Biologia Plantarum

, Volume 59, Issue 4, pp 661–670 | Cite as

Unravelling genome dynamics in Arabidopsis synthetic auto and allopolyploid species

  • M. Bento
  • D. Tomás
  • W. Viegas
  • M. Silva
Original Papers


Polyploidization is a major genome modification that results in plant species with multiple chromosome sets. Parental genome adjustment to co-habit a new nuclear environment results in additional innovation outcomes. We intended to assess genomic changes in polyploid model species with small genomes using inter retrotransposons amplified polymorphism (IRAP) and retrotransposon microsatellite amplified polymorphism (REMAP). Comparative analysis among diploid and autotetraploid A. thaliana and A. suecica lines with their parental lines revealed a marginal fraction of novel bands in both polyploids, and a vast loss of parental bands in allopolyploids. Sequence analysis of some remodelled bands shows that A. suecica parental band losses resulted mainly from sequence changes restricted to primer domains. Moreover, in A. suecica, both parental genomes presented rearrangement frequencies proportional to their sizes. Overall rates of genomic remodelling events detected in A. suecica were similar to those observed in species with a large genome supporting the role of retrotransposons and microsatellite sequences in the evolution of most allopolyploids.

Additional key words

microsatellites polyploidization retrotransposons sequence rearrangement 



amplified fragment length polymorphism


inter retrotransposons amplified polymorphism


long terminal repeats


retrotransposon microsatellite amplified polymorphism


simple sequence repeats


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Supplementary material

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  1. AGI (The Arabidopsis Genome Initiative): Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. — Nature 408: 796–815, 2000.CrossRefGoogle Scholar
  2. Ainouche, M.L.: Plant polyploidy. — New Phytol. 186 (Special Issue): 1–261, 2010.CrossRefPubMedGoogle Scholar
  3. Beaulieu, J., Jean, M., Belzile, F.: The allotetraploid Arabidopsis thaliana-Arabidopsis lyrata subsp. petraea as an alternative model system for the study of polyploidy in plants. — Mol. Genet. Genomics. 281: 421–435, 2009.CrossRefPubMedGoogle Scholar
  4. Bennett, M.D., Leitch, I.J.: Plant DNA C-values Database Release 6.0, Dec. 2012.
  5. Bento, M., Gustafson, P., Viegas, W., Silva, M.: Genome merger: from sequence rearrangements in triticale to their elimination in wheat-rye addition lines. — Theor. appl. Genet. 121: 489–497, 2010.CrossRefPubMedGoogle Scholar
  6. Bento, M., Pereira, S., Rocheta, M., Gustafson, P., Viegas, W., Silva, M.: Polyploidization as a retraction force in plant genome evolution: sequence rearrangements in triticale. — PLoS ONE 3: e1402, 2008.PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bento, M., Tomas, D., Viegas, W., Silva, M.: Retrotransposons represent the most labile fraction for genomic rearrangements in polyploid plant species. — Cytogenet. Genome Res. 140: 286–294, 2013.CrossRefPubMedGoogle Scholar
  8. Bomblies, K., Madlung, A.: Polyploidy in the Arabidopsis genus. — Chromosome Res. 22: 117–134, 2014.CrossRefPubMedGoogle Scholar
