, Volume 249, Issue 5, pp 1405–1415 | Cite as

Heterochromatin evolution in Arachis investigated through genome-wide analysis of repetitive DNA

  • Sergio S. SamolukEmail author
  • Laura M. I. Chalup
  • Carolina Chavarro
  • Germán Robledo
  • David J. Bertioli
  • Scott A. Jackson
  • Guillermo Seijo
Original Article


Main conclusion

The most conspicuous difference among chromosomes and genomes in Arachis species, the patterns of heterochromatin, was mainly modeled by differential amplification of different members of one superfamily of satellite DNAs.

Divergence in repetitive DNA is a primary driving force for genome and chromosome evolution. Section Arachis is karyotypically diverse and has six different genomes. Arachis glandulifera (D genome) has the most asymmetric karyotype and the highest reproductive isolation compared to the well-known A and B genome species. These features make A. glandulifera an interesting model species for studying the main repetitive components that accompanied the genome and chromosome diversification in the section. Here, we performed a genome-wide analysis of repetitive sequences in A. glandulifera and investigated the chromosome distribution of the identified satellite DNA sequences (satDNAs). LTR retroelements, mainly the Ty3-gypsy families “Fidel/Feral” and “Pipoka/Pipa”, were the most represented. Comparative analyses with the A and B genomes showed that many of the previously described transposable elements (TEs) were differently represented in the D genome, and that this variation accompanied changes in DNA content. In addition, four major satDNAs were characterized. Agla_CL8sat was the major component of pericentromeric heterochromatin, while Agla_CL39sat, Agla_CL69sat, and Agla_CL122sat were found in heterochromatic and/or euchromatic regions. Even though Agla_CL8sat belong to a different family than that of the major satDNA (ATR-2) found in the heterochromatin of the A, K, and F genomes, both satDNAs are members of the same superfamily. This finding suggests that closely related satDNAs of an ancestral library were differentially amplified leading to the major changes in the heterochromatin patterns that accompanied the karyotype and genome differentiation in Arachis.


Repetitive sequences Chromosome structure Genome evolution Satellite DNA Arachis species 



Satellite DNA


Fluorescent in situ hybridization


Ribosomal DNA


Long terminal repeat


Next-generation sequencing


Transposable elements



The authors gratefully acknowledge the financial support from the Agencia Nacional de Promoción Científica y Tecnológica, Argentina (Projects PICT 2007-01875 and PICT 2015-2804); Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina (Project PIP 11220120100192) under the “Exploring the Biological and Genetic Diversity of Arachis Germplasm” program.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2019_3096_MOESM1_ESM.docx (2.4 mb)
Supplementary material 1 (DOCX 2438 kb)


