Skip to main content
Log in

TAR30, a homolog of the canonical plant TTTAGGG telomeric repeat, is enriched in the proximal chromosome regions of peanut (Arachis hypogaea L.)

  • Original Article
  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Telomeres are the physical ends of eukaryotic linear chromosomes that play critical roles in cell division, chromosome maintenance, and genome stability. In many plants, telomeres are comprised of TTTAGGG tandem repeat that is widely found in plants. We refer to this repeat as canonical plant telomeric repeat (CPTR). Peanut (Arachis hypogaea L.) is a spontaneously formed allotetraploid and an important food and oil crop worldwide. In this study, we analyzed the peanut genome sequences and identified a new type of tandem repeat with 10-bp basic motif TTTT(C/T)TAGGG named TAndem Repeat (TAR) 30. TAR30 showed significant sequence identity to TTTAGGG repeat in 112 plant genomes suggesting that TAR30 is a homolog of CPTR. It also is nearly identical to the telomeric tandem repeat in Cestrum elegans. Fluorescence in situ hybridization (FISH) analysis revealed interstitial locations of TAR30 in peanut chromosomes but we did not detect visible signals in the terminal ends of chromosomes as expected for telomeric repeats. Interestingly, different TAR30 hybridization patterns were found between the newly induced allotetraploid ValSten and its diploid wild progenitors. The canonical telomeric repeat TTTAGGG is also present in the peanut genomes and some of these repeats are closely adjacent to TAR30 from both cultivated peanut and its wild relatives. Overall, our work identifies a new homolog of CPTR and reveals the unique distributions of TAR30 in cultivated peanuts and wild species. Our results provide new insights into the evolution of tandem repeats during peanut polyploidization and domestication.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

CPTR:

Canonical plant telomeric repeat

DAPI:

4,6-Diamidino-2-phenylindole

DNA:

Deoxyribonucleic acid

DSBs:

Double-strand breaks

FISH:

Fluorescence in situ hybridization

LTR:

Long terminal repeat

MYA:

Million years ago

TERT:

Telomerase reverse transcriptase

TEs:

Transposable elements

TSD:

Target site duplication

References

  • El Baidouri M, Carpentier MC, Cooke R, Gao D, Lasserre E, Llauro C, Mirouze M, Picault N, Jackson SA, Panaud O (2014) Widespread and frequent horizontal transfers of transposable elements in plants.

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertioli DJ, Cannon SB, Froenicke L, Huang G, Farmer AD, Cannon EK, Liu X, Gao D, Clevenger J, Dash S, Ren L, Moretzsohn MC, Shirasawa K, Huang W, Vidigal B, Abernathy B, Chu Y, Niederhuth CE, Umale P, Araújo AC, Kozik A, Kim KD, Burow MD, Varshney RK, Wang X, Zhang X, Barkley N, Guimarães PM, Isobe S, Guo B, Liao B, Stalker HT, Schmitz RJ, Scheffler BE, Leal-Bertioli SC, Xun X, Jackson SA, Michelmore R, Ozias-Akins P (2016) The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut. Nat Genet 48:438–446

    Article  CAS  PubMed  Google Scholar 

  • Bertioli DJ, Jenkins J, Clevenger J, Dudchenko O, Gao D, Seijo G, Leal-Bertioli SCM, Ren L, Farmer AD, Pandey MK, Samoluk SS, Abernathy B, Agarwal G, Ballén-Taborda C, Cameron C, Campbell J, Chavarro C, Chitikineni A, Chu Y, Dash S, El Baidouri M, Guo B, Huang W, Kim KD, Korani W, Lanciano S, Lui CG, Mirouze M, Moretzsohn MC, Pham M, Shin JH, Shirasawa K, Sinharoy S, Sreedasyam A, Weeks NT, Zhang X, Zheng Z, Sun Z, Froenicke L, Aiden EL, Michelmore R, Varshney RK, Holbrook CC, Cannon EKS, Scheffler BE, Grimwood J, Ozias-Akins P, Cannon SB, Jackson SA, Schmutz J (2019) The genome sequence of segmental allotetraploid peanut Arachis hypogaea. Nat Genet 51:877–884