  9. Brenchley, R., Spannagl, M., Pfeifer, M., Barker, G.L., D’Amore, R., Allen, A.M., McKenzie, N., Kramer, M., Kerhornou, A., Bolser, D., Kay, S., Waite, D., Trick, M., Bancroft, I., Gu, Y., Huo, N., Luo, M.C., Sehgal, S., Gill, B., Kianian, S., Anderson, O., Kersey, P., Dvorak, J., McCombie, W.R., Hall, A., Mayer, K.F., Edwards, K.J., Bevan, M.W., Hall, N.: Analysis of the bread wheat genome using whole-genome shotgun sequencing. — Nature 491: 705–710, 2012.PubMedCentralCrossRefPubMedGoogle Scholar
  10. Comai, L., Tyagi, A.P., Winter, K., Holmes-Davis, R, Reynolds, S.H., Stevens, Y., Byers, B.: Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. — Plant Cell 12: 1551–1567, 2000.PubMedCentralCrossRefPubMedGoogle Scholar
  11. Dong, Y.Z., Liu, Z.L., Shan, X.H., Qiu, T., He, M.Y., Liu, B.: Allopolyploidy in wheat induces rapid and heritable alterations in DNA methylation patterns of cellular genes and mobile elements. — Russ. J. Genet. 41: 890–896, 2005.CrossRefGoogle Scholar
  12. Dvořák, J.: Triticeae genome structure and evolution. — In: Muehlbauer, G.J., Feuillet, C. (ed.): Genetics and Genomics of the Triticeae. Pp. 685–711. Springer, New York 2009.Google Scholar
  13. Eilam, T., Anikster, Y., Millet, E., Manisterski, J., Feldman, M.: Nuclear DNA amount and genome downsizing in natural and synthetic allopolyploids of the genera Aegilops and Triticum. — Genome 51: 616–627, 2008.CrossRefPubMedGoogle Scholar
  14. Feldman, M., Levy, A.A.: Genome evolution in allopolyploid wheat-a revolutionary reprogramming followed by gradual changes. — J. Genet. Genomics 36: 511–518, 2009.CrossRefPubMedGoogle Scholar
  15. Ferreira-de-Carvalho, J., Chelaifa, H., Boutte, J., Poulain, J., Couloux, A., Wincker, P., Bellec, A., Fourment, J., Berge`s, H., Salmon, A., Ainouche, M.: Exploring the genome of the salt-marsh Spartina maritima (Poaceae, Chloridoideae) through BAC end sequence analysis. — Plant mol. Biol. 83: 591–606, 2013.CrossRefPubMedGoogle Scholar
  16. Hazzouri, R.M., Mohajer, A., Dejak, S.I., Otto, S.P., Wright, S.I.: Contrasting patterns of transposable-element insertion polymorphism and nucleotide diversity in autotetraploid and allotetraploid Arabidopsis species. — Genetics 179: 581–592, 2008.PubMedCentralCrossRefPubMedGoogle Scholar
  17. Henry, I.M., Dilkes, B.P., Tyagi, A., Gao, J., Christensen, B., Comai, L.: The BOY NAMED SUE quantitative trait locus confers increased meiotic stability to an adapted natural allopolyploid of Arabidopsis. — Plant Cell. 26: 181–194, 2014.PubMedCentralCrossRefPubMedGoogle Scholar
  18. Huang, S., Li, R., Zhang, Z., Li, L., Gu, X., Fan, W., Lucas, W.J., Wang, X., Xie, B., Ni, P., Ren, Y., Zhu, H., Li, J., Lin, K., Jin, W., Fei, Z., Li, G., Staub, J., Kilian, A., Van der Vossen, E.A., Wu, Y., Guo, J., He, J., Jia, Z., Ren, Y., Tian, G., Lu, Y., Ruan, J., Qian, W., Wang, M., Huang, Q., Li, B., Xuan, Z., Cao, J., Asan, Wu, Z., Zhang, J., Cai, Q., Bai, Y., Zhao, B., Han, Y., Li, Y., Li, X., Wang, S., Shi, Q., Liu, S., Cho, W.K., Kim, J.Y., Xu, Y., Heller-Uszynska, K., Miao, H., Cheng, Z., Zhang, S., Wu, J., Yang, Y., Kang, H., Li, M., Liang, H., Ren, X., Shi, Z., Wen, M., Jian, M., Yang, H., Zhang, G., Yang, Z., Chen, R., Liu, S., Li, J., Ma, L., Liu, H., Zhou, Y., Zhao, J., Fang, X., Li, G., Fang, L., Li, Y., Liu, D., Zheng, H., Zhang, Y., Qin, N., Li, Z., Yang, G., Yang, S., Bolund, L., Kristiansen, K., Zheng, H., Li, S., Zhang, X., Yang, H., Wang, J., Sun, R., Zhang, B., Jiang, S., Wang, J., Du, Y., Li, S.: The genome of the cucumber, Cucumis sativus L. — Nat. Genet. 41: 1275–1281, 2009.CrossRefPubMedGoogle Scholar
