Skip to main content

Papaya Repeat Database

  • Chapter
  • First Online:
Genetics and Genomics of Papaya

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

Abstract

In this chapter, we report a detailed analysis of repetitive elements in the papaya genome, including transposable elements (TEs), tandemly arrayed sequences, and high copy number genes. These repetitive sequences account for ~56 % of the papaya genome, with TEs being the most abundant at 52 %, tandem repeats at 1.3 %, and high copy number genes at 3 %. Most common types of TEs are represented in the papaya genome with retrotransposons being the dominant class, accounting for 40 % of the genome. The most prevalent retrotransposons are Ty3–gypsy (27.8 %) and Ty1–copia (5.5 %). Among the tandem repeats, microsatellites are the most abundant in number but represent only 0.19 % of the genome. Minisatellites and satellites are less abundant but represent 0.68 and 0.43 % of the genome, respectively, due to greater repeat length. Despite an overall smaller gene repertoire in papaya than many other angiosperms, a significant fraction of genes (>2 %) are present in large gene families with copy number greater than 20. Papaya sex chromosomes are significantly enriched of a repertoire of repetitive sequences, and the male-specific region expanded by massively accumulation of repeated DNA, representing 83 % (mostly TE), while the corresponding X region included 70 % of such repeats. In an effort to integrate all the information, we provide here the pipeline to gather and process data related to repetitive elements in papaya.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Arabidopsis Genome Initiative (2001) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Arkhipova IR (2005) Mobile genetic elements and sexual reproduction. Cytogenet Genome Res 110(1–4):372–382

    Article  PubMed  CAS  Google Scholar 

  • Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot (Lond) 95:127–132

    Article  CAS  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580

    Article  PubMed  CAS  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 

  • Bousios A, Minga E, Kalitsou N, Pantermali M, Tsaballa A, Darzentas N (2012) MASiVEdb: the sirevirus plant retrotransposon database. BMC Genomics 13(1):158

    Article  PubMed  CAS  Google Scholar 

  • Camacho JP, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc Lond B Biol Sci 355:163–178

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95(2):118–128

    Article  PubMed  CAS  Google Scholar 

  • 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(4):2481–2491

    Article  PubMed  CAS  Google Scholar 

  • Cheng XD, Ling HQ (2006) Non-LTR retrotransposons: LINEs and SINEs in plant genome. Yichuan 28:731–736

    CAS  Google Scholar 

  • Contento A, Heslop-Harrison JS, Schwarzacher T (2005) Diversity of a major repetitive DNA sequence in diploid and polyploid Triticeae. Cytogenet Genome Res 109:34–42

    Article  PubMed  CAS  Google Scholar 

  • de la Herrán R, Cuñado N, Navajas-Pérez R, Santos JL, Ruiz Rejón C, Garrido-Ramos MA, Ruiz Rejón M (2005) The controversial telomeres of lily plants. Cytogenet Genome Res 109(1–3):144–147

    PubMed  Google Scholar 

  • Edgar RC, Myers EW (2005) PILER: identification and classification of genomic repeats. Bioinformatics 21(Suppl 1):i152–i158

    Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5(6):435–445

    Article  PubMed  CAS  Google Scholar 

  • Eustice M, Yu Q, Lai C, Hou S, Thimmapuram J, Liu L, Alam M, Moore P, Presting G, Ming R (2008) Development and application of microsatellite markers for genomic analysis of papaya. Tree Genet Genomes 4:333–341

    Article  Google Scholar 

  • Fajkus J, Kovarik A, Kralovics R, Bezdek M (1995) Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol Gen Genet 247:633–638

    Article  PubMed  CAS  Google Scholar 

  • Fedoroff N (2000) Transposons and genome evolution in plants. Proc Natl Acad Sci USA 97(13):7002–7007

    Article  PubMed  CAS  Google Scholar 

  • Ganal MW, Lapitan NL, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3:87–94

    PubMed  CAS  Google Scholar 

  • Gemayel R, Vinces MD, Legendre M, Verstrepen KJ (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu Rev Genet 44:445–477

    Article  PubMed  CAS  Google Scholar 

  • 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 2011:929472

    Article  PubMed  Google Scholar 

  • Gschwend AR, Yu Q, Tong EJ, Zeng F, Han J, VanBuren R, Aryal R, Charlesworth D, Moore PH, Paterson AH, Ming R (2012) Rapid divergence and expansion of the X chromosome in papaya. Proc Natl Acad Sci USA. 109(34):13716–13721

