Skip to main content
SpringerLink
Log in

The gap in research on polyploidization between plants and vertebrates: model systems and strategic challenges

  • Review
  • Life & Medical Sciences
  • Published:
Science Bulletin

Abstract

Polyploidization via whole-genome duplications (WGD) is a common phenomenon in organisms. However, investigations into this phenomenon differ greatly between plants and animals. Recent research on polyploid plants illustrates the immediate changes that follow WGDs and the mechanisms behind in both genetic and epigenetic consequences. Unfortunately, equivalent questions remain to be explored in animals. Enlightened by botanical research, the study of polyploidization in vertebrates involves the identification of model animals and the establishment of strategies. Here we review and compare the research on plants and vertebrates while considering intrageneric or intraspecific variation in genome size. Suitable research methods on recently established polyploidy systems could provide important clues for understanding what happens after WGDs in vertebrates. The approach yields insights into survival and the rarity of polyploidization in vertebrates. The species of Carassius and the allopolyploid system of goldfish × common carp hybridization appear to be suitable models for unraveling the evolution and adaptation of polyploid vertebrates.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Soltis DE, Soltis PS (1999) Polyploidy recurrent formation and genome evolution. TREE 14:348–352

    Google Scholar 

  2. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437

    Article  Google Scholar 

  3. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  Google Scholar 

  4. Adams KL (2007) Evolution of duplicate gene expression in polyploid and hybrid plants. J Hered 98:136–141

    Article  Google Scholar 

  5. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  Google Scholar 

  6. Cui L, Wall PK, Leebens-Mack JH et al (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749

    Article  Google Scholar 

  7. Tang H, Wang X, Bowers JE et al (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18:1944–1954

    Article  Google Scholar 

  8. Lokki J, Saura A (1979) Polyploidy in insect evolution. Basic Life Sci 13:277–312

    Google Scholar 

  9. Bogart JP (1979) Evolutionary implications of polyploidy in amphibians and reptiles. Basic Life Sci 13:341–378

    Google Scholar 

  10. Mable BK, Alexandrou MA, Taylor MI (2011) Genome duplication in amphibians and fish: an extended synthesis. J Zool 284:151–182

    Article  Google Scholar 

  11. Hegarty MJ, Hiscock SJ (2008) Genomic clues to the evolutionary success of polyploid plants. Curr Biol 18:R435–R444

    Article  Google Scholar 

  12. Liu S, Liu Y, Yang X et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930

    Google Scholar 

  13. Flagel LE, Wendel JF, Udall JA (2012) Duplicate gene evolution, homoeologous recombination, and transcriptome characterization in allopolyploid cotton. BMC Genom 13:302

    Article  Google Scholar 

  14. Thorpe PH, Gonzalez-Barrera S, Rothstein R (2007) More is not always better: the genetic constraints of polyploidy. Trends Genet 23:263–266

    Article  Google Scholar 

  15. Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141

    Article  Google Scholar 

  16. Salmon A, Flagel L, Ying B et al (2010) Homoeologous nonreciprocal recombination in polyploid cotton. New Phytol 186:123–134

    Article  Google Scholar 

  17. Paterson AH, Wendel JF, Gundlach H et al (2012) Repeated polyploidization of gossypium genomes and the evolution of spinnable cotton fibres. Nature 492:423–427

    Article  Google Scholar 

  18. Nei M, Nozawa M (2011) Roles of mutation and selection in speciation: From Hugo de Vries to the modern genomic era. Genome Biol Evol 3:812–829

    Article  Google Scholar 

  19. Silan D, Wenkui W, Jiaping H (2002) Advances of researches on phylogeny of Dendranthema and origin of Chrysanthemum. J Beijing For Univ 24:230–234 (in Chinese)