  1. Barghini E, Natali L, Cossu RM, Giordani T, Pindo M, Cattonaro F, Scalabrin S, Velasco R, Morgante M, Cavallini A (2014) The peculiar landscape of repetitive sequences in the olive (Olea europaea L.) genome. Genome Biol Evol 6:776–791CrossRefPubMedPubMedCentralGoogle Scholar
  2. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bertioli DJ, Vidigal B, Nielen S, Ratnaparkhe MB, Lee TH, Leal-Bertioli SCM, Kim C, Guimarães PM, Seijo G, Schwarzacher T, Paterson AH, Heslop-Harrison P, Araujo ACG (2013) The repetitive component of the A genome of peanut (Arachis hypogaea) and its role in remodelling intergenic sequence space since its evolutionary divergence from the B genome. Ann Bot 112:545–559CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bertioli DJ, Cannon SB, Froenicke L et al (2016) The genome sequences of Arachis duranensis and Arachis ipaënsis, the diploid ancestors of cultivated peanut. Nat Genet 47:438–446CrossRefGoogle Scholar
  5. Biemont C, Vieira C (2006) Genetics: junk DNA as an evolutionary force. Nature 443:521–524CrossRefPubMedGoogle Scholar
  6. Biscotti MA, Canapa A, Forconi M, Olmo E, Barucca M (2015) Transcription of tandemly repetitive DNA: functional roles. Chromosome Res 23:463–477CrossRefPubMedGoogle Scholar
  7. Buchmann JP, Matsumoto T, Stein N, Keller B, Wicker T (2012) Inter-species sequence comparison of Brachypodium reveals how transposon activity corrodes genome colinearity. Plant J 71:550–563CrossRefPubMedGoogle Scholar
  8. Burow MD, Simpson CE, Starr JL, Paterson AH (2001) Transmission genetics of chromatin from a synthetic amphidiploid to cultivated peanut (Arachis hypogaea L.): broadening the gene pool of a monophyletic polyploid species. Genetics 159:823–837PubMedPubMedCentralGoogle Scholar
  9. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220CrossRefGoogle Scholar
  10. Chen X, Li H, Pandey MK et al (2016) Draft genome of the peanut A-genome progenitor (Arachis duranensis) provides insights into geocarpy, oil biosynthesis, and allergens. Proc Natl Acad Sci USA 113:6785–6790CrossRefPubMedGoogle Scholar
  11. Cloix C, Tutois S, Mathieu O, Cuvillier C, Espagnol MC, Picard G, Tourmente S (2000) Analysis of 5S rDNA arrays in Arabidopsis thaliana: physical mapping and chromosome-specific polymorphisms. Genome Res 10:679–690CrossRefPubMedPubMedCentralGoogle Scholar
  12. Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dhillon SS, Rake AV, Miksche JP (1980) Reassociation kinetics and cytophotometric characterization of peanut (Arachis hypogaea L.). DNA Plant Physiol 65:1121–1127CrossRefPubMedGoogle Scholar
  14. do Nascimento EFMB, Vidigal dos Santos B, Marques LOC, Guimarães PM, Brasileiro ACM, Leal-Bertioli SCM, Bertioli DJ, Araujo ACG (2018) The genome structure of Arachis hypogaea (Linnaeus, 1753) and an induced Arachis allotetraploid revealed by molecular cytogenetics. Comparative Cyt 12:111CrossRefGoogle Scholar
  15. Fernandez A, Krapovickas A (1994) Cromosomas y evolución en Arachis (Leguminosae). Bonplandia 8:187–220Google Scholar
  16. Ferree PM, Prasad S (2012) How can satellite DNA divergence cause reproductive isolation? Let us count the chromosomal ways. Genet Res Int. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fry K, Salser W (1977) Nucleotide sequences of HS-Α satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12:1069–1084CrossRefPubMedGoogle Scholar
  18. Gowda MVC, Bhat RS, Motagi BN, Sujay V, Kumari V, Bhat S (2010) Association of high-frequency origin of late leaf spot resistant mutants with AhMITE1 transposition in peanut. Plant Breed 129:567–569Google Scholar
  19. Gowda MVC, Bhat RS, Sujay V, Kusuma P, Bhat S, Varshney RK (2011) Characterization of AhMITE1 transposition and its association with the mutational and evolutionary origin of botanical types in peanut (Arachis spp.). Plant Syst Evol 291:153–158CrossRefGoogle Scholar
