Tree Genetics & Genomes

, 13:110 | Cite as

Retrotransposon-based insertion polymorphism markers in mango

  • Kenji Nashima
  • Shingo Terakami
  • Miyuki Kunihisa
  • Chikako Nishitani
  • Moriyuki Shoda
  • Masato Matsumura
  • Yuko Onoue-Makishi
  • Naoya Urasaki
  • Kazuhiko Tarora
  • Tatsushi Ogata
  • Toshiya YamamotoEmail author
Original Article
Part of the following topical collections:
  1. Genome Biology


Retrotransposons are major components of eukaryotic genomes and are present in high copy numbers. We developed retrotransposon-based insertion polymorphism (RBIP) markers based on long terminal repeat (LTR) sequences and flanking genome regions by using shotgun genome sequence data of mango (Mangifera indica L.). Three novel LTR sequences were identified based on two LTR retrotransposon structural features; a 5′ LTR located upstream of the primer binding site and a 3′ LTR showing high sequence similarity to the 5′ LTR. Starting with 377 unique sequences containing both 3′ LTR and downstream genome region sequences, we developed 82 RBIP markers that were applied to DNA fingerprinting of 16 mango accession. Five RBIP markers were enough to distinguish all 16 accessions. Our result showed that LTR identification from shotgun genome sequences was effective for development of retrotransposon-based DNA markers without whole-genome sequence information. We discuss application of the developed RBIP markers for identification of genetic diversity and construction of a genetic linkage map.


DNA marker LTR retrotransposon Mangifera indica RBIP marker 



We thank Mss. F. Hosaka, H. Oshino, N. Shigeta, and N. Yagihashi for their technical help. This study was partially supported by an Okinawa special promotion grant.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

All sequences obtained by 454 GS FLX Plus sequencing are available in the DDBJ Sequence Read Archive ( under the following accession numbers (Submission, DRA004360; BioProject, PRJDB4532; BioSample, SAMD00046318; experiment, DRX049157; and runs, DRR054307 and DRR054308). Nucleotide sequences of 82 retroratnsposon-based insertion polymorphism markers in mango are available in the DDBJ ( under the following accession nos. LC089767–LC089848.