    Google Scholar 

  • Harrison GE, Heslop-Harrison JS (1995) Centromeric repetitive DNA sequences in the genus Brassica. Theor Appl Genet 90:157–165

    Article  CAS  Google Scholar 

  • Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable “minisatellite” regions in human DNA. Nature 314:67–73

    Article  PubMed  CAS  Google Scholar 

  • Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, McCouch SR, Wessler SR (2003) An active DNA transposon family in rice. Nature 421(6919):163–167

    Article  PubMed  CAS  Google Scholar 

  • Jurka J (2003) Repetitive DNA: detection, annotation, and analysis. In: Krawetz SA, Womble DD (eds) Introduction to bioinformatics: a theoretical and practical approach. Humana Press, Totowa

    Google Scholar 

  • Kipling D (1995) The telomere. Oxford University Press, Oxford

    Google Scholar 

  • Kubis SE, Schmidt T, Heslop-Harrison JS (1998) Repetitive DNA elements as a major component of plant genomes. Ann Bot (Lond) 82:45–55

    Article  CAS  Google Scholar 

  • Li W, Godzik A (2006) CD-HIT: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659

    Article  PubMed  CAS  Google Scholar 

  • Lim KB, de Jong H, Yang TJ, Park JY, Kwon SJ, Kim JS, Lim MH, Kim JA, Jin M, Jin YM, Kim SH, Lim YP, Bang JW, Kim HI, Park BS (2005) Characterization of rDNAs and tandem repeats in the heterochromatin of Brassica rapa. Mol Cells 19:436–444

    PubMed  CAS  Google Scholar 

  • Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, Aguilar-Rodríguez J, Vicente-Ripolles M, Fuster G, Bernet GP, Maumus F, Muñoz-Pomer A, Sempere JM, Latorre A, Moya A (2011) The gypsy database (GyDB) of mobile genetic elements: release 2.0. Nucleic Acids Res 39 (database issue):D70–D74

    Google Scholar 

  • Lunyak VV, Prefontaine GG, Núñez E, Cramer T, Ju BG, Ohgi KA, Hutt K, Roy R, García-Díaz A, Zhu X, Yung Y, Montoliu L, Glass CK, Rosenfeld MG (2007) Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 317(5835):248–251

    Article  PubMed  CAS  Google Scholar 

  • 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(1):419–436

    Article  PubMed  CAS  Google Scholar 

  • Macas J, Mészáros T, Nouzová M (2002) PlantSat: a specialized database for plant satellite repeats. Bioinformatics 18:28–35

    Article  PubMed  CAS  Google Scholar 

  • Martienssen R, Irish V (1999) Copying out our ABCs: the role of gene redundancy in interpreting genetic hierarchies. Trends Genet 15(11):435–437

    Article  PubMed  CAS  Google Scholar 

  • Martinez-Zapater JM, Estelle MA, Somerville CR (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet 204:417–423

    Article  CAS  Google Scholar 

  • Matsunaga S (2009) Junk DNA promotes sex chromosome evolution. Heredity 102:525–526

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci USA 36:344–355

    Article  PubMed  CAS  Google Scholar 

  • Meagher TR, Vassiliadis C (2005) Phenotypic impacts of repetitive DNA in flowering plants. New Phytol 168:71–80

    Article  PubMed  CAS  Google Scholar 

  • Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KF, Wing RA (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354

    Article  PubMed  CAS  Google Scholar 

  • Miklos GL (1985) Localited highly repetitive DNA sequences in vertebrate and invertebrate genomes. In: McIntryre JR (ed) Molecular evolutionary genetics. Plenum, New York

    Google Scholar 

  • Miller JT, Jackson SA, Nasuda S, Gill BS, Wing RA, Jiang J (1998) Cloning and characterization of a centromere specific DNA element from Sorghum bicolor. Theor Appl Genet 96:832–839

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ming R, Hou S, Feng Y 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, Navajas-Pérez R, 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 13:176

    Google Scholar 

  • Nagarajan N, Pop M (2009) Parametric complexity of sequence assembly: theory and applications to next generation sequencing. J Comput Biol 16(7):897–908