  20. Guerra M (2000) Patterns of heterochromatin distribution in plant chromosomes. Genet Mol Biol 23:1029–1041CrossRefGoogle Scholar
  21. Heitkam T, Petrasch S, Zakrzewski F, Kögler A, Wenke T, Wanke S, Schmidt T (2015) Next-generation sequencing reveals differentially amplified tandem repeats as a major genome component of Northern Europe’s oldest Camellia japonica. Chromosome Res 23:791–806CrossRefPubMedGoogle Scholar
  22. Hemleben V, Kovarik A, Torres-Ruiz RA, Volkov RA, Beridze T (2007) Plant highly repeated satellite DNA: molecular evolution, distribution and use for identification of hybrids. Syst Biodivers 5:277–289CrossRefGoogle Scholar
  23. Heslop-Harrison JS, Schwarzacher T (2011) Organisation of the plant genome in chromosomes. Plant J 66:18–33CrossRefPubMedGoogle Scholar
  24. Iwata-Otsubo A, Radke B, Findley S, Abernathy B, Vallejos CE, Jackson SA (2016) Fluorescence in situ hybridization (FISH)-based karyotyping reveals rapid evolution of centromeric and subtelomeric repeats in common bean (Phaseolus vulgaris) and relatives. G3 Genes Genom Genet 6:1013–1022Google Scholar
  25. Jo SH, Koo DH, Kim JF, Hur CG, Lee S, Yang TJ, Kwon SY, Choi D (2009) Evolution of ribosomal DNA-derived satellite repeat in tomato genome. BMC Plant Biol 9:42CrossRefPubMedPubMedCentralGoogle Scholar
  26. Jurka J, Kohany O, Pavlicek A et al (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467CrossRefPubMedGoogle Scholar
  27. Kidwell MG, Lisch DR (2000) Transposable elements and host genome evolution. Trends Ecol Evol 15:95–99CrossRefPubMedGoogle Scholar
  28. Kirov I, Divashuk M, Van Laere K, Soloviev A, Khrustaleva L (2014) An easy “SteamDrop” method for high quality plant chromosome preparation. Mol Cytogenet 7:21CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kirov IV, Kiseleva AV, Van Laere K, Van Roy N, Khrustaleva LI (2017) Tandem repeats of Allium fistulosum associated with major chromosomal landmarks. Mol Genet Genomics 292:453–464CrossRefPubMedGoogle Scholar
  30. Kloc A, Martienssen R (2008) RNAi, heterochromatin and the cell cycle. Trends Genet 24:511–517CrossRefPubMedGoogle Scholar
  31. Krapovickas A, Gregory W (1994) Taxonomía del género Arachis (Leguminosae). Bonplandia 8:11–86Google Scholar
  32. Lu Q, Li H, Hong Y et al (2018) Genome sequencing and analysis of the peanut B-genome progenitor (Arachis ipaensis). Front Plant Sci 9:604CrossRefPubMedPubMedCentralGoogle Scholar
  33. Macas J, Navratilova A, Meszaros T (2003) Sequence subfamilies of satellite repeats related to rDNA intergenic spacer are differentially amplified on Vicia sativa chromosomes. Chromosoma 112:152–158CrossRefPubMedGoogle Scholar
  34. Macas J, Novák P, Pellicer J et al (2015) In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe Fabeae. PLoS One 10:e0143424CrossRefPubMedPubMedCentralGoogle Scholar
  35. Mallikarjuna N (2002) Gene introgression from Arachis glabrata into A. hypogaea, A. duranensis and A. diogoi. Euphytica 124:99–105CrossRefGoogle Scholar
  36. Mallikarjuna N, Pande S, Jadhav, Sastri DC, Rao JN (2004) Introgression of disease resistance genes from Arachis kempff-mercadoi into cultivated groundnut. Plant Breed 123:573–576CrossRefGoogle Scholar
  37. Marchler-Bauer A, Lu S, Anderson J (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229CrossRefPubMedGoogle Scholar
  38. Martienssen RA (2003) Maintenance of heterochromatin by RNA interference of tandem repeats. Nat Genet 35:213–214CrossRefPubMedGoogle Scholar
  39. Mehrotra S, Goyal V (2014) Repetitive sequences in plant nuclear DNA: types, distribution, evolution and function. Genom Proteom Bioinform 12:164–171CrossRefGoogle Scholar
  40. Melters D, Bradnam K, Young H et al (2013) Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol 14(1):R10CrossRefPubMedPubMedCentralGoogle Scholar
  41. Moretzsohn MC, Gouvea EG, Inglis PW, Leal-Bertioli SCM, Valls JFM, Bertioli DJ (2014) A study of the relationships of cultivated peanut (Arachis hypogaea) and its most closely related wild species using intron sequences and microsatellite markers. Ann Bot 111:113–126CrossRefGoogle Scholar
