Skip to main content
SpringerLink
Log in

Repeat Sequences in the Tomato Genome

  • Chapter
  • First Online:
The Tomato Genome

Part of the book series: Compendium of Plant Genomes ((CPG))

  • 1662 Accesses

Abstract

The sequencing of the tomato genome revealed that, though the moderated size when compared to most of the Solanaceae and other plant species, it comprises more than the 60 % of DNA repeats. This is in contrast with initial estimations assessing that the total genome comprised only about the 10–22 % of repetitive sequences. These preliminary hypotheses were probably biased by the presence of single-copy DNA within the repetitive portion of the genome and by the high sequence divergence of the repeat content. Though the release of the first version of the genome sequences in 2012, the complete view of the repeated regions in tomato at sequence level is still partial, because of difficulties due mainly to DNA repeat sequencing and assembling. However, deeper knowledge on the repeat content of the genome and its distribution was consistently supported by cytogenetics, molecular markers and reassociation kinetics, accompanied by advanced approaches such as Fluorescence In Situ Hybridization (FISH) and more recently Optical Mapping. These techniques helped to clarify many of the principal aspects related to the distribution and the organization of the major repeat classes in tomato, contributing to a consistent overview of this essential part of the genome. The main focus of this chapter is to describe the repeat content of the tomato genome as revealed from the sequencing effort and associated bioinformatics, mainly considering the distribution of highly and moderately repeated DNA sequences. We provide a general overview on plant genome complexity and repeat content, presenting the main repeat categories and their organization. Then we describe the bioinformatics for DNA repeats sequence analysis, focusing on most common approaches for investigations in large genomic sequences, as well as on major repeated sequence collections available to support plant genome annotations. Details on the methods employed to analyze the tomato genome sequences (assembly v. 2.40) published in 2012 will be presented. The description of what is known from tomato concerning the major DNA repeat classes is therefore overviewed highlighting the major results or confirmations obtained thanks to the genome sequencing effort. The discussion is mainly focused on the general description of repeat occurrence in the tomato genome, though questions on the specific role and evolution of these extended regions in tomato and in plant genomes, as well as in other eukaryotes, still remain open.

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

Access this chapter

Log in via an institution
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

  • Ahn S, Anderson JA, Sorrells ME, Tanksley SD (1993) Homoeologous relationships of rice, wheat and maize chromosomes. Mol Gen Genet 241(5–6):483–490

    Article  CAS  PubMed  Google Scholar 

  • Al-Mssallem IS, Hu S, Zhang X, Lin Q, Liu W et al (2013) Genome sequence of the date palm Phoenix dactylifera L. Nat Commun 4:2274

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arabidopsis Genome Initiative T (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815

    Article  Google Scholar 

  • Arens P, Odinot P, Heusden AV, Lindhout P, Vosman B (1995) GATA-and GACA-repeats are not evenly distributed throughout the tomato genome. Genome 38(1):84–90

    Article  CAS  PubMed  Google Scholar 

  • Argout X, Salse J, Aury JM, Guiltinan MJ, Droc G et al (2011) The genome of Theobroma cacao. Nat Genet 43(2):101–108

    Article  CAS  PubMed  Google Scholar 

  • Bao Z, Eddy SR (2002) Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res 12(8):1269–1276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender J (2004) Chromatin-based silencing mechanisms. Curr Opin Plant Biol 7(5):521–526

    Article  CAS  PubMed  Google Scholar 

  • Bennett M, Leitch I (2005) Plant DNA C-values database. Royal Botanic Gardens, Kew

    Google Scholar 

  • Bennett MD, Smith JB (1976) Nuclear dna amounts in angiosperms. Philos Trans R Soc Lond B Biol Sci 274(933):227–274

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL (2000) Comparative sequence analysis of plant nuclear genomes: microcolinearity and its many exceptions. Plant Cell 12(7):1021–1030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennetzen JL, Kellogg EA (1997) Do plants have a one-way ticket to genomic obesity? Plant Cell 9(9):1509–1514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27(2):573–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bermudez-Santana C, Attolini CS, Kirsten T, Engelhardt J, Prohaska SJ et al (2010) Genomic organization of eukaryotic tRNAs. BMC Genomics 11(1):270

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bibillo A, Eickbush TH (2004) End-to-end template jumping by the reverse transcriptase encoded by the R2 retrotransposon. J Biol Chem 279(15):14945–14953

