Rapid Genomic and Genetic Changes in the First Generation of Autotetraploid Lineages Derived from Distant Hybridization of Carassius auratus Red Var. (♀) × Megalobrama amblycephala (♂)

  • Qinbo Qin
  • Liu Cao
  • Yude Wang
  • Li Ren
  • Qiwen Liu
  • Yuwei Zhou
  • Chongqing Wang
  • Huan Qin
  • Chun Zhao
  • Shaojun LiuEmail author
Original Article


Autopolyploids are traditionally used to demonstrate multivalent pairing and unstable inheritance. However, the autotetraploid fish (4nRR) (RRRR, 4n = 200) derived from the distant hybridization of Carassius auratus red var. (RCC) (RR, 2n = 100) (♀) × Megalobrama amblycephala (BSB) (BB, 2n = 48) (♂) exhibits chromosome number (or ploidy) stability over consecutive generations (F1F10). Comparative analysis based on somatic and gametic chromosomal loci [centromeric, 5S rDNA, and Ag-NORs (silver-stained nucleolar organizer regions)] revealed that a substantial loss of chromosomal loci during genome doubling increases the divergence between homologous chromosomes and that diploid-like chromosome pairing was restored during meiosis in the first generation of 4nRR lineages. In addition, a comparative analysis of genomes and transcriptomes from 4nRR (F1) and its diploid progenitor (RCC) exhibited significant genomic structure and gene expression changes. From these data, we suggest that genomes and genes diverge and that expression patterns change in the first generations following autotetraploidization, which are processes that might contribute to the stable inheritance and successful establishment of autotetraploid lineages.


Autotetraploid lineages Chromosomal locus Genome Transcriptome Meiosis 


Authors’ Contributions

This study is conceived and designed by S.J.L. and Q.B.Q; Q.B.Q. contributed experimental work, most statistical analyses and the manuscript writing; L.C., Y.D.W., and L.R. contributed primers design and bioinformatics analyses; Q.W.L., Y.W.Z., C.Q.W., H.Q., and C.Z. contributed experimental materials and data collect. All authors read and approve the final manuscript.

Funding Information

This research was financially supported by grants from the Natural Science Foundation of Hunan Province for Distinguished Young Scholars (Grant Nos. 2017JJ1022), the Key Research and Development Program of Hunan Province (Grant Nos. 2018NK2072), the National Natural Science Foundation of China (Grant Nos. 31430088 and 31210103918), the Major Program of the Educational Commission of Hunan Province (Grant No. 17A133), the State Key Laboratory of Developmental Biology of Freshwater Fish, the Cooperative Innovation Center of Engineering and New Products for Developmental Biology of Hunan Province (20134486), the Earmarked Fund for China Agriculture Research System (CARS-45) and the Construction Project of Key Disciplines of Hunan Province and China.

Compliance with Ethical Standards

All the fish were cultured in ponds at the Protection Station of Polyploid Fish, Hunan Normal University, and fed with artificial feed. Fish treatments were performed according to the Care and Use of Agricultural Animals in Agricultural Research and Teaching, approved by the Science and Technology Bureau of China. Approval from the Department of Wildlife Administration was not required for the experiments conducted in this study. Fish were deeply anesthetized with 100 mg/L MS-222 (Sigma-Aldrich) before dissection.

Competing Interests

The authors declare that they have no competing interests.

Supplementary material

10126_2018_9859_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 14 kb)
10126_2018_9859_MOESM2_ESM.docx (24 kb)
ESM 2 (DOCX 23 kb)
10126_2018_9859_MOESM3_ESM.docx (14 kb)
ESM 3 (DOCX 14 kb)
10126_2018_9859_MOESM4_ESM.docx (14 kb)
ESM 4 (DOCX 14 kb)
10126_2018_9859_MOESM5_ESM.xlsx (533 kb)
ESM 5 (XLSX 532 kb)
10126_2018_9859_MOESM6_ESM.xlsx (231 kb)
ESM 6 (XLSX 230 kb)


