Abstract
Sex chromosomes in flowering plants evolved recently and many of them remain homomorphic, including those in papaya. We investigated the chromosomal location of papaya’s small male specific region of the hermaphrodite Y (Yh) chromosome (MSY) and its genomic features. We conducted chromosome fluorescence in situ hybridization mapping of Yh-specific bacterial artificial chromosomes (BACs) and placed the MSY near the centromere of the papaya Y chromosome. Then we sequenced five MSY BACs to examine the genomic features of this specialized region, which resulted in the largest collection of contiguous genomic DNA sequences of a Y chromosome in flowering plants. Extreme gene paucity was observed in the papaya MSY with no functional gene identified in 715 kb MSY sequences. A high density of retroelements and local sequence duplications were detected in the MSY that is suppressed for recombination. Location of the papaya MSY near the centromere might have provided recombination suppression and fostered paucity of genes in the male specific region of the Y chromosome. Our findings provide critical information for deciphering the sex chromosomes in papaya and reference information for comparative studies of other sex chromosomes in animals and plants.
Similar content being viewed by others
References
Carvalho AB, Clark AG (2005) Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307:108–110
Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033
Charlesworth D (2002) Plant sex determination and sex chromosomes. Heredity 88:94–101
Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997
Charlesworth B, Langley CH, Stephan W (1986) The evolution of restricted recombination and the accumulation of repeated DNA sequences. Genetics 112:947–962
Darlington CD (1958) The evolution of genetic systems. Basic Books Inc., New York
Desfeux C, Maurice S, Henry J-P, Lejeune B, Gouyon P-H (1996) Evolution of reproductive systems in the genus Silene. Proc R Soc Lond B 263:409–414
Di Stilio VS, Kesseli RV, Mulcahy DL (1998) A pseudoautosomal random amplified polymorphic DNA marker for the sex chromosomes of Silene dioica. Genetics 148:2057–2062
Filatov DA (2005) Evolutionary history of Silene latifolia sex chromosomes revealed by genetic mapping of four genes. Genetics 170:975–979
Haupt W, Fischer TC, Winderl S, Fransz P, Torres-Ruiz RA (2001) The CENTROMERE 1 (CEN1) region of Arabidopsis thaliana: architecture and functional impact of chromatin. Plant J 27:285–296
Heslop-Harrison JS (1998) Cytogenetic analysis of Arabidopsis. In: Martinez-Zapater JM, Salinas J (Eds) Arabidopsis protocols. Humana Press, Totowa, pp. 119–127
Jackson SA, Wang M, Goodman HM, Jiang J (1998) Fiber-FISH analysis of repetitive DNA elements in Arabidopsis thaliana. Genome 41:566–572
Jaarola M, Martin RH, Ashley T (1998) Direct evidence for suppression of recombination with two pericentric inversions in humans: a new sperm-FISH technique. Am J Hum Genet 63:218–224
Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular views of plant centromeres. Trends Plant Sci 12:570–575
Kondo M, Hornung U, Nanda I, Imai S, Sasaki T, Shimizu A, Asakawa S, Hori H, Schmid M, Shimizu N, Schartl M (2006) Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16:815–826
Kondo M, Nanda I, Hornung U, Schmid M, Schartl M (2004) Evolutionary origin of the medaka Y chromosome. Curr Biol 14:1664–1669
Kurata N, Nonomura K-I, Harushima Y (2002) Rice genome organization: the centromere and genome interactions. Ann Bot 90:427–435
Lai CWJ, Yu Q, Hou S, Skelton RL, Jones MR, Lewis KLT, Murray J, Eustice M, Guan P, Agbayani R, Moore PH, Ming R, Presting GG (2006) Analysis of papaya BAC end sequences reveals first insights into the organization of a fruit tree genome. Mol Genet Genomics 276:1–12
Lengerova M, Moore RC, Grant SR, Vyskot B (2003) The sex chromosomes of Silene latifolia revisited and revised. Genetics 165:935–938
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
Ma H, Moore PH, Liu Z, Kim MS, Yu Q, Fitch MMM, Sekioka T, Paterson AH, Ming R (2004) High-density linkage mapping revealed suppression of recombination at the sex determination locus in papaya. Genetics 166:419–436
Maloisel L, Rossignol J-L (1998) Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev 12:1381–1389
Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaquchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559–563
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
Ming R, Q Yu, Moore PH (2007) Sex determination in papaya. Semin Cell Dev Biol (in press)
Nagaki K, Talbert PB, Zhong CX, Dawe RK, Henikoff S, Jaing J (2003) Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics 163:1221–1225
Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M (2002) A duplicated copy of DMRT1 in the sex determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99:11778–11783
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 Biol 3:47–56
Ohno S (1967) Sex chromosomes and sex linked genes. Springer, Berlin, pp 5–13
Peichel CL, Ross JA, Matson CK, Dickson M, Grimwood J, Schmutz J, Myers RM, Mori S, Schluter D, Kingsley DM (2004) The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Curr Biol 14:1416–1424
Raymond CS, Parker ED, Kettlewell JR, Brown LG, Page DC, Kusz K, Jaruzelska J, Reinberg Y, Flejter WL, Bardwell VJ, Hirsch B, Zarkower D (1999) A region of human chromosome 9 p required for testis development contains two genes related to known sexual regulators. Hum Mol Genet 8:989–996
Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP et al (2005) The DNA sequence of the human X chromosome. Nature 434:325–337
Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837
Smith CA, Sinclair AH (2004) Sex determination: insights from the chicken. BioEssays 26:120–132
Storey WB (1976) Papaya. In: Simmonds NW (Ed) Evolution of crop plants. Longman, London, pp 21–24
Waters PD, Wallis MC, Graves, JAM (2007) Mammalian sex-origin and evolution of the Y chromosome and SRY. Semin Cell Dev Biol. doi: 10.1016/j.semcdb.2007.02.007
Westergaard M (1958) The mechanism of sex determination in flowering plants. Adv Genet 9:217–281
Yan H, Jin W, Nagaki K, Tian S, Ouyang S, Buell CR, Talbert PB, Henikoff S, Jiang J (2005) Transcription and histone modifications in the recombination-free region spanning a rice centromere. Plant Cell 17:3227–3238
Zluvova J, Janousek B, Negrutiu I, Vyskot B (2005) Comparison of the X and Y chromosome organization in Silene latifolia. Genetics 170:1431–1434
Acknowledgments
We thank Jianping Wang, Jong-Kuk Na, Zdenek Kubat, Wenli Zhang, Andrea Gschwend, and Virginie Lachaise for technical assistance, and Henrik Albert and Stephanie Whalen for reviewing the manuscript. 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), a USDA-ARS Cooperative Agreement (CA 58-3020-8-134) with the Hawaii Agriculture Research Center, and a GACR grant to B.V. (521/06/0056) from the Czech Republic.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Y. Van de Peer.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yu, Q., Hou, S., Hobza, R. et al. Chromosomal location and gene paucity of the male specific region on papaya Y chromosome. Mol Genet Genomics 278, 177–185 (2007). https://doi.org/10.1007/s00438-007-0243-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-007-0243-z