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Marine Biotechnology

, Volume 19, Issue 4, pp 401–409 | Cite as

Chimeras Linked to Tandem Repeats and Transposable Elements in Tetraploid Hybrid Fish

  • Lihai Ye
  • Ni Jiao
  • Xiaojun Tang
  • Yiyi Chen
  • Xiaolan Ye
  • Li Ren
  • Fangzhou Hu
  • Shi Wang
  • Ming Wen
  • Chun Zhang
  • Min Tao
  • Shaojun LiuEmail author
Original Article

Abstract

The formation of the allotetraploid hybrid lineage (4nAT) encompasses both distant hybridization and polyploidization processes. The allotetraploid offspring have two sets of sub-genomes inherited from both parental species, and therefore, it is important to explore its genetic structure. Herein, we construct a bacterial artificial chromosome library of allotetraploids, and then sequence and analyze the full-length sequences of 19 bacterial artificial chromosomes. Sixty-eight DNA chimeras are identified, which are divided into four models according to the distribution of the genomic DNA derived from the parents. Among the 68 genetic chimeras, 44 (64.71%) are linked to tandem repeats (TRs) and 23 (33.82%) are linked to transposable elements (TEs). The chimeras linked to TRs are related to slipped-strand mispairing and double-strand break repair while the chimeras linked to TEs benefit from the intervention of recombinases. In addition, TRs and TEs can also result in insertions/deletions of DNA segments. We conclude that DNA chimeras accompanied by TRs and TEs coordinate a balance between the sub-genomes derived from the parents. It is the first report on the relationship between formation of the DNA chimeras and TRs and TEs in the polyploid animals.

Keywords

Chimeras Tandem repeats Transposable elements Tetraploid hybrid fish 

Notes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grants 30930071, 91331105, 31360514, 31430088, and 31210103918), the Cooperative Innovation Center of Engineering and New Products for Developmental Biology of Hunan Province (20134486), the Construction Project of Key Discipline of Hunan Province and China, and the National High Technology Research and Development Program of China (Grant No. 2011AA100403).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10126_2017_9764_MOESM1_ESM.docx (4 mb)
ESM 1 (DOCX 4133 kb)