Supplementary material

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  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  2. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Report 9:208–218CrossRefGoogle Scholar
  3. Boeke JD, Stoye JP (1997) Retrotransposons, endogenous retroviruses and the evolution of retroviruses. In: Coffin J, Hughes S, Varmus H (eds) Retroviruses. Cold Spring Harbor Laboratory Press, New York, pp 343–435Google Scholar
  4. Chunwongse C, Phumichai C, Tongyoo P, Juejun N, Chunwongse J (2015) Development of di-nucleotide microsatellite markers and construction of genetic linkage map in mango (Mangifera indica L.) Songklanakarin J Sci Technol 37:119–127Google Scholar
  5. Diwan N, Cregan PB (1997) Automated sizing of fluorescent-labeled simple sequence repeat (SSR) markers to assay genetic variation in soybean. Theor Appl Genet 95:723–733CrossRefGoogle Scholar
  6. Duval MF, Bunel J, Sitbon C, Risterucci AM (2005) Development of microsatellite markers of mango. Mol Ecol Notes 5:824–826CrossRefGoogle Scholar
  7. Ellinghaus D, Kurtz S, Willhoeft U (2008) LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformat 9:18CrossRefGoogle Scholar
  8. Evans EA, Mendoza OJ (2009) World mango trade and the economics of mango production. In: Litz RE (ed) The mango: botany, production and uses. CAB International, Oxfordshire, pp 606–627CrossRefGoogle Scholar
  9. Flavell AJ, Knox MR, Pearce SR, Ellis TH (1998) Retrotransposon-based insertion polymorphisms (RBIP) for high throughput marker analysis. Plant J 16:643–650CrossRefPubMedGoogle Scholar
  10. Fujii H, Ogata T, Shimada T, Endo T, Iketani H, Shimizu T, Yamamoto T, Omura M (2013) Minimal marker: an algorithm and computer program for the identification of minimal sets of discriminating DNA markers for efficient variety identification. J Bioinforma Comput Biol 11:1250022CrossRefGoogle Scholar
  11. Hollender CA, Dardick C (2015) Molecular basis of angiosperm tree architecture. New Phytol 206:541–556CrossRefPubMedGoogle Scholar
  12. Honsho C, Nishiyama K, Eiadthong W, Yonemori K (2005) Isolation and characterization of new microsatellites markers in mango. Mol Ecol Notes 5:152–154CrossRefGoogle Scholar
  13. Jing R, Vershinin A, Grzebyta J, Shaw P, Smýkal P, Marshall D, Ambrose MJ, Ellis TH, Flavell AJ (2010) The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis. BMC Evol Biol 10:44CrossRefPubMedPubMedCentralGoogle Scholar
  14. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467CrossRefPubMedGoogle Scholar
  15. Kalendar R, Grob T, Regina M, Suoniemi A, Schulman A (1999) IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Genet 98:704–711CrossRefGoogle Scholar
  16. Kalendar R, Antonius K, Smýkal P, Schulman AH (2010) iPBS: a universal method for DNA fingerprinting and retrotransposon isolation. Theor Appl Genet 121:1419–1430CrossRefPubMedGoogle Scholar
  17. Kashkush K, Jinggui F, Tomer E, Hillel J, Lavi U (2001) Cultivar identification and genetic map of mango (Mangifera indica). Euphytica 122:129–136CrossRefGoogle Scholar
  18. Kim H, Yamamoto M, Hosaka F, Terakami S, Nishitani C, Sawamura Y, Yamane H, Wu JZ, Matsumoto T, Matsuyama T, Yamamoto T (2011) Molecular characterization of novel Ty1-copia-like retrotransposons in pear (Pyrus pyrifolia). Tree Genet Genomes 7:845–856CrossRefGoogle Scholar
  19. Kim H, Terakami S, Nishitani C, Kurita K, Kanamori H, Katayose Y, Sawamura Y, Saito T, Yamamoto T (2012) Development of cultivar-specific DNA markers based on retrotransposon-based insertional polymorphism in Japanese pear. Breed Sci 62:53–62CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982CrossRefPubMedGoogle Scholar
  21. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532CrossRefPubMedGoogle Scholar
  22. Kumar A, Hirochika H (2001) Applications of retrotransposons as genetic tools in plant biology. Trends Plant Sci 6:127–134CrossRefPubMedGoogle Scholar
  23. Lopez-Valenzuela JA, Martinez O, Paredes-Lopez O (1997) Geographic differentiation and embryo type identification in Mangifera indica L. cultivars using RAPD markers. Hortic Sci 32:1105–1108Google Scholar
  24. Luby JJ, Shaw DV (2001) Does marker-assisted selection make dollars and sense in a fruit breeding program? Hortic Sci 36:872–879Google Scholar
  25. Luo C, Shu B, Yao Q, Wu H, Xu W, Wang S (2016) Construction of a high-density genetic map based on large-scale marker development in mango using specific-locus amplified fragment sequencing (SLAF-seq). Front Plant Sci 7:1310PubMedPubMedCentralGoogle Scholar
  26. Lyer CPA, Schnell RJ (2009) Breeding and genetics. In: Litz RE (ed) The mango: botany, production and uses. CAB International, Oxfordshire, pp 67–96Google Scholar
  27. Mahato AK, Sharma N, Singh A, Srivastav M, Jaiprakash SSK, Singh AK, Sharma TR, Singh NK (2016) Leaf transcriptome sequencing for identifying genic-SSR markers and SNP heterozygosity in crossbred mango variety ‘Amrapali’ (Mangifera indica L.) PLoS ONE 11:e0164325CrossRefPubMedPubMedCentralGoogle Scholar
  28. McCarthy EM, McDonald JF (2003) LTR_STRUC: a novel search and identification program for LTR retrotransposons. Bioinformatics 19:362–367CrossRefPubMedGoogle Scholar
  29. Monden Y, Tahara M (2015) Plant transposable elements and their application to genetic analysis via high-throughput sequencing platform. Hortic J 84:283–294CrossRefGoogle Scholar
