Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

satDNA:

Satellite DNA

FISH:

Fluorescent in situ hybridization

rDNA:

Ribosomal DNA

LTR:

Long terminal repeat

NGS:

Next-generation sequencing

TEs:

Transposable elements

References

  • 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 6:776–791

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 112:545–559

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 47:438–446

    Google Scholar 

  • Biemont C, Vieira C (2006) Genetics: junk DNA as an evolutionary force. Nature 443:521–524

    CAS  PubMed  Google Scholar 

  • Biscotti MA, Canapa A, Forconi M, Olmo E, Barucca M (2015) Transcription of tandemly repetitive DNA: functional roles. Chromosome Res 23:463–477

    CAS  PubMed  Google Scholar 

  • 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 71:550–563

    CAS  PubMed  Google Scholar 

  • 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 159:823–837

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 113:6785–6790

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10:679–690

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dhillon SS, Rake AV, Miksche JP (1980) Reassociation kinetics and cytophotometric characterization of peanut (Arachis hypogaea L.). DNA Plant Physiol 65:1121–1127

    CAS  PubMed  Google Scholar 

  • 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 12:111

    Google Scholar 

  • Fernandez A, Krapovickas A (1994) Cromosomas y evolución en Arachis (Leguminosae). Bonplandia 8:187–220

    Google Scholar 

  • Ferree PM, Prasad S (2012) How can satellite DNA divergence cause reproductive isolation? Let us count the chromosomal ways. Genet Res Int. https://doi.org/10.1155/2012/430136

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 12:1069–1084

    CAS  PubMed  Google Scholar 

  • 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 129:567–569

    CAS  Google Scholar 

  • 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 291:153–158

    Google Scholar 

  • Guerra M (2000) Patterns of heterochromatin distribution in plant chromosomes. Genet Mol Biol 23:1029–1041

    Google Scholar 

  • 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 23:791–806

    CAS  PubMed  Google Scholar 

  • 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 5:277–289

    Google Scholar 

  • Heslop-Harrison JS, Schwarzacher T (2011) Organisation of the plant genome in chromosomes. Plant J 66:18–33

    CAS  PubMed  Google Scholar 

  • 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 6:1013–1022

    CAS  Google Scholar 

  • 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 9:42

    PubMed  PubMed Central  Google Scholar 

  • Jurka J, Kohany O, Pavlicek A et al (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467

    CAS  PubMed  Google Scholar 

  • Kidwell MG, Lisch DR (2000) Transposable elements and host genome evolution. Trends Ecol Evol 15:95–99

    CAS  PubMed  Google Scholar 

  • Kirov I, Divashuk M, Van Laere K, Soloviev A, Khrustaleva L (2014) An easy “SteamDrop” method for high quality plant chromosome preparation. Mol Cytogenet 7:21

    PubMed  PubMed Central  Google Scholar 

  • 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 292:453–464

    CAS  PubMed  Google Scholar 

  • Kloc A, Martienssen R (2008) RNAi, heterochromatin and the cell cycle. Trends Genet 24:511–517

    CAS  PubMed  Google Scholar 

  • Krapovickas A, Gregory W (1994) Taxonomía del género Arachis (Leguminosae). Bonplandia 8:11–86

    Google Scholar 

  • Lu Q, Li H, Hong Y et al (2018) Genome sequencing and analysis of the peanut B-genome progenitor (Arachis ipaensis). Front Plant Sci 9:604

    PubMed  PubMed Central  Google Scholar 

  • 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 112:152–158

    CAS  PubMed  Google Scholar 

  • 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:e0143424

    PubMed  PubMed Central  Google Scholar 

  • Mallikarjuna N (2002) Gene introgression from Arachis glabrata into A. hypogaea, A. duranensis and A. diogoi. Euphytica 124:99–105

    CAS  Google Scholar 

  • Mallikarjuna N, Pande S, Jadhav, Sastri DC, Rao JN (2004) Introgression of disease resistance genes from Arachis kempff-mercadoi into cultivated groundnut. Plant Breed 123:573–576

    CAS  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson J (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229

    CAS  PubMed  Google Scholar 

  • Martienssen RA (2003) Maintenance of heterochromatin by RNA interference of tandem repeats. Nat Genet 35:213–214

    CAS  PubMed  Google Scholar 

  • Mehrotra S, Goyal V (2014) Repetitive sequences in plant nuclear DNA: types, distribution, evolution and function. Genom Proteom Bioinform 12:164–171

    Google Scholar 

  • 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):R10

    PubMed  PubMed Central  Google Scholar 

  • 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 111:113–126

    Google Scholar 

  • Naito K, Zhang F, Tsukiyama T et al (2009) Unexpected consequences of sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134