References

  1. Anderson LK, Hooker KD, Stack SM (2001) The distribution of early recombination nodules on zygotene bivalents from plants. Genetics 159:1259–1269PubMedPubMedCentralGoogle Scholar
  2. Belancio VP, Roy-Engel AM, Deininger PL (2010) All y’all need to know ‘bout retroelements in cancer. Semin Cancer Biol 20:200–210CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269CrossRefPubMedGoogle Scholar
  4. Bennetzen JL (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15:621–627CrossRefPubMedGoogle Scholar
  5. Bichara M, Wagner J, Lambert IB (2006) Mechanisms of tandem repeat instability in bacteria. Mutat Res Fundam Mol Mech Mutagen 598:144–163Google Scholar
  6. Blair MW, Torres MM, Giraldo MC, Pedraza F (2009) Development and diversity of Andean-derived, gene-based microsatellites for common bean (Phaseolus vulgaris L.) BMC Plant Biol 9:100CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bruggmann R, Bharti AK, Gundlach H, Lai J, Young S et al (2006) Uneven chromosome contraction and expansion in the maize genome. Genome Res 16:1241–1251CrossRefPubMedPubMedCentralGoogle Scholar
  8. Catasti P, Chen X, Mariappan SVS, Bradbury EM, Gupta G (1999) DNA repeats in the human genome. Genetica 106:15–36CrossRefPubMedGoogle Scholar
  9. Christiansen G, Molitor C, Philmus B, Kurmayer R (2008) Nontoxic strains of cyanobacteria are the result of major gene deletion events induced by a transposable element. Mol Biol Evol 25:1695–1704CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cox R, Mirkin SM (1997) Characteristic enrichment of DNA repeats in different genomes. Proc Natl Acad Sci U S A 94:5237–5242Google Scholar
  11. Cridland JM, Macdonald SJ, Long AD, Thornton KR (2013) Abundance and distribution of transposable elements in two Drosophila QTL mapping resources. Mol Biol Evol 30:2311–2327CrossRefPubMedPubMedCentralGoogle Scholar
  12. Debrauwere H, Gendrel CG, Lechat S, Dutreix M (1997) Differences and similarities between various tandem repeat sequences: minisatellites and microsatellites. Biochimie 79:577–586CrossRefPubMedGoogle Scholar
  13. Du RQ (2003) Biostatistics (in Chinese), 2nd edn. Higher Education Press, Beijing, pp 80–81Google Scholar
  14. Echenique VC, Stamova B, Wolters P, Lazo G, Carollo V et al (2002) Frequencies of Ty1-copia and Ty3-gypsy retroelements within the Triticeae EST databases. Theor Appl Genet 104:840–844CrossRefPubMedGoogle Scholar
  15. Finnegan DJ (1992) Transposable elements. Curr Opin Genet Dev 2(6):153–184CrossRefGoogle Scholar
  16. Gaeta RT, Chris PJ (2010) Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol 186:18–28CrossRefPubMedGoogle Scholar
  17. Gemayel R, Vinces MD, Legendre M, Verstrepen KJ (2010) Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annu Rev Genet 44:445–477CrossRefPubMedGoogle Scholar
  18. Goodwin TJ, Butler MI, Poulter RT (2003) Cryptons: a group of tyrosine-recombinase-encoding DNA transposons from pathogenic fungi. Microbiology 149:3099–3109CrossRefPubMedGoogle Scholar
  19. Heyer WD, Ehmsen KT, Jie L (2010) Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44:113–139CrossRefPubMedPubMedCentralGoogle Scholar
  20. Jelesko JG, Carter K, Thompson W, Kinoshita Y, Gruissem W (2004) Meiotic recombination between paralogous RBCSB genes on sister chromatids of Arabidopsis thaliana. Genetics 166:947–957CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jiang N, Bao Z, Zhang X, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–573CrossRefPubMedGoogle Scholar
  22. Kapitonov VV, Jurka J (2006) Self-synthesizing DNA transposons in eukaryotes. Proc Natl Acad Sci U S A 103:4540–4545Google Scholar
  23. Katti MV, Ranjekar PK, Gupta VS (2001) Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 18:1161–1167CrossRefPubMedGoogle Scholar
  24. Kazazian HH (2004) Mobile elements: drivers of genome evolution. Science 303:1626–1632CrossRefPubMedGoogle Scholar
  25. Kunze R, Saedler H, Lonnig WE (1997) Plant transposable elements. Adv Bot Res 27:331–470CrossRefGoogle Scholar
  26. Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221PubMedGoogle Scholar
  27. Li L, Jean M, Belzile F (2006) The impact of sequence divergence and DNA mismatch repair on homeologous recombination in Arabidopsis. Plant J 45:908–916CrossRefPubMedGoogle Scholar
  28. Lim KY, Kovarik A, Matyasek R, Mark W, Chase MW, James JC et al (2007) Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol 175:756–763CrossRefPubMedGoogle Scholar
  29. Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM et al (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437:94–100CrossRefPubMedPubMedCentralGoogle Scholar
  30. Liu B, Wendel JF (2002) Non-Mendelian phenomena in allopolyploid genome evolution. Curr Genomics 3:489–505Google Scholar
  31. Liu S, Liu Y, Zhou G, Zhang X, Luo C et al (2001) The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture 192:171–186CrossRefGoogle Scholar