  42. Naito K, Zhang F, Tsukiyama T et al (2009) Unexpected consequences of sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134CrossRefPubMedGoogle Scholar
  43. Nielen S, Campos- Fonseca F, Leal- Bertioli S, Guimaraes P, Seijo G, Town C, Arrial R, Bertioli D (2010) FIDEL—a retrovirus-like retrotransposon and its distinct evolutionary histories in the A- and B-genome components of cultivated peanut. Chrom Res 18:227–246CrossRefPubMedGoogle Scholar
  44. Nielen S, Vidigal B, Leal-Bertioli S, Ratnaparkhe M, Paterson A, Garsmeur O, D’Hont A, Guimarães P, Bertioli D (2012) Matita, a new retroelement from peanut: characterization and evolutionary context in the light of the Arachis A-B genome divergence. Mol Genet Genom 287:21–38CrossRefGoogle Scholar
  45. Novak P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11:378CrossRefGoogle Scholar
  46. Novak P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793CrossRefPubMedGoogle Scholar
  47. Patel M, Jung S, Moore K, Powell G, Ainsworth C, Abbott A (2004) High-oleate peanut mutants result from a MITE insertion into the FAD2 gene. Theor Appl Genet 108:1492–1502CrossRefPubMedGoogle Scholar
  48. Pezer Z, Brajkovic J, Feliciello I, Ugarkovic D (2012) Satellite DNA-mediated effects on genome regulation. Genome Dyn 7:153–169CrossRefPubMedGoogle Scholar
  49. Plohl M, Luchetti A, Mestrovic N, Mantovani B (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution patterns of tandem repeats in centromeric (hetero) chromatin. Gene 409:72–82CrossRefPubMedGoogle Scholar
  50. Presgraves DC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11:175CrossRefPubMedGoogle Scholar
  51. Preuss SB, Costa-Nunes P, Tucker S et al (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell 32:673–684CrossRefPubMedPubMedCentralGoogle Scholar
  52. Raskina O, Barber JC, Nevo E, Belyayev A (2008) Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res 120:351–357CrossRefPubMedGoogle Scholar
  53. Robledo G, Seijo JG (2008) Characterization of Arachis D genome using physical mapping of heterochromatic regions and rDNA loci by FISH. Genet Mol Biol 31:717–724CrossRefGoogle Scholar
  54. Robledo G, Seijo G (2010) Species relationships among the wild B genome of Arachis species (section Arachis) based on FISH mapping of rDNA loci and heterochromatin detection: a new proposal for genome arrangement. Theor Appl Genet 121:1033–1046CrossRefPubMedGoogle Scholar
  55. Robledo G, Lavia GI, Seijo G (2009) Species relations among wild Arachis species with the A genome as revealed by FISH mapping of rDNA loci and heterochromatin detection. Theor Appl Genet 118:1295–1307CrossRefPubMedGoogle Scholar
  56. Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333CrossRefPubMedPubMedCentralGoogle Scholar
  57. Samoluk SS, Chalup L, Robledo G, Seijo JG (2015a) Genome sizes in diploid and allopolyploid Arachis L. species (section Arachis). Genet Res Crop Evol 62:747–763CrossRefGoogle Scholar
  58. Samoluk SS, Robledo G, Podio M, Chalup L, Ortiz JPA, Pessino SC, Seijo JG (2015b) First insight into divergence, representation and chromosome distribution of reverse transcriptase fragments from L1 retrotransposons in peanut and wild relative species. Genetica 143:113–125CrossRefPubMedGoogle Scholar
  59. Samoluk SS, Robledo G, Bertioli D, Seijo JG (2017) Evolutionary dynamics of an AT-rich satellite DNA and its contribution to karyotype differentiation in wild diploid Arachis species. Mol Genet Genom 292:283–296CrossRefGoogle Scholar
  60. SanMiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82:37–44CrossRefGoogle Scholar
  61. Santana SH, Valls JF (2015) Arachis veigae (Fabaceae), the most dispersed wild species of the genus, and yet taxonomically overlooked. Bonplandia 24:139–150CrossRefGoogle Scholar
  62. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefPubMedGoogle Scholar