  19. Jiang, B., Lou, Q., Wu, Z., Zhang, W., Wang, D., Mbira, K.G., Weng, Y., Chen, J.: Retrotransposon- and microsatellite sequence-associated genomic changes in early generations of a newly synthesized allotetraploid Cucumis × hytivus Chen & Kirkbride. — Plant mol. Biol. 77: 225–233, 2009.CrossRefGoogle Scholar
  20. Jiao, Y.N., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H.Y., Soltis, P.S., Soltis, D.E., Clifton, S.W., Schlarbaum, S.E., Schuster, S.C., Ma, H., Leebens-Mack, J., De Pamphilis, C.W.: Ancestral polyploidy in seed plants and angiosperms. — Nature 473: 97–100, 2011.CrossRefPubMedGoogle Scholar
  21. Jones, R.N., Hegarty, M.: Order out of chaos in the hybrid plant nucleus. — Cytogenet. Genome Res. 126: 376–389, 2009.CrossRefPubMedGoogle Scholar
  22. Kalendar, R., Grob, T., Regina, M., Suoniemi, A., Schulman, A.: IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. — Theor. appl. Genet. 98: 704–711, 1999.CrossRefGoogle Scholar
  23. Kalendar, R., Schulman, A.H.: IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. — Nat. Protocols 1: 2478–2484, 2006.CrossRefPubMedGoogle Scholar
  24. Kashkush, K., Feldman, M., Levy, A.A.: Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. — Genetics 160: 1651–1659, 2002.PubMedCentralPubMedGoogle Scholar
  25. Ma, X.F., Fang, P., Gustafson, J.P.: Polyploidization-induced genome variation in triticale. — Genome 47: 839–848, 2004.CrossRefPubMedGoogle Scholar
  26. Ma, X.F., Gustafson, J.P.: Timing and rate of genome variation in triticale following allopolyploidization. — Genome 49: 950–958, 2006.CrossRefPubMedGoogle Scholar
  27. Ma, X.F., Gustafson, J.P.: Allopolyploidization-accommodated genomic sequence changes in triticale. — Ann. Bot. 101: 825–832, 2008.PubMedCentralCrossRefPubMedGoogle Scholar
  28. Madlung, A., Tyagi, A.P., Watson, B., Jiang, H.M., Kagochi, T., Doerge, R.W., Martienssen, R., Comai, L.: Genomic changes in synthetic Arabidopsis polyploids. — Plant J. 41: 221–230, 2005.CrossRefPubMedGoogle Scholar
  29. Ozkan, H., Tuna, M., Galbrainth, D.W.: No DNA loss in autotetraploid of Arabidopsis thaliana. — Plant Breed. 125: 288–291, 2006.CrossRefGoogle Scholar
  30. Parisod, C., Salmon, A., Zerjal, T., Tenaillon, M., Grandbastien, M.A., Ainouche, M.: Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. — New Phytol. 184: 1003–1015, 2009.CrossRefPubMedGoogle Scholar
  31. Pecinka, A., Fang, W., Rehmsmeier, M., Levy, A.A., Scheid, O.M.: Polyploidization increases meiotic recombination frequency in Arabidopsis. — BMC Biol. 9: 24, 2011.PubMedCentralCrossRefPubMedGoogle Scholar
  32. Peterson-Burch, B.D., Nettleton, D., Voytas, D.F.: Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae. — Genome Biol. 5: R78, 2004.PubMedCentralCrossRefPubMedGoogle Scholar