    Article  CAS  PubMed  Google Scholar 

  • Bolzán AD (2017) Interstitial telomeric sequences in vertebrate chromosomes: origin, function, instability and evolution. Mutat Res 773:51–65

    Article  Google Scholar 

  • Burge CB, Karlin S (1998) Finding the genes in genomic DNA. Curr Opin Struct Biol 8:346–354

    Article  CAS  PubMed  Google Scholar 

  • Bzikadze AV, Pevzner PA (2020) Automated assembly of centromeres from ultra-long error-prone reads. Nat Biotechnol 38:1309–1316

    Article  CAS  PubMed  Google Scholar 

  • Chester M, Gallagher JP, Symonds VV, Cruz da Silva AV, Mavrodiev EV, Leitch AR, Soltis PS, Soltis DE (2012) Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proc Natl Acad Sci U S A 109:1176–1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi JY, Abdulkina LR, Yin J, Chastukhina IB, Lovell JT, Agabekian IA, Young PG, Razzaque S, Shippen DE, Juenger TE, Shakirov EV, Purugganan MD (2021) Natural variation in plant telomere length is associated with flowering time. Plant Cell 33:1118–1134

    Article  PubMed  PubMed Central  Google Scholar 

  • Du P, Li LN, Zhang ZX, Liu H, Qin L, Huang BY, Dong WZ, Tang FS, Qi ZJ, Zhang XY (2016) Chromosome painting of telomeric repeats reveals new evidence for genome evolution in peanut. J Integr Agr 15:2488–2496

    Article  CAS  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    Article  CAS  PubMed  Google Scholar 

  • Dvořáčková M, Fojtová M, Fajkus J (2015) Chromatin dynamics of plant telomeres and ribosomal genes. Plant J 83:18–37

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fuchs J, Brandes A, Schubert I (1995) Telomere sequence localization and karyotype evolution in higher plants. Plant Syst Evol 196:227–241

    Article  CAS  Google Scholar 

  • Fulnecková J, Sevcíková T, Fajkus J, Lukesová A, Lukes M, Vlcek C, Lang BF, Kim E, Eliás M, Sykorová E (2013) A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol 5:468–483

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao D, Gill N, Kim HR, Walling JG, Zhang W, Fan C, Yu Y, Ma J, SanMiguel P, Jiang N, Cheng Z, Wing RA, Jiang J, Jackson SA (2009) A lineage-specific centromere retrotransposon in Oryza brachyantha. Plant J 60:820–831

    Article  CAS  PubMed  Google Scholar 

  • Gao D, Jiang N, Wing RA, Jiang J, Jackson SA (2015) Transposons play an important role in the evolution and diversification of centromeres among closely related species. Front Plant Sci 6:216

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao D, Li Y, Kim KD, Abernathy B, Jackson SA (2016) Landscape and evolutionary dynamics of terminal repeat retrotransposons in miniature in plant genomes. Genome Biol 17:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao D, Chu Y, Xia H, Xu C, Heyduk K, Abernathy B, Ozias-Akins P, Leebens-Mack JH, Jackson SA (2018) Horizontal Transfer of non-LTR retrotransposons from arthropods to flowering plants. Mol Biol Evol 35:354–364

    Article  CAS  PubMed  Google Scholar 

  • Gao D, Araujo A, Nascimento E, Chavarro MC, Xia H, Jackson S, Bertioli D, Leal-Bertioli S (2021) ValSten: a new wild species derived allotetraploid for increasing genetic diversity of the peanut crop. Genet Resour Crop Evol 68:1471–1485

    Article  CAS  Google Scholar 

  • Gemayel R, Cho J, Boeynaems S, Verstrepen KJ (2012) Beyond junk-variable tandem repeats as facilitators of rapid evolution of regulatory and coding sequences. Genes (basel) 3:461–480

    Article  PubMed Central  Google Scholar 

  • Genome Res 24:831–838

  • Graham MK, Meeker A (2017) Telomeres and telomerase in prostate cancer development and therapy. Nat Rev Urol 14:607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grewal SI, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8:35–46