  32. Liu S, Luo J, Chai J, Ren L, Zhou Y et al (2016) Genomic incompatibilities in the diploid and tetraploid offspring of the goldfish × common carp cross. Proc Natl Acad Sci U S A 113:1327–1332CrossRefPubMedPubMedCentralGoogle Scholar
  33. Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424CrossRefPubMedGoogle Scholar
  34. Mezard C, Vignard J, Drouaud J, Mercier R (2007) The road to crossovers: plants have their say. Trends Genet 23:91–99CrossRefPubMedGoogle Scholar
  35. Naranjo T, Corredor E (2008) Nuclear architecture and chromosome dynamics in the search of the pairing partner in meiosis in plants. Cytogenet Genome Res 120:320–330CrossRefPubMedGoogle Scholar
  36. Oliver KR, Greene WK (2009) Transposable elements: powerful facilitators of evolution. Genes Genomes 31:703–714Google Scholar
  37. Pontes O, Neves N, Silva M, Lewis MS, Madlung A et al (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc Natl Acad Sci U S A 101:18240–18245CrossRefPubMedPubMedCentralGoogle Scholar
  38. Qi L, Friebe B, Zhang P, Gill BS (2007) Homoeologous recombination, chromosome engineering and crop improvement. Chromosom Res 15:3–19CrossRefGoogle Scholar
  39. Rizzon C, Marais G, Gouy M, Biémont C (2002) Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res 12:400–407CrossRefPubMedPubMedCentralGoogle Scholar
  40. Salmon A, Flagel L, Ying B, Udall JA, Wendel JF (2010) Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol 186(1):123–134CrossRefPubMedGoogle Scholar
  41. San FJ, Sung P, Klein H (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77:229–257CrossRefGoogle Scholar
  42. Sang T, Crawford DJ, Stuessy TF (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proc Natl Acad Sci U S A 92:6813–6817CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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
  44. Schug MD, Hutter CM, Wetterstrand KA, Gaudette MS, Mackay TF et al (1998) The mutation rates of di-, tri- and tetranucleotide repeats in Drosophila melanogaster. J Neurosci Res 15:1751–1760Google Scholar
  45. Shapiro JA (2005) A 21st century view of evolution: genome system architecture, repetitive DNA, and natural genetic engineering. Gene 345:91–100CrossRefPubMedGoogle Scholar
  46. Shapiro JA, Sternberg RV (2005) Why repetitive DNA is essential to genome function. Biol Rev 80:227–250CrossRefPubMedGoogle Scholar
  47. Sharma A, Wolfgruber TK, Presting GG (2013) Tandem repeats derived from centromeric retrotransposons. BMC Genomics 14:1–11CrossRefGoogle Scholar
  48. Song C, Liu S, Xiao J, He WG, Zhou Y et al (2012) Polyploid organisms. Sci China Life Sci 55:301–311CrossRefPubMedGoogle Scholar
  49. Stults DM, Killen MW, Williamson EP, Hourigan JS, Vargas HD et al (2009) Human rRNA gene clusters are recombinational hotspots in cancer. Cancer Res 69:9096–9104CrossRefPubMedGoogle Scholar
  50. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell Sci 33:25–35CrossRefGoogle Scholar
  51. Toth G, Gaspari ZJ (2002) Microsatellites in different eukaryotic genomes: survey and analysis. Sociol Rural 46:40–60Google Scholar
  52. Udall JA, Quijada PA, Osborn TC (2005) Detection of chromosomal rearrangements derived from homeologous recombination in four mapping populations of Brassica napus L. Genetics 169:967–979CrossRefPubMedPubMedCentralGoogle Scholar
  53. Verstrepen KJ, An J, Lewitter F, Fink GR (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37(9):986CrossRefPubMedPubMedCentralGoogle Scholar
  54. Wang J, Ye LH, Liu QZ, Peng LY, Liu W et al (2015) Rapid genomic DNA changes in allotetraploid fish hybrids. Heredity 114:601–609CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249CrossRefPubMedGoogle Scholar
  56. Wendel JF, Schnabel T, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci U S A 92(1):280–284CrossRefPubMedPubMedCentralGoogle Scholar
  57. White SE, Wessler SR (1994) Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci U S A 91:11792–11796CrossRefPubMedPubMedCentralGoogle Scholar
  58. Yang S, Arguello JR, Li X, Ding Y, Zhou Q et al (2008) Repetitive element-mediated recombination as a mechanism for new gene origination in, Drosophila. PLoS Genet 4:63–71Google Scholar
  59. Zwierzykowski Z, Tayyar R, Brunell M, Lukaszewski AJ (1998) Genome recombination in intergeneric hybrids between tetraploid Festuca pratensis and Lolium multiflorum. J Hered 89:324–328CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Lihai Ye
    • 1
    • 2
  • Ni Jiao
    • 1
    • 2
  • Xiaojun Tang
    • 1
    • 2
  • Yiyi Chen
    • 1
    • 2
  • Xiaolan Ye
    • 1
    • 2
  • Li Ren
    • 1
    • 2
  • Fangzhou Hu
    • 1
    • 2
  • Shi Wang
    • 1
    • 2
  • Ming Wen
    • 1
    • 2
  • Chun Zhang
    • 1
    • 2
  • Min Tao
    • 1
    • 2
  • Shaojun Liu
    • 1
    • 2
    Email author
  1. 1.State Key Laboratory of Developmental Biology of Freshwater FishHunan Normal UniversityChangshaPeople’s Republic of China
  2. 2.College of Life SciencesHunan Normal UniversityChangshaPeople’s Republic of China

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