    Google Scholar 

  20. Song C, Liu S, Xiao J et al (2012) Polyploid organisms. Sci China Life Sci 55:301–311

    Article  Google Scholar 

  21. Jin XX, Zhang QX (2005) Advances in the studies of breeding Primula. Chin Bull Bot 6:013 (in Chinese)

    Google Scholar 

  22. Liu D, Fang H (2002) Study on the role of Chinese Ae. Tauschii in the evolution of Chinese common wheat landraces. Southwest China J Agric Sci 16:32–35 (in Chinese)

    Google Scholar 

  23. Huang ML, Deng XP, Zhao YZ et al (2007) Water and nutrient use efficiency in diploid, tetraploid and hexaploid wheats. J Integr Plant Biol 49:706–715

    Article  Google Scholar 

  24. Liu JH, Sun JY, Dai TB et al (2007) Late-growth photosynthetic characteristics and grain yield of different wheat evolutionary materials. J Plant Ecol 31:138–144 (in Chinese)

    Google Scholar 

  25. Parisod C, Christin PA (2008) Genome-wide association to fine-scale ecological heterogeneity within a continuous population of Biscutella laevigata (Brassicaceae). New Phytol 178:436–447

    Article  Google Scholar 

  26. Gasser M (1986) Genetic-ecological investigations in Biscutella levigatal. Dissertation for Doctoral Degree, ETH Zürich

  27. Symonová R, Flajšhans M, Sember A et al (2013) Molecular cytogenetics in artificial hybrid and highly polyploid sturgeons: an evolutionary story narrated by repetitive sequences. Cytogenet Genome Res 141:153–162

    Article  Google Scholar 

  28. Birstein VJ, Hanner R, DeSalle R (1997) Phylogeny of the acipenseriformes: cytogenetic and molecular approaches. Environ Biol Fishes 48:127–155

    Article  Google Scholar 

  29. Xiao J, Zou T, Chen Y et al (2011) Coexistence of diploid, triploid and tetraploid crucian carp (Carassius auratus) in natural waters. BMC Genet 12:20

    Article  Google Scholar 

  30. Zhou L, Gui JF (2002) Karyotypic diversity in polyploid gibel carp, Carassius auratus gibelio bloch. Genetica 115:223–232

    Article  Google Scholar 

  31. Stöck M, Ustinova J, Betto-Colliard C et al (2012) Simultaneous mendelian and clonal genome transmission in a sexually reproducing, all-triploid vertebrate. Proc Biol Sci 279:1293–1299

    Article  Google Scholar 

  32. Stöck M, Ustinova J, Lamatsch DK (2010) A vertebrate reproductive system involving three ploidy levels: hybrid origin of triploids in a contact zone of diploid and tetraploid palearctic green toads (Bufo viridis subgroup). Evolution 64:944–959

    Article  Google Scholar 

  33. Marsden JE, Schwagert SJ, May B (1987) Single-locus inheritance in the tetraploid treefrog Hyla versicolor with an analysis of expected progeny ratios in tetraploid organisms. Genetics 116:299–311

    Google Scholar 

  34. Mable BK, Bogart JP (1995) Hybridization between tetraploid and diploid species of treefrogs (genus Hyla). J Hered 86:432–440

    Google Scholar 

  35. Brunes TO, Sequeira F, Haddad CF et al (2010) Gene and species trees of a neotropical group of treefrogs: genetic diversification in the Brazilian atlantic forest and the origin of a polyploid species. Mol Phylogenet Evol 57:1120–1133

    Article  Google Scholar 

  36. Davis E, Parker J, Selander RK (1976) The organization of genetic diversity in the parthenogenetic lizard Cnemidophorus tesselatus. Genetics 84:791–805

    Google Scholar 

  37. Bogart JP, Bi K (2013) Genetic and genomic interactions of animals with different ploidy levels. Cytogenet Genome Res 140:117–136