    Article  CAS  PubMed  Google Scholar 

  • Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120(4):1095–1103

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bowen NJ, Jordan IK (2002) Transposable elements and the evolution of eukaryotic complexity. Curr Issues Mol Biol 4(3):65–76

    CAS  PubMed  Google Scholar 

  • Bredemeijer G, Cooke R, Ganal M, Peeters R, Isaac P et al (2002) Construction and testing of a microsatellite database containing more than 500 tomato varieties. Theor Appl Genet 105(6–7):1019–1026

    PubMed  Google Scholar 

  • Broun P, Ganal MW, Tanksley SD (1992) Telomeric arrays display high levels of heritable polymorphism among closely related plant varieties. Proc Natl Acad Sci 89(4):1354–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broun P, Tanksley S (1996) Characterization and genetic mapping of simple repeat sequences in the tomato genome. Mol Gen Genet MGG 250(1):39–49

    Article  CAS  PubMed  Google Scholar 

  • Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9(1):49–56

    Article  CAS  PubMed  Google Scholar 

  • Burge SW, Daub J, Eberhardt R, Tate J, Barquist L et al (2013) Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41:D226–D232

    Article  CAS  PubMed  Google Scholar 

  • Buschiazzo E, Gemmell NJ (2006) The rise, fall and renaissance of microsatellites in eukaryotic genomes. BioEssays 28(10):1040–1050

    Article  CAS  PubMed  Google Scholar 

  • Chang SB, Yang TJ, Datema E, van Vugt J, Vosman B et al (2008) FISH mapping and molecular organization of the major repetitive sequences of tomato. Chromosome Res 16(7):919–933

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371(6494):215–220

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Huang Q, Gao D, Wang J, Lang Y et al (2013) Whole-genome sequencing of Oryza brachyantha reveals mechanisms underlying Oryza genome evolution. Nat Commun 4:1595

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cotton J (2001) Retroviruses from retrotransposons.  Genome Biol 2(2):1

    Google Scholar 

  • Craig NL, Craigie R, Gellert M, Lambowitz AM (2002) Mobile DNA II. ASM Press, Washington, DC

    Book  Google Scholar 

  • Cuadrado A, Jouve N (2007a) The nonrandom distribution of long clusters of all possible classes of trinucleotide repeats in barley chromosomes. Chromosome Res 15(6):711–720

    Article  CAS  PubMed  Google Scholar 

  • Cuadrado A, Jouve N (2007b) Similarities in the chromosomal distribution of AG and AC repeats within and between Drosophila, human and barley chromosomes. Cytogenet Genome Res 119(1–2):91–99

    Article  CAS  PubMed  Google Scholar 

  • Cuadrado A, Schwarzacher T (1998) The chromosomal organization of simple sequence repeats in wheat and rye genomes. Chromosoma 107(8):587–594

    Article  CAS  PubMed  Google Scholar 

  • Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE et al (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16(6):738–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Hont A, Denoeud F, Aury J-M, Baurens F-C, Carreel F et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488(7410):213–217

    Article  PubMed  CAS  Google Scholar 

  • de Jong JH (1998) High resolution FISH reveals the molecular and chromosomal organization of repetitive sequences in tomato. Cytogenet Cell Genet 81:104

    Google Scholar 

  • de Jong JH, Zhong XB, Fransz PF, Wennekes-van Eden J, Jacobsen E et al (2000) High resolution FISH reveals the molecular and chromosomal organisation of repetitive sequences of individual tomato chromosomes. In: Olmo E, Redi C (eds) Chromosomes today. Birkhäuser, Basel, pp 267–275

    Chapter  Google Scholar 

  • Defraia C, Slotkin RK (2014) Analysis of retrotransposon activity in plants. Methods Mol Biol 1112:195–210

    Article  CAS  PubMed  Google Scholar 

  • Denoeud F, Carretero-Paulet L, Dereeper A, Droc G, Guyot R et al (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science 345(6201):1181–1184

    Article  CAS  PubMed  Google Scholar 

  • Devos KM, Gale MD (1993) Extended genetic maps of the homoeologous group 3 chromosomes of wheat, rye and barley. Theor Appl Genet 85(6–7):649–652

    CAS  PubMed  Google Scholar 

  • Devos KM, Gale MD (1997) Comparative genetics in the grasses. Plant Mol Biol 35(1–2):3–15

    Article  CAS  PubMed  Google Scholar 

  • Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12(5):637–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Domenico T, Potenza E, Walsh I, Parra RG, Giollo M et al (2014) RepeatsDB: a database of tandem repeat protein structures. Nucleic Acids Res 42:D352–D357