    CAS  PubMed  Google Scholar 

  • 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 18:227–246

    CAS  PubMed  Google Scholar 

  • 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 287:21–38

    CAS  Google Scholar 

  • Novak P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11:378

    Google Scholar 

  • 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 29:792–793

    CAS  PubMed  Google Scholar 

  • 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 108:1492–1502

    CAS  PubMed  Google Scholar 

  • Pezer Z, Brajkovic J, Feliciello I, Ugarkovic D (2012) Satellite DNA-mediated effects on genome regulation. Genome Dyn 7:153–169

    CAS  PubMed  Google Scholar 

  • 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 409:72–82

    CAS  PubMed  Google Scholar 

  • Presgraves DC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11:175

    CAS  PubMed  Google Scholar 

  • 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 32:673–684

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raskina O, Barber JC, Nevo E, Belyayev A (2008) Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res 120:351–357

    CAS  PubMed  Google Scholar 

  • Robledo G, Seijo JG (2008) Characterization of Arachis D genome using physical mapping of heterochromatic regions and rDNA loci by FISH. Genet Mol Biol 31:717–724

    CAS  Google Scholar 

  • 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 121:1033–1046

    PubMed  Google Scholar 

  • 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 118:1295–1307

    CAS  PubMed  Google Scholar 

  • Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333

    CAS  PubMed  PubMed Central  Google Scholar 

  • Samoluk SS, Chalup L, Robledo G, Seijo JG (2015a) Genome sizes in diploid and allopolyploid Arachis L. species (section Arachis). Genet Res Crop Evol 62:747–763

    Google Scholar 

  • 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 143:113–125

    CAS  PubMed  Google Scholar 

  • 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 292:283–296

    CAS  Google Scholar 

  • 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 82:37–44

    CAS  Google Scholar 

  • Santana SH, Valls JF (2015) Arachis veigae (Fabaceae), the most dispersed wild species of the genus, and yet taxonomically overlooked. Bonplandia 24:139–150

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 91:2293–2303

    Google Scholar 

  • 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 94:1963–1971

    PubMed  Google Scholar 

  • 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. https://doi.org/10.2135/cropsci2018.02.0088

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 12:80

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 301:555–562

    Google Scholar 

  • Simpson CE (2001) Use of wild Arachis species/introgression of genes into A. hypogaea L. Peanut Sci 28:114–116

    CAS  Google Scholar 

  • 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 25:191–200

    CAS  PubMed  Google Scholar 

  • Stalker HT (1991) A new species-section Arachis of peanuts with D genome. Am J Bot 78:630–637

    Google Scholar 

  • 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 14:502

    CAS  Google Scholar 

  • Valls JFM, Simpson CE (2005) New species of Arachis (Leguminosae) from Brazil, Paraguay and Bolivia. Bonplandia 14:35–64

    Google Scholar 

  • Valls JFM, Simpson CE (2017) A new species of Arachis (Fabaceae) from Mato Grosso, Brazil, related to Arachis matiensis. Bonplandia 26:143–149

    Google Scholar 

  • Valls JFM, Da Costa LC, Custodio AR (2013) A novel trifoliolate species of Arachis (Fabaceae) and further comments on the taxonomic section Trierectoides. Bonplandia 22:91–97

    Google Scholar 

  • Waminal NE, Ryu KB, Park BR, Kim HH (2014) Phylogeny of Cucurbitaceae species in Korea based on 5S rDNA non-transcribed spacer. Genes Genom 36:57–64

    Google Scholar 

  • 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 137:31–41

    CAS  PubMed  Google Scholar 

  • 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 211:1424–1439

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Facultad de Ciencias Agrarias, Instituto de Botánica del Nordeste (UNNE-CONICET), Corrientes, Argentina

    Sergio S. Samoluk, Laura M. I. Chalup, Germán Robledo & Guillermo Seijo

  2. Center for Applied Genetic Technologies, University of Georgia, Athens, GA, USA

    Carolina Chavarro, David J. Bertioli & Scott A. Jackson

  3. Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Corrientes, Argentina

    Germán Robledo & Guillermo Seijo

Authors
  1. Sergio S. Samoluk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura M. I. Chalup
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolina Chavarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Germán Robledo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David J. Bertioli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Scott A. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guillermo Seijo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sergio S. Samoluk.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2438 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Samoluk, S.S., Chalup, L.M.I., Chavarro, C. et al. Heterochromatin evolution in Arachis investigated through genome-wide analysis of repetitive DNA. Planta 249, 1405–1415 (2019). https://doi.org/10.1007/s00425-019-03096-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03096-4

Keywords

Search

Navigation