  30. Monden Y, Fujii N, Yamaguchi K, Ikeo K, Nakazawa Y, Waki T, Hirashima K, Uchimura Y, Tahara M (2014) Efficient screening of long terminal repeat retrotransposons that show high insertion polymorphism via high-throughput sequencing of the primer binding site. Genome 57:245–252CrossRefPubMedGoogle Scholar
  31. Monden Y, Hara T, Okada Y, Jahana O, Kobayashi A, Tabushi H, Onaga S, Tahara M (2015) Construction of a linkage map based on retrotransposon insertion polymorphisms in sweetpotato via high-throughput sequencing. Breed Sci 65:143–153CrossRefGoogle Scholar
  32. Mukherjee SK (1953) The mango—its botany, cultivation, uses and future improvement, especially as observed in India. Econ Bot 7:130–162CrossRefGoogle Scholar
  33. Mukherjee SK, Litz RE (2009) Introduction: botany and importance. In: Litz RE (ed) The mango: botany, production and uses. CAB International, Oxfordshire, pp 1–19Google Scholar
  34. Okada K, Wada M, Moriya S, Katayose Y, Fujisawa H, Wu JZ, Kanamori H, Kurita K, Sasaki H, Fujii H, Terakami S, Iwanami H, Yamamoto T, Abe K (2016) Expression of a putative dioxygenase gene adjacent to an insertion mutation is involved in the short internodes of columnar apples (Malus × domestica). J Plant Res 129:1109–1126CrossRefPubMedGoogle Scholar
  35. Queen RA, Gribbon BM, James C, Jack P, Flavell AJ (2004) Retrotransposon-based molecular markers for linkage and genetic diversity analysis in wheat. Mol Gen Genomics 271:91–97CrossRefGoogle Scholar
  36. Ravishankar KV, Dinesh MR, Nischita P, Sandya BS (2015) Development and characterization of microsatellite markers in mango (Mangifera indica) using next-generation sequencing technology and their transferability across species. Mol Breed 35:93CrossRefGoogle Scholar
  37. Rohlf FJ (1998) NTSYS, numerical taxonomy and multivariate analysis system, ver. 2.01. Exeter Publishing, Ltd., SetauketGoogle Scholar
  38. Schnell RJ, Ronning CM, Knight RJ (1995) Identification of cultivars and validation of genetic relationships in Mangifera indica L. using RAPD markers. Theor Appl Genet 90:269–271CrossRefPubMedGoogle Scholar
  39. Schnell RJ, Olano CT, Quintanilla WE, Meerow AW (2005) Isolation and characterization of 15 microsatellite loci from mango (Mangifera indica L.) and cross-species amplification in closely related taxa. Mol Ecol Notes 5:625–627CrossRefGoogle Scholar
  40. Sherman A, Rubinstein M, Eshed R, Benita M, Ish-Shalom M, Sharabi-Schwager M, Rozen A, Saada D, Cohen Y, Ophir R (2015) Mango (Mangifera indica L.) germplasm diversity based on single nucleotide polymorphisms derived from the transcriptome. BMC Plant Biol 15:277CrossRefPubMedPubMedCentralGoogle Scholar
  41. Shudo A, Tarora K, Makishi Y, Ichi R, Takahashi K, Matsumura M, Shimabukuro S, Matsuda N, Nakasone S, Urasaki N (2013) Development of CAPS markers and their application in breeding for mango, Mangifera indica L. Euphytica 190:345–355CrossRefGoogle Scholar
  42. Tahara M, Aoki T, Suzuka S, Yamashita H, Tanaka M, Matsunaga S, Kokumai S (2004) Isolation of an active element from a high-copy-number family of retrotransposons in the sweetpotato genome. Mol Gen Genomics 272:116–127CrossRefGoogle Scholar
  43. Vendramin E, Pea G, Dondini L, Pacheco I, Dettori MT, Gazza L, Scalabrin S, Strozzi F, Tartarini S, Bassi D, Verde I, Rossini L (2014) A unique mutation in a MYB gene cosegregates with the nectarine phenotype in peach. PLoS One 9(3):e90574CrossRefPubMedPubMedCentralGoogle Scholar
  44. Viruel MA, Escribano P, Barbieri M, Ferri M, Hormaza JI (2005) Fingerprinting, embryo type and geographic differentiation in mango (Mangifera indica L., Anacardiaceae) with microsatellites. Mol Breed 15:383–393CrossRefGoogle Scholar
  45. Vitte C, Ishii T, Lamy F, Brar D, Panaud O (2004) Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L). Mol Gen Genomics 272:504–511CrossRefGoogle Scholar
  46. Waugh R, McLean K, Flavell AJ, Pearce SR, Kumar A, Thomas BB, Powell W (1997) Genetic distribution of Bare-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol Gen Genet 253:687–694CrossRefPubMedGoogle Scholar
  47. Xu Z, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res 35:W265–W268CrossRefPubMedPubMedCentralGoogle Scholar
  48. You FM, Huo N, Gu YQ, Luo MC, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) Batch primer 3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformat 9:253CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Kenji Nashima
    • 1
    • 2
  • Shingo Terakami
    • 1
  • Miyuki Kunihisa
    • 1
  • Chikako Nishitani
    • 1
  • Moriyuki Shoda
    • 3
  • Masato Matsumura
    • 4
  • Yuko Onoue-Makishi
    • 4
  • Naoya Urasaki
    • 3
  • Kazuhiko Tarora
    • 3
  • Tatsushi Ogata
    • 5
  • Toshiya Yamamoto
    • 1
    Email author
  1. 1.Institute of Fruit Tree and Tea ScienceNAROTsukubaJapan
  2. 2.College of Bioresource SciencesNihon UniversityFujisawaJapan
  3. 3.Okinawa Prefectural Agricultural Research CenterItomanJapan
  4. 4.Okinawa Prefectural Agricultural Research Center Nago BranchNagoJapan
  5. 5.Tropical Agricultuer Research FrontJapan International Research Center for Agricultural SciencesIshigakiJapan

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