    Article  PubMed  CAS  Google Scholar 

  • Di Filippo M, Traini A, D’Agostino N, Frusciante L, Chiusano ML (2012) Euchromatic and heterochromatic compositional properties emerging from the analysis of Solanum lycopersicum BAC sequences. Gene 499(1):176–181

    Article  PubMed  CAS  Google Scholar 

  • Eigen M, Lindemann BF, Tietze M, Winkler-Oswatitsch R, Dress A et al (1989) How old is the genetic code? Statistical geometry of tRNA provides an answer. Science 244(4905):673–679

    Article  CAS  PubMed  Google Scholar 

  • Ercolano MR, Sacco A, Ferriello F, D’Alessandro R, Tononi P et al (2014) Patchwork sequencing of tomato San Marzano and Vesuviano varieties highlights genome-wide variations. BMC Genomics 15:138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Flavell RB, Bennett MD, Smith JB, Smith DB (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem Genet 12(4):257–269

    Article  CAS  PubMed  Google Scholar 

  • Ganal MW, Broun P, Tanksley SD (1992) Genetic mapping of tandemly repeated telomeric DNA sequences in tomato (Lycopersicon esculentum). Genomics 14(2):444–448

    Article  CAS  PubMed  Google Scholar 

  • Ganal MW, Lapitan NL, Tanksley SD (1988) A molecular and cytogenetic survey of major repeated DNA sequences in tomato (Lycopersicon esculentum). Mol Gen Genet MGG 213(2–3):262–268

    Article  CAS  Google Scholar 

  • Ganal MW, Lapitan NL, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3(1):87–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia S, Garnatje T, Kovarik A (2012) Plant rDNA database: ribosomal DNA loci information goes online. Chromosoma 121(4):389–394

    Article  CAS  PubMed  Google Scholar 

  • Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B et al (1991) RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor Appl Genet 83(1):49–57

    Article  CAS  PubMed  Google Scholar 

  • Gelfand Y, Rodriguez A, Benson G (2007) TRDB—the tandem repeats database. Nucleic Acids Res 35(suppl 1):D80–D87

    Article  CAS  PubMed  Google Scholar 

  • Gong Z, Wu Y, Koblížková A, Torres GA, Wang K et al (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell Online 24(9):3559–3574

    Article  CAS  Google Scholar 

  • Grandillo S, Tanksley S (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor Appl Genet 92(8):935–951

    Article  CAS  PubMed  Google Scholar 

  • Greilhuber J, Doležel J, Lysák MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Ann Bot 95(1):255–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grover CE, Wendel JF (2010) Recent insights into mechanisms of genome size change in plants. J Bot 2010:8

    Google Scholar 

  • Hall IM, Shankaranarayana GD, Noma K-I, Ayoub N, Cohen A et al (2002) Establishment and maintenance of a heterochromatin domain. Science 297(5590):2232–2237

    Article  CAS  PubMed  Google Scholar 

  • Hawkins JS, Proulx SR, Rapp RA, Wendel JF (2009) Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc Natl Acad Sci U S A 106(42):17811–17816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He L, Liu J, Torres GA, Zhang H, Jiang J et al (2013) Interstitial telomeric repeats are enriched in the centromeres of chromosomes in Solanum species. Chromosome Res 21(1):5–13

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293(5532):1098–1102

    Article  CAS  PubMed  Google Scholar 

  • Hertel J, Hofacker IL, Stadler PF (2008) SnoReport: computational identification of snoRNAs with unknown targets. Bioinformatics 24(2):158–164

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison JS (2000) Comparative genome organization in plants: from sequence and markers to chromatin and chromosomes. Plant Cell 12(5):617–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heslop-Harrison JS, Brandes A, Schwarzacher T (2003) Tandemly repeated DNA sequences and centromeric chromosomal regions of Arabidopsis species. Chromosome Res 11(3):241–253

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa H, Shirasawa K, Miyatake K, Nunome T, Negoro S et al (2014) Draft genome sequence of eggplant (Solanum melongena L.): the representative solanum species indigenous to the old world. DNA Res 21(6):649–660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houben A, Schubert I (2003) DNA and proteins of plant centromeres. Curr Opin Plant Biol 6(6):554–560

    Article  CAS  PubMed  Google Scholar 

  • Hu TT, Pattyn P, Bakker EG, Cao J, Cheng JF et al (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43(5):476–481