    Article  Google Scholar 

  38. Li SS (1991) Amphibian chromosomes and their evolution. Chin J Zool 26:47–52 (in Chinese)

    Google Scholar 

  39. Mable BK (2003) Breaking down taxonomic barriers in polyploidy research. Trends Plant Sci 8:582–590

    Article  Google Scholar 

  40. Zhou S, Wang J (1996) The cytologic study on ten species of Dendranthema. Wuhan Bot Res 15:289–292 (in Chinese)

    Google Scholar 

  41. Huang RF, Hong Y (1996) Euploidic variation in filial generation of spontaneous triploid Allium tuberosum. Acta Bot Yunnanica 8:85–90 (in Chinese)

    Google Scholar 

  42. Hahn SK, Bai KV, Asiedu R (1990) Tetraploids, triploids, and 2n pollen from diploid interspecific crosses with cassava. Theor Appl Genet 79:433–439

    Article  Google Scholar 

  43. Sherman RA, Voigt PW, Burson BL et al (1991) Apomixis in diploid × triploid Tripsacum dactyloides hybrids. Genome 34:528–532

    Article  Google Scholar 

  44. Scheid OM, Jakovleva L, Afsar K et al (1996) A change of ploidy can modify epigenetic. Proc Natl Acad Sci USA 93:7114–7119

    Article  Google Scholar 

  45. Hegarty MJ, Jones JM, Wilson ID et al (2005) Development of anonymous cdna microarrays to study changes to the senecio floral transcriptome during hybrid speciation. Mol Ecol 14:2493–2510

    Article  Google Scholar 

  46. Hegarty MJ, Barker GL, Wilson ID et al (2006) Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16:1652–1659

    Article  Google Scholar 

  47. Church SA, Spaulding EJ (2009) Gene expression in a wild autopolyploid sunflower series. J Hered 100:491–495

    Article  Google Scholar 

  48. Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17

    Article  Google Scholar 

  49. Xu Y, Zhao Q, Mei S et al (2012) Genomic and transcriptomic alterations following hybridisation and genome doubling in trigenomic allohexaploid Brassica carinata × Brassica rapa. Plant Biol (Stuttg). doi:10.1111/j.1438-8677.2011.00553.x

    Google Scholar 

  50. Henry IM, Dilkes BP, Young K et al (2005) Aneuploidy and genetic variation in the Arabidopsis thaliana triploid response. Genetics 170:1979–1988

    Article  Google Scholar 

  51. Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406

    Article  Google Scholar 

  52. Chen ZJ, Ni ZF (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. BioEssays 28:240–252

    Article  Google Scholar 

  53. Ng DW, Miller M, Yu HH et al (2014) A role for CHH methylation in the parent-of-origin effect on altered circadian rhythms and biomass heterosis in Arabidopsis intraspecific hybrids. Plant Cell 26:2430–2440

    Article  Google Scholar 

  54. Miller M, Zhang CQ, Chen ZJ (2012) Ploidy and hybridity effects on growth vigor and gene expression in Arabidopsis thaliana hybrids and their parents. G3 2:505–513

    Article  Google Scholar 

  55. Osborn TC, Pires JC, Birchler JA et al (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147

    Article  Google Scholar 

  56. Mayfield D, Chen ZJ, Pires JC (2011) Epigenetic regulation of flowering time in polyploids. Curr Opin Plant Biol 14:174–178

    Article  Google Scholar 

  57. Leitch HJ, Bennett ND (1997) Polyploidy in angiosperms. Trends Plant Sci 2:470–476

    Article  Google Scholar 

  58. Ni Z, Kim ED, Ha M et al (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331

    Article  Google Scholar 

  59. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

    Article  Google Scholar 

  60. Sémon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17:505–512

    Article  Google Scholar 

  61. Mable BK (2004) ‘Why polyploidy is rarer in animals than in plants’: myths and mechanisms. Biol J Linn Soc Lond 82:453–466

    Article  Google Scholar 

  62. Wertheim B, Beukeboom LW, van de Zande L (2013) Polyploidy in animals: effects of gene expression on sex determination, evolution and ecology. Cytogenet Genome Res 140:256–269