  63. Seijo G, Lavia GI, Fernández A, Krapovickas A, Ducasse D, Moscone EA (2004) Physical mapping of 5S and 18S-25S rRNA genes evidences that Arachis duranensis and A. ipaensis are the wild diploid species involved in the origin of A. hypogaea (Leguminosae). Am J Bot 91:2293–2303CrossRefGoogle Scholar
  64. Seijo G, Lavia GI, Fernández A, Krapovickas A, Ducasse D, Bertioli DJ, Moscone EA (2007) Genomic relationships between the cultivated peanut (Arachis hypogaea, Leguminosae) and its close relatives revealed by double GISH. Am J Bot 94:1963–1971CrossRefPubMedGoogle Scholar
  65. Seijo JG, Kovalsky IE, Chalup LMI, Samoluk SS, Fávero A, Robledo G (2018) Karyotype stability and genome specific nucleolar dominance in peanut, its wild 4× ancestor and in a synthetic AABB polyploidy. Crop Sci. CrossRefGoogle Scholar
  66. Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109:15–26CrossRefPubMedGoogle Scholar
  67. Shirasawa K, Koilkonda P, Aoki K et al (2012) In silico polymorphism analysis for the development of simple sequence repeat and transposon markers and construction of linkage map in cultivated peanut. BMC Plant Biol 12:80CrossRefPubMedPubMedCentralGoogle Scholar
  68. Silvestri MC, Ortiz AM, Lavia GI (2014) rDNA loci and heterochromatin positions support a distinct genome type for ‘x = 9 species’ of section Arachis (Arachis, Leguminosae). Plant Syst Evol 301:555–562CrossRefGoogle Scholar
  69. Simpson CE (2001) Use of wild Arachis species/introgression of genes into A. hypogaea L. Peanut Sci 28:114–116CrossRefGoogle Scholar
  70. Sousa A, Fuchs J, Renner SS (2017) Cytogenetic comparison of heteromorphic and homomorphic sex chromosomes in Coccinia (Cucurbitaceae) points to sex chromosome turnover. Chromosome Res 25:191–200CrossRefPubMedGoogle Scholar
  71. Stalker HT (1991) A new species-section Arachis of peanuts with D genome. Am J Bot 78:630–637CrossRefGoogle Scholar
  72. Sveinsson S, Gill N, Kane NC, Cronk Q (2013) Transposon fingerprinting using low coverage whole genome shotgun sequencing in Cacao (Theobroma cacao L.) and related species. BMC Genom 14:502CrossRefGoogle Scholar
  73. Valls JFM, Simpson CE (2005) New species of Arachis (Leguminosae) from Brazil, Paraguay and Bolivia. Bonplandia 14:35–64Google Scholar
  74. Valls JFM, Simpson CE (2017) A new species of Arachis (Fabaceae) from Mato Grosso, Brazil, related to Arachis matiensis. Bonplandia 26:143–149CrossRefGoogle Scholar
  75. Valls JFM, Da Costa LC, Custodio AR (2013) A novel trifoliolate species of Arachis (Fabaceae) and further comments on the taxonomic section Trierectoides. Bonplandia 22:91–97CrossRefGoogle Scholar
  76. Waminal NE, Ryu KB, Park BR, Kim HH (2014) Phylogeny of Cucurbitaceae species in Korea based on 5S rDNA non-transcribed spacer. Genes Genom 36:57–64CrossRefGoogle Scholar
  77. Zhang L, Xu C, Yu W (2012) Cloning and characterization of chromosomal markers from a Cot-1 library of peanut (Arachis hypogaea L.). Cytogenet Genome Res 137:31–41CrossRefPubMedGoogle Scholar
  78. Zhang L, Yang X, Tian L, Chen L, Yu W (2016) Identification of peanut (Arachis hypogaea) chromosomes using a fluorescence in situ hybridization system reveals multiple hybridization events during tetraploid peanut formation. New Phytol 211:1424–1439CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Sergio S. Samoluk
    • 1
    Email author
  • Laura M. I. Chalup
    • 1
  • Carolina Chavarro
    • 2
  • Germán Robledo
    • 1
    • 3
  • David J. Bertioli
    • 2
  • Scott A. Jackson
    • 2
  • Guillermo Seijo
    • 1
    • 3
  1. 1.Facultad de Ciencias AgrariasInstituto de Botánica del Nordeste (UNNE-CONICET)CorrientesArgentina
  2. 2.Center for Applied Genetic TechnologiesUniversity of GeorgiaAthensUSA
  3. 3.Facultad de Ciencias Exactas y Naturales y AgrimensuraUniversidad Nacional del NordesteCorrientesArgentina

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