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang S, Li R, Zhang Z, Li L, Gu X et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41(12):1275–1281

    Article  CAS  PubMed  Google Scholar 

  • International Barley Genome Sequencing, Mayer CKF, Waugh R, Brown JW, Schulman A et al (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491(7426):711–716

    Google Scholar 

  • International Rice Genome Sequencing, P (2005) The map-based sequence of the rice genome. Nature 436(7052):793–800

    Article  CAS  Google Scholar 

  • IWGSC (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345(6194):1251788

    Article  CAS  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467

    Article  CAS  PubMed  Google Scholar 

  • Jarne P, Lagoda PJ (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11(10):424–429

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR et al (2012) A genome triplication associated with early diversification of the core eudicots. Genome Biol 13(1):R3

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345):97–100

    Article  CAS  PubMed  Google Scholar 

  • Jo S-H, Koo D-H, Kim J, Hur C-G, Lee S et al (2009) Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Biol 9(1):42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jurka J (1997) Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci 94(5):1872–1877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O et al (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110(1–4):462–467

    Article  CAS  PubMed  Google Scholar 

  • Kalitsis P, Choo KH (2012) The evolutionary life cycle of the resilient centromere. Chromosoma 121(4):327–340

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Park M, Yeom SI, Kim YM, Lee JM et al (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46(3):270–278

    Article  CAS  PubMed  Google Scholar 

  • King DG, Soller M, Kashi Y (1997) Evolutionary tuning knobs. Endeavour 21(1):36–40

    Article  Google Scholar 

  • Knapp S et al (2004) Solanaceae—a model for linking genomics with biodiversity. Comp Funct Genomics 5(3):285–291

    Google Scholar 

  • Knight CA, Molinari NA, Petrov DA (2005) The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot 95(1):177–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in repbase: repbasesubmitter and censor. BMC Bioinform 7:474

    Article  CAS  Google Scholar 

  • Kolpakov R (2003) mreps: efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res 31(13):3672–3678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kramerov DA, Vassetzky NS (2005) Short retroposons in eukaryotic genomes. Int Rev Cytol 247:165–221

    Article  CAS  PubMed  Google Scholar 

  • Kruglyak S, Durrett RT, Schug MD, Aquadro CF (1998) Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. Proc Natl Acad Sci USA 95(18):10774–10778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532

    Article  CAS  PubMed  Google Scholar 

  • Lapitan NL, Ganal MW, Tanksley SD (1989) Somatic chromosome karyotype of tomato based on in situ hybridization of the TGRI satellite repeat. Genome 32(6):992–998

    Article  Google Scholar 

  • Lapitan NLV, Ganal MW, Tanksley SD (1991) Organization of the 5S ribosomal RNA genes in the genome of tomato. Genome 34(4):509–514

    Article  CAS  Google Scholar 

  • Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32(1):11–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee S-I, Kim N-S (2014) Transposable elements and genome size variations in plants. Genom Inform 12(3):87–97

    Article  Google Scholar 

  • Ling HQ, Zhao S, Liu D, Wang J, Sun H et al (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496(7443):87–90

    Article  CAS  PubMed  Google Scholar 

  • Lippman Z, Gendrel A-V, Black M, Vaughn MW, Dedhia N et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430(6998):471–476

    Article  CAS  PubMed  Google Scholar 

  • Liu Z-W, Biyashev R, Maroof MS (1996) Development of simple sequence repeat DNA markers and their integration into a barley linkage map. Theor Appl Genet 93(5–6):869–876

    Article  CAS  PubMed  Google Scholar 

  • Livingstone KD, Lackney VK, Blauth JR, Van Wijk R, Jahn MK (1999) Genome mapping in Capsicum and the evolution of genome structure in the Solanaceae. Genetics 152(3):1183–1202

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lysak MA, Koch MA, Pecinka A, Schubert I (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res 15(4):516–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macas J, Meszaros T, Nouzova M (2002) PlantSat: a specialized database for plant satellite repeats. Bioinformatics 18(1):28–35

    Article  CAS  PubMed  Google Scholar 

  • Majerová E, Mandáková T, Vu GTH, Fajkus J, Lysak MA et al (2014) Chromatin features of plant telomeric sequences at terminal vs. internal positions. Front Plant Sci 5:593