    Article  Google Scholar 

  63. Wang J, Ye LH, Liu QZ et al (2015) Rapid genomic DNA changes in allotetraploid fish hybrids. Heredity 114:601–609

    Article  Google Scholar 

  64. Ohno S (1970) Evolution by gene duplication. Springer, London

    Book  Google Scholar 

  65. Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104

    Article  Google Scholar 

  66. Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462

    Article  Google Scholar 

  67. Feuillet C, Leach JE, Rogers J et al (2011) Crop genome sequencing: lessons and rationales. Trends Plant Sci 16:77–88

    Article  Google Scholar 

  68. Mayer KFX, Rogers J, Dolezel J et al (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:11

    Google Scholar 

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

    Article  Google Scholar 

  70. Gallardo MH, Bickham JW, Honeycutt RL et al (1999) Discovery of tetraploidy in a mammal. Nature 401:341

    Article  Google Scholar 

  71. Bacquet C, Imamura T, Gonzalez CA et al (2008) Epigenetic processes in a tetraploid mammal. Mamm Genome 19:439–447

    Article  Google Scholar 

  72. Ma W, Zhu ZH, Bi XY et al (2014) Allopolyploidization is not so simple: evidence from the origin of the tribe Cyprinini (Teleostei: Cypriniformes). Curr Mol Med 14:1–8

    Article  Google Scholar 

  73. Luo J, Gao Y, Ma W et al (2014) Tempo and mode of recurrent polyploidization in the Carassius auratus species complex (Cypriniformes, Cyprinidae). Heredity 112:415–427

    Article  Google Scholar 

  74. Gruber SL, Silva AP (2013) Cytogenetic analysis of Phyllomedusa distincta lutz, 1950 (2n = 2x = 26), P. tetraploidea pombal and haddad, 1992 (2n = 4x = 52), and their natural triploid hybrids (2n = 3x = 39) (Anura, Hylidae, Phyllomedusinae). BMC Genet 14:1–13

    Article  Google Scholar 

  75. Hiromichi K (1978) Production of triploid and gynogenetic diploid Xenopus by cold treatment. Dev Growth Differ 20:227–236

    Article  Google Scholar 

  76. Vandepoele K, De Vos W, Taylor JS et al (2004) Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proc Natl Acad Sci USA 101:1638–1643

    Article  Google Scholar 

  77. Hardie DC, Hebert PD (2004) Genome-size evolution in fishes. Can J Fish Aquat Sci 61:1636–1646

    Article  Google Scholar 

  78. Phillips R, Rab P (2001) Chromosome evolution in the Salmonidae (Pisces): an update. Biol Rev 76:1–25

    Article  Google Scholar 

  79. Thorgaard GH, Gall GAE (1979) Adult triploids in a rainbow trout family. Genetics 93:961–973

    Google Scholar 

  80. Johnson RM, Shrimpton JM, Cho GK et al (2007) Dosage effects on heritability and maternal effects in diploid and triploid chinook salmon (Oncorhynchus tshawytscha). Heredity 98:303–310

    Article  Google Scholar 

  81. Carmona JA, Sanjur OI, Doadrio I et al (1997) Hybridogenetic reproduction and maternal ancestry of polyploid Iberian fish: the Tropidophoxinellus alburnoides complex. Genetics 146:983–993

    Google Scholar 

  82. Liu SJ, Liu Y, Zhou GJ et al (2001) The formation of tetraploid stocks of red crucian carp × common carp hybrids as an effect of interspecific hybridization. Aquaculture 192:171–186

    Article  Google Scholar 

  83. Liu S, Qin Q, Xiao J et al (2007) The formation of the polyploid hybrids from different subfamily fish crossings and its evolutionary significance. Genetics 176:1023–1034

    Article  Google Scholar 

  84. D’Hont A, Denoeud F, Aury JM et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217

    Article  Google Scholar 

  85. Harper AL, Trick M, Higgins J et al (2012) Associative transcriptomics of traits in the polyploid crop species Brassica napus. Nat Biotechnol 30:798–802