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Han F (2014) Asymmetric epigenetic modification and elimination of rDNA sequences by polyploidization in wheat. Plant Cell 26:4311–4327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Holbrook CC, Culbreath AK (2007) Registration of ‘Tifrunner’ peanut. J Plant Registrations 1:124

    Article  Google Scholar 

  • Hong JP, Byun MY, Koo DH, An K, Bang JW, Chung IK, An G, Kim WT (2007) Suppression of RICE TELOMERE BINDING PROTEIN 1 results in severe and gradual developmental defects accompanied by genome instability in rice. Plant Cell 19:1770–1781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hudson WH, Ortlund EA (2014) The structure, function and evolution of proteins that bind DNA and RNA. Nat Rev Mol Cell Biol 15:749–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kilian A, Stiff C, Kleinhofs A (1995) Barley telomeres shorten during differentiation but grow in callus culture. Proc Natl Acad Sci U S A 92:9555–9559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982

    Article  PubMed  Google Scholar 

  • Lee HR, Zhang W, Langdon T, Jin W, Yan H, Cheng Z, Jiang J (2005) Chromatin immunoprecipitation cloning reveals rapid evolutionary patterns of centromeric DNA in Oryza species. Proc Natl Acad Sci U S A 102:11793–11798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim KY, Kovarik A, Matyasek R, Chase MW, Clarkson JJ, Grandbastien MA, Leitch AR (2007) Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol 175:756–763

    Article  CAS  PubMed  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, Munoz-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):D70–74

  • Long M, Betrán E, Thornton K, Wang W (2003) The origin of new genes: glimpses from the young and old. Nat Rev Genet 4:865–875

    Article  CAS  PubMed  Google Scholar 

  • Maxwell PH, Belote JM, Levis RW (2006) Identification of multiple transcription initiation, polyadenylation, and splice sites in the Drosophila melanogaster TART family of telomeric retrotransposons. Nucleic Acids Res 4:5498–5507

    Article  Google Scholar 

  • Meyne J, Ratliff RL, Moyzis RK (1989) Conservation of the human telomere sequence (TTAGGG)n among vertebrates. Proc Natl Acad Sci U S A 86:7049–7053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizuno H, Wu J, Kanamori H, Fujisawa M, Namiki N, Saji S, Katagiri S, Katayose Y, Sasaki T, Matsumoto T (2006) Sequencing and characterization of telomere and subtelomere regions on rice chromosomes 1S, 2S, 2L, 6L, 7S, 7L and 8S. Plant J 46:206–217

    Article  CAS  PubMed  Google Scholar 

  • Mondello C, Pirzio L, Azzalin CM, Giulotto E (2000) Instability of interstitial telomeric sequences in the human genome. Genomics 68:111–117

    Article  CAS  PubMed  Google Scholar 

  • Nergadze SG, Rocchi M, Azzalin CM, Mondello C, Giulotto E (2004) Insertion of telomeric repeats at intrachromosomal break sites during primate evolution. Genome Res 14:1704–1710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parker J, Tsagkogeorga G, Cotton JA, Liu Y, Provero P, Stupka E, Rossiter SJ (2013) Genome-wide signatures of convergent evolution in echolocating mammals. Nature 502:228–231

    Article  CAS  PubMed  Google Scholar 

  • Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A (2002) Chromosomal map of the model legume Lotus japonicus. Genet 161:1661–1672

    Article  CAS  Google Scholar 

  • Peška V, Fajkus P, Fojtová M, Dvořáčková M, Hapala J, Dvořáček V, Polanská P, Leitch AR, Sýkorová E, Fajkus J (2015) Characterisation of an unusual telomere motif (TTTTTTAGGG)n in the plant Cestrum elegans (Solanaceae), a species with a large genome. Plant J 82:644–654

    Article  PubMed  Google Scholar 

  • Peska V, Garcia S (2020) Origin, diversity, and evolution of telomere sequences in plants. Front Plant Sci 11:117