    Article  PubMed  PubMed Central  Google Scholar 

  • Maluszynska J, Heslop-Harrison J (1991) Localization of tandemly repeated DMA sequences in Arabidopsis thaliana. Plant J 1(2):159–166

    Article  Google Scholar 

  • Marshall OJ et al (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82(2):261–282

    Google Scholar 

  • Martienssen RA, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293(5532):1070–1074

    Article  CAS  PubMed  Google Scholar 

  • Martin GB, Ganal MW, Tanksley SD (1992) Construction of a yeast artificial chromosome library of tomato and identification of cloned segments linked to two disease resistance loci. Mol Gen Genet MGG 233(1–2):25–32

    Article  CAS  PubMed  Google Scholar 

  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118(1):9–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Zapater JM, Estelle MA, Somerville CR (1986) A highly repeated DNA sequence in Arabidopsis thaliana. Mol Gen Genet MGG 204(3):417–423

    Article  CAS  Google Scholar 

  • Mason JM, Biessmann H (1995) The unusual telomeres of Drosophila. Trends Genet 11(2):58–62

    Article  CAS  PubMed  Google Scholar 

  • Maughan P, Maroof MS, Buss G (1995) Microsatellite and amplified sequence length polymorphisms in cultivated and wild soybean. Genome 38(4):715–723

    Article  CAS  PubMed  Google Scholar 

  • McCarthy EM, McDonald JF (2003) LTR_STRUC: a novel search and identification program for LTR retrotransposons. Bioinformatics 19(3):362–367

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1953) Induction of instability at selected loci in maize. Genetics 38(6):579–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • McCouch SR, Chen X, Panaud O, Temnykh S, Xu Y et al (1997) Microsatellite marker development, mapping and applications in rice genetics and breeding. Plant Mol Biol 35(1–2):89–99

    Article  CAS  PubMed  Google Scholar 

  • Melters DP, Bradnam KR, Young HA, Telis N, May MR et al (2013) Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol 14(1):R10

    Article  PubMed  PubMed Central  Google Scholar 

  • Meraldi P, McAinsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7(3):R23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meyne J, Baker RJ, Hobart HH, Hsu T, Ryder OA et al (1990) Distribution of non-telomeric sites of the (TTAGGG) n telomeric sequence in vertebrate chromosomes. Chromosoma 99(1):3–10

    Article  CAS  PubMed  Google Scholar 

  • Michael TP (2014) Plant genome size variation: bloating and purging DNA. Brief Funct Genomics 13(4):308–317

    Article  CAS  PubMed  Google Scholar 

  • Michaud M, Cognat V, Duchêne A-M, Maréchal-Drouard L (2011) A global picture of tRNA genes in plant genomes. Plant J 66(1):80–93

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW, Paran I, Kesseli R (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci 88(21):9828–9832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milbourne D, Meyer R, Bradshaw JE, Baird E, Bonar N et al (1997) Comparison of PCR-based marker systems for the analysis of genetic relationships in cultivated potato. Mol Breed 3(2):127–136

    Article  CAS  Google Scholar 

  • Minajigi A, Francklyn CS (2010) Aminoacyl transfer rate dictates choice of editing pathway in threonyl-tRNA synthetase. J Biol Chem 285(31):23810–23817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452(7190):991–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ming R, VanBuren R, Liu Y, Yang M, Han Y et al (2013) Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol 14(5):R41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mueller LA, Lankhorst RK, Tanksley SD, Giovannoni JJ, White R et al (2009) A snapshot of the emerging tomato genome sequence. Plant Gen 2(1):78–92

    Article  CAS  Google Scholar 

  • Nagaki K, Murata M (2005) Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res 13(2):195–203

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Shibata F, Kanatani A, Kashihara K, Murata M (2012) Isolation of centromeric-tandem repetitive DNA sequences by chromatin affinity purification using a HaloTag7-fused centromere-specific histone H3 in tobacco. Plant Cell Rep 31(4):771–779

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Shibata F, Suzuki G, Kanatani A, Ozaki S et al (2011) Coexistence of NtCENH3 and two retrotransposons in tobacco centromeres. Chromosome Res 19(5):591–605

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Song J, Stupar RM, Parokonny AS, Yuan Q et al (2003) Molecular and cytological analyses of large tracks of centromeric DNA reveal the structure and evolutionary dynamics of maize centromeres. Genetics 163(2):759–770

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nawrocki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25(10):1335–1337