  1. Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168:2217–2226CrossRefGoogle Scholar
  2. Altshuler D et al (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303CrossRefGoogle Scholar
  3. Barker MS, Arrigo N, Baniaga AE, Li Z, Levin DA (2016) On the relative abundance of autopolyploids and allopolyploids. New Phytol 210:391–398CrossRefGoogle Scholar
  4. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846CrossRefGoogle Scholar
  5. Comai L, Tyagi AP, Winter K, Holmesdavis R, Reynolds SH, Stevens Y, Byers B (2000) Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12:1551–1568CrossRefGoogle Scholar
  6. Conesa A, Götz S, Garcíagómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefGoogle Scholar
  7. De Bodt S, Maere S, Van de Peer Y (2005) Genome duplication and the origin of angiosperms. Trends Ecol Evol 20:591–597CrossRefGoogle Scholar
  8. Dion-Côté AM, Renaut S, Normandeau E, Bernatchez L (2014) RNA-seq reveals transcriptomic shock involving transposable elements reactivation in hybrids of young lake whitefish species. Mol Biol Evol 31:1188–1199CrossRefGoogle Scholar
  9. Gaeta RT, Pires JC, Iniguezluy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19:3403–3417CrossRefGoogle Scholar
  10. He WG, Qin Q, Liu S, Li T, Wang J, Xiao J, Xie L, Zhang C, Liu Y (2012) Organization and variation analysis of 5S rDNA in different ploidy-level hybrids of red crucian carp × Topmouth Culter. PLoS One 7:e38976CrossRefGoogle Scholar
  11. Jackson RC (1982) Polyploidy and Diploidy: new perspectives on chromosome pairing and its evolutionary implications. Am J Bot 69:1512–1523CrossRefGoogle Scholar
  12. Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659Google Scholar
  13. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. Bmc Bioinformatics 12:323CrossRefGoogle Scholar
  14. Li H, Durbin R (2010) Fast and accurate long-read alignment with burrows–wheeler transform. Bioinformatics 26:589–595CrossRefGoogle Scholar
  15. Lim KY, Soltis DE, Soltis PS, Tate J, Matyasek R, Srubarova H, Kovarik A, Pires JC, Xiong Z, Leitch AR (2008) Rapid chromosome evolution in recently formed Polyploids in Tragopogon (Asteraceae). PLoS One 3:e3353CrossRefGoogle Scholar
  16. Liu SJ (2010) Distant hybridization leads to different ploidy fishes. Sci China Life Sci 53:416–425CrossRefGoogle Scholar
  17. Liu S, Qin Q, Xiao J, Lu W, Shen J, Li W, Liu J, Duan W, Zhang C, Tao M, Zhao R, Yan J, Liu Y (2007) The formation of the polyploid hybrids from different subfamily fish crossings and its evolutionary significance. Genetics 176:1023–1034CrossRefGoogle Scholar
  18. Mallet J (2007) Hybrid speciation. Nature 446:279–283CrossRefGoogle Scholar
  19. Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264:421–424CrossRefGoogle Scholar
  20. Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331CrossRefGoogle Scholar
  21. Osborn TC, Chris Pires J, Birchler JA, Auger DL, Jeffery Chen Z, Lee HS, Comai L, Madlung A, Doerge RW, Colot V, Martienssen RA (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147CrossRefGoogle Scholar
  22. Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462CrossRefGoogle Scholar
  23. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437CrossRefGoogle Scholar
  24. Parisod C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17CrossRefGoogle Scholar
  25. Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 101:9903–9908CrossRefGoogle Scholar
  26. Pontes O, Neves N, Silva M, Lewis MS, Madlung A, Comai L, Viegas W, Pikaard CS (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc Natl Acad Sci U S A 101:18240–18245CrossRefGoogle Scholar
  27. Qin Q, He W, Liu S, Wang J, Xiao J, Liu Y (2010) Analysis of 5S rDNA organization and variation in polyploid hybrids from crosses of different fish subfamilies. J Exp Zool B Mol Dev Evol 314:403–411CrossRefGoogle Scholar
  28. Qin Q, Wang Y, Wang J, Dai J, Liu Y, Liu S (2014a) Abnormal chromosome behavior during meiosis in the allotetraploid of Carassius auratus red var. (♀) × Megalobrama amblycephala (♂). BMC Genet 15:95CrossRefGoogle Scholar
  29. Qin Q et al (2014b) The autotetraploid fish derived from hybridization of Carassius auratus red var. (female) × Megalobrama amblycephala (male). Biol Reprod 91:93CrossRefGoogle Scholar
  30. Qin Q, Wang J, Dai J, Wang Y, Liu Y, Liu S (2015a) Induced all-female Autotriploidy in the Allotetraploids of Carassius auratus red var. (♀) × Megalobrama amblycephala (♂). Mar Biotechnol 17:1–9CrossRefGoogle Scholar
  31. Qin Q, Wang J, Wang Y, Liu Y, Liu S (2015b) Organization and variation analysis of 5S rDNA in gynogenetic offspring of Carassius auratus red var. (♀) × Megalobrama amblycephala (♂). BMC Genet 16:26CrossRefGoogle Scholar
  32. Qin Q, Lai Z, Cao L, Xiao Q, Wang Y, Liu S (2016) Rapid genomic changes in allopolyploids of Carassius auratus red var. (♀) × Megalobrama amblycephala (♂). Sci Rep 6:34417CrossRefGoogle Scholar
  33. Ramsey J, Schemske DW (2002) Neopolyploidy in flowering plants. Annu Rev Ecol Syst 33:589–639CrossRefGoogle Scholar
  34. Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914CrossRefGoogle Scholar
  35. Skalická K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik A (2005) Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytol 166:291–303CrossRefGoogle Scholar
  36. Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proc Natl Acad Sci U S A 97:7051–7057CrossRefGoogle Scholar
  37. Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588CrossRefGoogle Scholar
  38. Soltis DE, Soltis PS (2010) What we still don’t know about polyploidy. Taxon 59:1387–1403Google Scholar
  39. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, de Pamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96:336–348CrossRefGoogle Scholar
  40. Song K, Lu P, Tang K, Osborn TC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Natl Acad Sci U S A 92:7719–7723CrossRefGoogle Scholar
  41. Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge RW, Comai L, Chen ZJ (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517CrossRefGoogle Scholar
  42. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249CrossRefGoogle Scholar
  43. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci U S A 106:13875–13879CrossRefGoogle Scholar
  44. Wu R, Gallomeagher M, Littell RC, Zeng ZB (2001) A general polyploid model for analyzing gene segregation in outcrossing tetraploid species. Genetics 159:869–882Google Scholar
  45. Xiong Z, Gaeta RT, Pires JC (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Natl Acad Sci U S A 108:7908–7913CrossRefGoogle Scholar
  46. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297CrossRefGoogle Scholar
  47. Zheng Y, Georg H, Michaela M, Thomas R, Klaus F, Alfons G, Ramon A (2010) Impact of natural genetic variation on the transcriptome of autotetraploid Arabidopsis thaliana. Proc Natl Acad Sci USA 107:17809–17814Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018
corrected publication 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life SciencesHunan Normal UniversityChangshaPeople’s Republic of China

Personalised recommendations