    Article  PubMed  PubMed Central  Google Scholar 

  • Peska V, Mátl M, Mandáková T, Vitales D, Fajkus P, Fajkus J, Garcia S (2020) Human-like telomeres in Zostera marina reveal a mode of transition from the plant to the human telomeric sequences. J Exp Bot 71:5786–5793

    Article  CAS  PubMed  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 U S A 87:8222–8226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piegu B, Guyot R, Picault N, Roulin A, Sanyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, Panaud O (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podlevsky JD, Bley CJ, Omana RV, Chen QX, JJ, (2008) The telomerase database. Nucleic Acids Res 36:D339-343

    Article  CAS  PubMed  Google Scholar 

  • Ramachandran D, McKain MR, Kellogg EA, Hawkins J (2020) Evolutionary dynamics of transposable elements following a shared polyploidization event in the tribe Andropogoneae. G3 (Bethesda) 10:4387–4398

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691–1698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Röder MS, Lapitan NL, Sorrells ME, Tanksley SD (1993) Genetic and physical mapping of barley telomeres. Mol Gen Genet 238:294–303

    Article  PubMed  Google Scholar 

  • Schlötterer C, Tautz D (1992) Slippage synthesis of simple sequence DNA. Nucleic Acids Res 20:211–215

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwarzacher T, Heslop-Harrison J (2000) Practical in situ hybridization. BIOS Scientific Publishers Ltd., Oxford

    Google Scholar 

  • Seijo GJ, Lavia GI, Fernandez A, Krapovickas A, Ducasse D, Bertioli DJ, Moscone DEA (2007) Genomic relationships between the cultivated peanut (Arachis hypogaea––Leguminosae) and its close relatives revealed by double GISH. Am J Bot 94:1963–1971

    Article  PubMed  Google Scholar 

  • Shippen DE, McKnight TD (1998) Telomeres, telomerases and plant development. Trend Plant Sci 3:126–130

    Article  Google Scholar 

  • Sulovari A, Li R, Audano PA, Porubsky D, Vollger MR, Logsdon GA; Human Genome Structural Variation Consortium, Warren WC, Pollen AA, Chaisson MJP, Eichler EE (2019) Human specific tandem repeat expansion and differential gene expression during primate evolution. Proc Natl Acad Sci U S A 116:23243–23253

    Article  Google Scholar 

  • Sýkorová E, Lim KY, Kunická Z, Chase MW, Bennett MD, Fajkus J, Leitch AR (2003) Telomere variability in the monocotyledonous plant order Asparagales. Proc Biol Sci 270:1893–1904

    Article  PubMed  PubMed Central  Google Scholar 

  • Sýkorová E, Leitch AR, Fajkus J (2006) Asparagales telomerases which synthesize the human type of telomeres. Plant Mol Biol 60:633–646

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Van de Peer Y, Maere S, Meyer A (2009) The evolutionary significance of ancient genome duplications. Nat Rev Genet 10:725–732

    Article  PubMed  Google Scholar 

  • Wessler SR (2006) Transposable elements and the evolution of eukaryotic genomes. Proc Natl Acad Sci U S A 103:17600–17601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Z, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35:W265–W268

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang QF, Liu L, Liu Y, Zhou ZG (2017) Telomeric localization of the Arabidopsis-type heptamer repeat, (TTTAGGG)n, at the chromosome ends in Saccharina japonica (Phaeophyta). J Phycol 53:235–240

    Article  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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Drs. Corley Holbrook and Gongshe Hu for their valuable comments. We also thank the three anonymous reviewers for their helpful comments.

Funding

This research was funded by the grants from National Peanut Board in the USA and Georgia Peanut Commission.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Dongying Gao, Ana C. G. Araujo or David J. Bertioli.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Disclaimer

Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Additional information

Responsible Editor: Aurora Ruiz-Herrera

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 296 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, D., Nascimento, E.F.M.B., Leal-Bertioli, S.C.M. et al. TAR30, a homolog of the canonical plant TTTAGGG telomeric repeat, is enriched in the proximal chromosome regions of peanut (Arachis hypogaea L.). Chromosome Res 30, 77–90 (2022). https://doi.org/10.1007/s10577-022-09684-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-022-09684-7

Keywords

Navigation