    Google Scholar 

  • Nowacki M, Higgins BP, Maquilan GM, Swart EC, Doak TG et al (2009) A functional role for transposases in a large eukaryotic genome. Science 324(5929):935–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • NSF (1990) Document 90–80. A long-range plan for the multinational coordinated Arabidopsis thaliana genome research project. National Science Foundation, Washington, DC

    Google Scholar 

  • Nussbaumer T, Martis MM, Roessner SK, Pfeifer M, Bader KC et al (2013) MIPS PlantsDB: a database framework for comparative plant genome research. Nucleic Acids Res 41:D1144–D1151

    Article  CAS  PubMed  Google Scholar 

  • Ouyang S, Buell CR (2004) The TIGR plant repeat databases: a collective resource for the identification of repetitive sequences in plants. Nucleic Acids Res 32:D360–D363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park M, Jo S, Kwon J-K, Park J, Ahn JH et al (2011) Comparative analysis of pepper and tomato reveals euchromatin expansion of pepper genome caused by differential accumulation of Ty3/Gypsy-like elements. BMC Genomics 12(1):85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556

    Article  CAS  PubMed  Google Scholar 

  • Peters SA, Datema E, Szinay D, van Staveren MJ, Schijlen EG et al (2009) Solanum lycopersicum cv. Heinz 1706 chromosome 6: distribution and abundance of genes and retrotransposable elements. Plant J 58(5):857–869

    Article  CAS  PubMed  Google Scholar 

  • Peterson DG, Pearson WR, Stack SM (1998) Characterization of the tomato (Lycopersicon esculentum) genome using in vitro and in situ DNA reassociation. Genome 41(3):346–356

    Article  CAS  Google Scholar 

  • Peterson DG, Stack SM, Price HJ, Johnston JS (1996) DNA content of heterochromatin and euchromatin in tomato (Lycopersicon esculentum) pachytene chromosomes. Genome 39(1):77–82

    Article  CAS  PubMed  Google Scholar 

  • Phizicky EM, Hopper AK (2010) tRNA biology charges to the front. Genes Dev 24(17):1832–1860

    Article  PubMed  PubMed Central  Google Scholar 

  • Piegu B, Guyot R, Picault N, Roulin A, Saniyal A et al (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16(10):1262–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podlevsky JD, Bley CJ, Omana RV, Qi X, Chen JJL (2008) The telomerase database. Nucleic Acids Res 36:D339–D343

    Article  CAS  PubMed  Google Scholar 

  • Potato Genome Sequencing Consortium, T (2011) Genome sequence and analysis of the tuber crop potato. Nature 475(7355):189–195

    Article  CAS  Google Scholar 

  • Presting GG, Frary A, Pillen K, Tanksley SD (1996) Telomere-homologous sequences occur near the centromeres of many tomato chromosomes. Mol Gen Genet MGG 251(5):526–531

    Article  CAS  PubMed  Google Scholar 

  • Price AL, Jones NC, Pevzner PA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21(Suppl 1):i351–i358

    Article  CAS  PubMed  Google Scholar 

  • Prince JP, Pochard E, Tanksley SD (1993) Construction of a molecular linkage map of pepper and a comparison of synteny with tomato. Genome 36(3):404–417

    Article  CAS  PubMed  Google Scholar 

  • Qin C, Yu C, Shen Y, Fang X, Chen L et al (2014) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc Natl Acad Sci USA 111(14):5135–5140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293(5532):1089–1093

    Article  CAS  PubMed  Google Scholar 

  • Richard G-F, Kerrest A, Dujon B (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol Mol Biol Rev 72(4):686–727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity 108(1):59–67

    Article  CAS  PubMed  Google Scholar 

  • Sakowicz T, Gadzalski M, Pszczółkowski W (2009) Short interspersed elements (SINEs) in plant genomes. Adv Cell Biol 1:1–12

    Article  Google Scholar 

  • Sangiovanni M, Vigilante A, Chiusano ML (2013) Exploiting a reference genome in terms of duplications: the network of paralogs and single copy genes in Arabidopsis thaliana. Biol (Basel) 2(4):1465–1487

    Google Scholar 

  • Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T et al (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15(4):227–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33:W686–W689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt T, Heslop-Harrison J (1998) Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends Plant Sci 3(5):195–199

    Article  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326(5956):1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Schweizer G, Ganal M, Ninnemann H, Hemleben V (1988) Species-specific DNA sequences for identification of somatic hybrids between Lycopersicon esculentum and Solanum acaule. Theor Appl Genet 75(5):679–684