    Article  PubMed  CAS  Google Scholar 

  • Nagarajan N, Navajas-Pérez R, Pop M, Alam M, Ming R, Paterson AH, Salzberg SL (2008) Genome-wide analysis of repetitive elements in papaya. Trop Plant Biol 1(3–4):191–201

    Article  CAS  Google Scholar 

  • Navajas-Pérez R (2012) The genus Rumex: a plant model to study sex-chromosomes evolution. In: Navajas-Pérez R (ed) New insights on plant sex chromosomes, 1st edn. Nova, Hauppauge

    Google Scholar 

  • Navajas-Pérez R, Paterson AH (2009) Patterns of tandem repetition in plant whole genome assemblies. Mol Gen Genomics 281:579–590

    Article  Google Scholar 

  • Navajas-Pérez R, Rubio-Escudero C, Aznarte JL, Ruiz Rejón M, Garrido-Ramos MA (2007) satDNA Analyzer: a computing tool for satellite-DNA evolutionary analysis. Bioinformatics 23(6):767–768

    Article  PubMed  Google Scholar 

  • Navajas-Pérez R, Quesada del Bosque ME, Garrido-Ramos MA (2009a) Effect of location, organization, and repeat copy number in satellite-DNA evolution. Mol Gen Genomics 282:395–406

    Article  Google Scholar 

  • Navajas-Pérez R, Schwarzacher T, Ruiz Rejón M, Garrido-Ramos MA (2009b) Characterization of RUSI, a telomere-associated satellite-DNA, in the genus Rumex (Polygonaceae). Cytogenet Genome Res 124(1):81–89

    Article  PubMed  Google Scholar 

  • Novikov A, Smyshlyaev G, Novikova O (2012) Evolutionary history of LTR retrotransposon chromodomains in plants. Int J Plant Genomics 2012:874743

    Article  PubMed  Google Scholar 

  • Ohno S (1972) So much “junk” DNA in our genome. Brookhaven Symp Biol 23:366–370

    PubMed  CAS  Google Scholar 

  • Orgel LE, Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607

    Article  PubMed  CAS  Google Scholar 

  • Pace NR (2009) Mapping the tree of life: progress and prospects. Microbiol Mol Biol Rev 73(4):565–576

    Article  PubMed  CAS  Google Scholar 

  • Pérez OJ, Dambier D, Ollitrault P, Coppens DG et al (2006) Microsatellite markers in Carica papaya L.: isolation, characterization and transferability to Vasconcellea species. Mol Ecol Notes 6:212–217

    Article  Google Scholar 

  • Petracek ME, Lefebvre PA, Silflow CD, Berman J (1990) Chlamydomonas telomere sequences are A + T rich but contain three consecutive G-C base pairs. Proc Natl Acad Sci USA 87:8222–8226

    Article  PubMed  CAS  Google Scholar 

  • Poole RL (2007) The TAIR database. Methods Mol Biol 406:179–212

    PubMed  CAS  Google Scholar 

  • Price AL, Jones NC, Pevzner PA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21:351–358

    Article  Google Scholar 

  • Ramos HC, Pereira MG, Silva FF, Gonçalves LS, Pinto FO, de Souza Filho GA, Pereira TS (2011) Genetic characterization of papaya plants (Carica papaya L.) derived from the first backcross generation. Genet Mol Res 10(1):393–403

    Article  PubMed  CAS  Google Scholar 

  • Ray DA (2007) SINEs of progress: mobile element applications to molecular ecology. Mol Ecol 16(1):19–33

    Article  PubMed  CAS  Google Scholar 

  • Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53:127–136

    Article  PubMed  CAS  Google Scholar 

  • Riethman H, Ambrosini A, Paul S (2005) Human subtelomere structure and variation. Chromosome Res 13:505–515

    Article  PubMed  CAS  Google Scholar 

  • Robles F, De La Herrán R, Ludwig A, Ruiz Rejón C, Ruiz Rejón M, Garrido-Ramos MA (2004) Evolution of ancient satellite DNAs in sturgeon genomes. Gene 338:133–142

    Article  PubMed  CAS  Google Scholar 

  • Román AC, González-Rico FJ, Moltó E, Hernando H, Neto A, Vicente-García C, Ballestar E, Gómez-Skarmeta JL, Vavrova-Anderson J, White RJ, Montoliu L, Fernández-Salguero PM (2011) Dioxin receptor and SLUG transcription factors regulate the insulator activity of B1 SINE retrotransposons via an RNA polymerase switch. Genome Res 21(3):422–432