    Article  Google Scholar 

  86. Higgins J, Magusin A, Trick M et al (2012) Use of mRNA-seq to discriminate contributions to the transcriptome from the constituent genomes of the polyploid crop species Brassica napus. BMC genomics 13:247

    Article  Google Scholar 

  87. Evans BJ, Kelley DB, Tinsley RC et al (2004) A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol Phylogenet Evol 33:197–213

    Article  Google Scholar 

  88. Gao Y, Wang SY, Luo J et al (2012) Quaternary palaeoenvironmental oscillations drove the evolution of the Eurasian Ccarassius auratus complex (Cypriniformes, Cyprinidae). J Biogeogr 39:2264–2278

    Article  Google Scholar 

  89. Wang SY, Luo J, Murphy RW et al (2013) Origin of Chinese goldfish and sequential loss of genetic diversity accompanies new breeds. PLoS ONE 8:e59571

    Article  Google Scholar 

  90. Saski CA, Feltus FA, Parida L et al (2015) BAC sequencing using pooled methods. Methods Mol Biol 1227:55–67

    Article  Google Scholar 

  91. Gupta PK (2008) Single-molecule DNA sequencing technologies for future genomics research. Methods Mol Biol 26:602–611

    Google Scholar 

  92. McCarthy A (2010) Third generation DNA sequencing: Pacific biosciences’ single molecule real time technology. Chem Biol 17:675–676

    Article  Google Scholar 

  93. Shin SC, Ahn DH, Kim SJ et al (2013) Advantages of single-molecule real-time sequencing in high-GC content genomes. PLoS ONE 8:e68824

    Article  Google Scholar 

  94. Chin CS, Alexander DH, Marks P et al (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569

    Article  Google Scholar 

  95. Abbott JC, Butcher SA (2012) Strategies towards sequencing complex crop genomes. Genome Biol 13:3

    Article  Google Scholar 

  96. Gruenheit N, Deusch O, Esser C et al (2012) Cutoffs and K-mers: implications from a transcriptome study in allopolyploid plants. BMC Genom 13:19

    Article  Google Scholar 

  97. Sankoff D, Zheng C, Zhu Q (2007) Polyploids, genome halving and phylogeny. Bioinformatics 23:i433–i439

    Article  Google Scholar 

  98. Lin YR, Draye X, Qian X et al (2000) Locus-specific contig assembly in highly-duplicated genomes, using the BAC-rf method. Nucleic Acids Res 28:E23

    Article  Google Scholar 

  99. Chin FY, Leung HC, Yiu SM (2014) Sequence assembly using next generation sequencing data—challenges and solutions. Sci China Life Sci 57:1140–1148

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (91331105, 31360514), Laboratory of Conservation and Utilization of Bio-resources and Key Laboratory for Animal Genetic Diversity and Evolution of High Education in Yunnan Province, and State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

    Authors and Affiliations

    1. Laboratory of Conservation and Utilization of Bio-resources and Key Laboratory for Animal Genetic Diversity and Evolution of High Education in Yunnan Province, School of Life Sciences, Yunnan University, Kunming, 650091, China

      Jing Chai, Yuebo Su, Feng Huang & Jing Luo

    2. State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, 650223, China

      Jing Chai & Robert W. Murphy

    3. Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, 650000, China

      Jing Chai

    4. College of Life Sciences, Hunan Normal University, Changsha, 410081, China

      Shaojun Liu & Min Tao

    5. Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON, M5S 2C6, Canada

      Robert W. Murphy

    Authors
    1. Jing Chai
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Yuebo Su
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Feng Huang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Shaojun Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Min Tao
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Robert W. Murphy
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Jing Luo
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Jing Luo.

    Additional information

    Jing Chai and Yuebo Su have contributed equally to this work.

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Chai, J., Su, Y., Huang, F. et al. The gap in research on polyploidization between plants and vertebrates: model systems and strategic challenges. Sci. Bull. 60, 1471–1478 (2015). https://doi.org/10.1007/s11434-015-0879-8

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11434-015-0879-8

    Keywords

    Search

    Navigation