    Article  CAS  Google Scholar 

  • Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109(1–3):15–26

    Article  CAS  PubMed  Google Scholar 

  • Sharma SK, Bolser D, de Boer J, Sønderkær M, Amoros W et al (2013) Construction of reference chromosome-scale pseudomolecules for potato: integrating the potato genome with genetic and physical maps. G3 Genes Genomes Genet 3(11):2031–2047

    Google Scholar 

  • Shearer LA, Anderson LK, de Jong H, Smit S, Goicoechea JL, et al (2014) Fluorescence in situ hybridization and optical mapping to correct scaffold arrangement in the tomato genome. G3 Genes Genomes Genet 4(8):1395–1405

    Google Scholar 

  • Sherman JD, Stack SM (1995) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 141(2):683–708

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43(2):109–116

    Article  CAS  PubMed  Google Scholar 

  • Sierro N, Battey JN, Ouadi S, Bakaher N, Bovet L et al (2014) The tobacco genome sequence and its comparison with those of tomato and potato. Nat Commun 5:3833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smit AFA, Hubley R,  Green P (1996) RepeatMasker Open-3.0. http://www.repeatmasker.org

  • Smulders MJM, Bredemeijer G, Rus-Kortekaas W, Arens P, Vosman B (1997) Use of short microsatellites from database sequences to generate polymorphisms among Lycopersicon esculentum cultivars and accessions of other Lycopersicon species. Theor Appl Genet 94(2):264–272

    Article  CAS  Google Scholar 

  • Smyth DR (1991) Dispersed repeats in plant genomes. Chromosoma 100(6):355–359

    Article  Google Scholar 

  • Suresh BV, Roy R, Sahu K, Misra G, Chattopadhyay D (2014) Tomato genomic resources database: an integrated repository of useful tomato genomic information for basic and applied research. PLoS One 9(1):e86387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swift H (1950) The constancy of desoxyribose nucleic acid in plant nuclei. Proc Natl Acad Sci USA 36(11):643–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szinay D, Chang SB, Khrustaleva L, Peters S, Schijlen E et al (2008) High-resolution chromosome mapping of BACs using multi-colour FISH and pooled-BAC FISH as a backbone for sequencing tomato chromosome 6. Plant J 56(4):627–637

    Article  CAS  PubMed  Google Scholar 

  • Tang H, Bowers JE, Wang X, Ming R, Alam M et al (2008a) Synteny and collinearity in plant genomes. Science 320(5875):486–488

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Szinay D, Lang C, Ramanna MS, van der Vossen EA et al (2008b) Cross-species bacterial artificial chromosome-fluorescence in situ hybridization painting of the tomato and potato chromosome 6 reveals undescribed chromosomal rearrangements. Genetics 180(3):1319–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanksley SD, Bernatzky R, Lapitan NL, Prince JP (1988) Conservation of gene repertoire but not gene order in pepper and tomato. Proc Natl Acad Sci USA 85(17):6419–6423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tautz D, Schlotterer (1994) Simple sequences. Curr Opin Genet Dev 4(6):832–837

    Article  CAS  PubMed  Google Scholar 

  • Tek AL, Jiang J (2004) The centromeric regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequence. Chromosoma 113(2):77–83

    Article  CAS  PubMed  Google Scholar 

  • Tomato Genome Consortium, T (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485(7400):635–641

    Article  CAS  Google Scholar 

  • Traini A, Iorizzo M, Mann H, Bradeen JM, Carputo D, Frusciante L, Chiusano ML (2013) Genome microscale heterogeneity among wild potatoes revealed by diversity arrays technology marker sequences. Int Journal Genomics 2013:9

    Google Scholar 

  • Vallejos CE, Tanksley SD, Bernatzky R (1986) Localization in the tomato genome of DNA restriction fragments containing sequences homologous to the rRNA (45s), the major chlorophyll a/b binding polypeptide and the ribulose bisphosphate carboxylase genes. Genetics 112(1):93–105

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vaughan H, Heslop-Harrison J, Hewitt G (1999) The localization of mitochondrial sequences to chromosomal DNA in orthopterans. Genome 42(5):874–880

    Article  CAS  Google Scholar 

  • Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI et al (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297(5588):1833–1837

    Article  CAS  PubMed  Google Scholar 

  • von Sternberg R (2002) On the roles of repetitive DNA elements in the context of a unified genomic-epigenetic system. Ann NY Acad Sci 981:154–188