  33. Petit, M., Guidat, C., Daniel, J., Denis, E., Montoriol, E., Bui, Q.T., Lim, K.Y., Kovarik, A., Leitch, A.R., Grandbastien, M.A., Mhiri, C.: Mobilization of retrotransposons in synthetic allotetraploid tobacco. — New Phytol. 186: 135–147, 2010.CrossRefPubMedGoogle Scholar
  34. Pontes, O., Neves, N., Silva, M., Lewis, M.S., Madlung, A., Comai, L., Viegas, W., Pikaard, C.S.: Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. — PNAS 101: 18240–18245, 2004.PubMedCentralCrossRefPubMedGoogle Scholar
  35. Rakoczy-Trojanowska, M., Bolibok, H.: Characteristics and a comparison of three classes of microsatellite-based markers and their application in plants. — Cell. mol. Biol. Lett. 9: 221–238, 2004.PubMedGoogle Scholar
  36. Renny-Byfield, S., Kovarik, A., Kelly, L.J., Macas, J., Novak, P., Chase, M.W., Nichols, R.A., Pancholi, M.R., Grandbastien, M.A., Leitch, A.R.: Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high-copy sequences. — Plant J. 74: 829–839, 2013.CrossRefPubMedGoogle Scholar
  37. Rocheta, M., Cordeiro, J., Oliveira, M., Miguel, C.: PpRT1: the first complete gypsy-like retrotransposon isolated in Pinus pinaster. — Planta 225: 551–562, 2007.CrossRefPubMedGoogle Scholar
  38. Saghai-Maroof, M.A., Soliman, K.M., Jorgensen, R.A., Allard, R.W.: Ribosomal DNA spacer-length polymorphisms in barley - Mendelian inheritance, chromosomal location, and population-dynamics. — PNAS 81: 8014–8018, 1984.PubMedCentralCrossRefPubMedGoogle Scholar
  39. Santos, J.L., Alfaro, D., Sanchez-Moran, E., Armstrong, S.J., Franklin, F.C.H.: Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. — Genetics 165: 1533–1540, 2003.PubMedCentralPubMedGoogle Scholar
  40. Shaked, H., Kashkush, K., Ozkan, H., Feldman, M., Levy, A.A.: Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. — Plant Cell 13: 1749–1759, 2001.PubMedCentralCrossRefPubMedGoogle Scholar
  41. Shi, J.Q., Huang, S.M., Fu, D.H., Yu, J.Y., Wang, X.F., Hua, W., Liu, S.Y., Liu, G.H., Wang, H.Z.: Evolutionary dynamics of microsatellite distribution in plants: insight from the comparison of sequenced Brassica, Arabidopsis and other angiosperm species. — Plos One. 8: e59988, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  42. Sierro, N., Battey, J.N., Ouadi, S., Bovet, L., Goepfert, S., Bakaher, N., Peitsch, M.C., Ivanov, N.V.: Reference genomes and transcriptomes of Nicotiana sylvestris and Nicotiana tomentosiformis. — Genome Biol. 14: R60, 2013.PubMedCentralCrossRefPubMedGoogle Scholar
  43. Song, K.M., Lu, P., Tang, K.L., Osborn, T.C.: Rapid genome change in synthetic polyploids of Brassica and Its implications for polyploid evolution. — PNAS 92: 7719–7723, 1995.PubMedCentralCrossRefPubMedGoogle Scholar
  44. Stöck, M., Lamatsch, D.K.: Trends in polyploidy research in animals and plants. — Cytogenet. Genome Res. 140: 2–4, 2013.CrossRefGoogle Scholar
  45. Yu, Z., Haberer, G., Matthes, M., Rattei, T., Mayer, K.F.X., Gierl, A., Torres-Ruiz, R.A.: Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. — PNAS 107: 17809–17814, 2010.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Linking Landscape, Environment, Agriculture and Food (LEAF), Instituto Superior de AgronomiaUniversidade de Lisboa, Tapada da AjudaLisboaPortugal

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