    Article  PubMed  Google Scholar 

  • Saini N, Shultz J, Lightfoot DA (2008) Re-annotation of the physical map of Glycine max for polyploid-like regions by BAC end sequence driven whole genome shotgun read assembly. BMC Genomics 9:323

    Article  PubMed  Google Scholar 

  • Santos SC, Ruggiero C, Silva CLSP, Lemos GM (2003) A microsatellite library for Carica papaya L. cv Sunrise Solo. Rev Bras Frutic 25:263–267

    Article  Google Scholar 

  • Schmidt AL, Anderson LM (2006) Repetitive DNA elements as mediators of genomic change in response to environmental cues. Biol Rev Camb Philos Soc 81(4):531–543

    Google Scholar 

  • Shakirov EV, Salzberg SL, Alam M, Shippen DE (2008) Analysis of Carica papaya telomeres and telomere-associated proteins: insights into the evolution of telomere maintenance in Brassicales. Trop Plant Biol 1(3–4):202–215

    Article  PubMed  CAS  Google Scholar 

  • Sola-Campoy PJ, de la Herrán R, Ruiz Rejón C, Navajas-Pérez R (2012) Plant sex-chromosomes evolution. In: Navajas-Pérez R (ed) New insights on plant sex chromosomes, 1st edn. Nova, Hauppauge

    Google Scholar 

  • Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, Leitch AR, Fajkus J (2003) The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J 34:283–291

    Article  PubMed  CAS  Google Scholar 

  • Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452

    Article  PubMed  CAS  Google Scholar 

  • Thomas CA Jr (1971) The genetic organization of chromosomes. Annu Rev Genet 5:237–256

    Article  PubMed  CAS  Google Scholar 

  • Thornburg BG, Gotea V, Makalowski W (2006) Transposable elements as a significant source of transcription regulating signals. Gene 365:104–110

    Article  PubMed  CAS  Google Scholar 

  • Ugarkovic D, Plohl M (2002) Variation in satellite DNA profiles, causes and effects. EMBO J 21:5955–5959

    Article  PubMed  CAS  Google Scholar 

  • Wang ZX, Kurata N, Saji S, Katayose Y, Minobe Y (1995) A chromosome 5-specific repetitive DNA sequence in rice (Oryza sativa L.). Theor Appl Genet 90:907–913

    Article  CAS  Google Scholar 

  • Wang J, Chen C, Na JK, Yu Q, Hou S, Paull RE, Moore PH, Alam M, Ming R (2008) Genome-wide comparative analyses of microsatellites in papaya. Trop Plant Biol 1(3–4):278–292

    Article  CAS  Google Scholar 

  • Wang Y, Wang X, Paterson AH (2012) Genome and gene duplications and gene expression divergence: a view from plants. Ann N Y Acad Sci 1256(1):1–14

    Article  PubMed  Google Scholar 

  • Wang J, Na JK, Yu Q, Gschwend AR, Han J, Zeng F, Aryal R, VanBuren R, Murray JE, Zhang W, Navajas-Pérez R, Feltus FA, Lemke C, Tong EJ, Chen C, Wai CM, Singh R, Wang ML, Min XJ, Alam M, Charlesworth D, Moore PH, Jiang J, Paterson AH, Ming R (2012) Sequencing papaya X and Yh chromosomes reveals molecular basis of incipient sex chromosome evolution. Proc Natl Acad Sci USA. 109(34):13710– 13715

    Google Scholar 

  • Wang J, Na J-K, Ming R (2013) Physical mapping of papaya sex chromosomes. In: Ming R, Moore P (eds) Genetics and genomics of papaya. Springer Science + Business Media, New York

    Google Scholar 

  • Watson JM, Riha K (2010) Comparative biology of telomeres: where plants stand. FEBS Lett 584(17):3752–3759

    Article  PubMed  CAS  Google Scholar 

  • 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(2):177–185

    Article  PubMed  CAS  Google Scholar 

  • Yunis JJ, Yasmineh WG (1971) Heterochromatin, satellite DNA, and cell function. Science 174(4015):1200–1209

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rafael Navajas-Pérez .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Nagarajan, N., Navajas-Pérez, R. (2014). Papaya Repeat Database. 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_13

Download citation

Publish with us

Policies and ethics