    Article  Google Scholar 

  • Vosman B, Arens P, Rus-Kortekaas W, Smulders M (1992) Identification of highly polymorphic DNA regions in tomato. Theor Appl Genet 85(2–3):239–244

    CAS  PubMed  Google Scholar 

  • Wang L, Zeng Z, Zhang W, Jiang J (2014) Three potato centromeres are associated with distinct haplotypes with or without megabase-sized satellite repeat arrays. Genetics 196(2):397–401

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang H, Wang J, Sun R, Wu J et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43(10):1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Diehl A, Wu F, Vrebalov J, Giovannoni J et al (2008) Sequencing and comparative analysis of a conserved syntenic segment in the Solanaceae. Genetics 180(1):391–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Tang X, Cheng Z, Mueller L, Giovannoni J et al (2006) Euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172(4):2529–2540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wikstrom N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc Biol Sci 268(1482):2211–2220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiley G, Macmil S, Qu C, Wang P, Xing Y et al (2009) Methods for generating shotgun and mixed shotgun/paired-end libraries for the 454 DNA sequencer. Curr Prot Hum Genet 18.11:11-18–11-21

    Google Scholar 

  • Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286(5439):481–486

    Article  CAS  PubMed  Google Scholar 

  • Wu F, Eannetta NT, Xu Y, Durrett R, Mazourek M et al (2009) A COSII genetic map of the pepper genome provides a detailed picture of synteny with tomato and new insights into recent chromosome evolution in the genus Capsicum. Theor Appl Genet 118(7):1279–1293

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Earle ED (1996a) Direct FISH of 5S rDNA on tomato pachytene chromosomes places the gene at the heterochromatic knob immediately adjacent to the centromere of chromosome 1. Genome 39(1):216–221

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Earle ED (1996b) High resolution physical mapping of 45S (5.8S, 18S and 25S) rDNA gene loci in the tomato genome using a combination of karyotyping and FISH of pachytene chromosomes. Chromosoma 104(8):545–550

    Article  CAS  PubMed  Google Scholar 

  • Yan H, Ito H, Nobuta K, Ouyang S, Jin W et al (2006) Genomic and genetic characterization of rice Cen3 reveals extensive transcription and evolutionary implications of a complex centromere. Plant Cell 18(9):2123–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasuhara JC, Wakimoto BT (2006) Oxymoron no more: the expanding world of heterochromatic genes. Trends Genet 22(6):330–338

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zamir D, Tanksley S (1988) Tomato genome is comprised largely of fast-evolving, low copy-number sequences. Mol Gen Genet MGG 213(2–3):254–261

    Article  CAS  Google Scholar 

  • Zhang H, Koblizkova A, Wang K, Gong Z, Oliveira L et al (2014) Boom-bust turnovers of megabase-sized centromeric DNA in solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26(4):1436–1447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong CX, Marshall JB, Topp C, Mroczek R, Kato A et al (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell Online 14(11):2825–2836

    Article  CAS  Google Scholar 

  • Zhong XB, Fransz PF, Wennekes-van Eden J, Kammen AV, Zabel P et al (1998) FISH studies reveal the molecular and chromosomal organization of individual telomere domains in tomato. Plant J 13(4):507–517

    Article  CAS  PubMed  Google Scholar 

  • Zhu W, Ouyang S, Iovene M, O’Brien K, Vuong H et al (2008) Analysis of 90 Mb of the potato genome reveals conservation of gene structures and order with tomato but divergence in repetitive sequence composition. BMC Genomics 9:286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agraria, University Federico II of Naples, Naples, Italy

    Maria Luisa Chiusano & Chiara Colantuono

Authors
  1. Maria Luisa Chiusano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chiara Colantuono
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Luisa Chiusano .

Editor information

Editors and Affiliations

  1. GAFL, INRA, Montfavet Cedex, France

    Mathilde Causse

  2. Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, New York, USA

    Jim Giovannoni

  3. INRA-INP Toulouse, Castanet Tolosan, France

    Mondher Bouzayen

  4. INRA-INP Toulouse, Castanet Tolosan, France

    Mohamed Zouine

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Chiusano, M.L., Colantuono, C. (2016). Repeat Sequences in the Tomato Genome. In: Causse, M., Giovannoni, J., Bouzayen, M., Zouine, M. (eds) The Tomato Genome. Compendium of Plant Genomes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-53389-5_10

Download citation

Publish with us

Policies and ethics

Search

Navigation