOC 73 kb).
Rights and permissions
About this article
Cite this article
Yu, Q., Navajas-Pérez, R., Tong, E. et al. Recent Origin of Dioecious and Gynodioecious Y Chromosomes in Papaya. Tropical Plant Biol. 1, 49–57 (2008). https://doi.org/10.1007/s12042-007-9005-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12042-007-9005-7