Skip to main content

Genomic aspects of research involving polyploid plants

Abstract

Almost all extant plant species have doubled their genomes at least once in their evolutionary histories, resulting in polyploidy which provided a rich genomic resource for evolutionary processes. Moreover, superior polyploid clones have been developed during the process of crop domestication. Polyploid plants generated by evolutionary processes and/or crop domestication have been the intentional or serendipitous focus of research dealing with the dynamics and consequences of genome evolution. One of the new trends in genomics research is to create synthetic polyploid plants which provide materials for studying the initial genomic changes/responses immediately after polyploid formation. Polyploid plants are also used in functional genomics research to study gene expression in a complex genomic background. In this review, we summarize recent progress in genomics research involving ancient, young, and synthetic polyploid plants, with a focus on genome size evolution, genomic diversity, genomic rearrangement, genetic and epigenetic changes in duplicated genes, gene discovery, and comparative genomics. Implications on plant sciences including evolution, functional genomics, and plant breeding are presented. Polyploids will be a focus of genomic research in the future as rapid advances in DNA sequencing technology create unprecedented opportunities for discovering and monitoring genomic and transcriptomic changes. The accumulation of knowledge on polyploid formation, maintenance, and divergence at whole-genome and subgenome levels will not only help plant biologists understand how plants have evolved and diversified, but also assist plant breeders in designing new strategies for crop improvement.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Abel S, Mollers C, Becker HC (2005) Development of synthetic Brassica napus lines for the analysis of “fixed heterosis” in allopolyploid plants. Euphytica 146:157–163

    CAS  Article  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  4. Adams KL, Cronn R, Percifield R et al (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100:4649–4654

    CAS  Article  PubMed  Google Scholar 

  5. Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theor Appl Genet 119:507–517

    CAS  Article  PubMed  Google Scholar 

  6. Ampomah-Dwamena C, Morris BA, Sutherland P et al (2002) Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol 130:605–617

    CAS  Article  PubMed  Google Scholar 

  7. Ananiev EV, Wu C, Chamberlin MA et al (2009) Artificial chromosome formation in maize (Zea mays L.). Chromosoma 118:157–177

    CAS  Article  PubMed  Google Scholar 

  8. Beaulieu J, Jean M, Belzile F (2009) 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

    CAS  Article  PubMed  Google Scholar 

  9. Bennett MD (2004) Perspectives on polyploidy in plants—ancient and neo. Biol J Linn Soc 82:411–423

    Article  Google Scholar 

  10. Besnard G, Garcia-Verdugo C, De Casas RR et al (2008) Polyploidy in the olive complex (Olea europaea): evidence from flow cytometry and nuclear microsatellite analyses. Ann Bot-London 101:25–30

    CAS  Article  Google Scholar 

  11. Birchler JA, Veitia RA (2010) The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol 186:54–62

    CAS  Article  PubMed  Google Scholar 

  12. Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    CAS  Article  PubMed  Google Scholar 

  13. Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13:137–144

    CAS  Article  PubMed  Google Scholar 

  14. Bowers JE, Chapman BA, Rong J et al (2003) Unravelling Angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    CAS  Article  PubMed  Google Scholar 

  15. Bretagnolle F, Thompson J (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol 129:1–22

    Article  Google Scholar 

  16. Buggs RJA, Elliott NM, Zhang LJ et al (2010) Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. New Phytol 186:175–183

    CAS  Article  PubMed  Google Scholar 

  17. Bundock PC, Eliott FG, Ablett G et al (2009) Targeted single nucleotide polymorphism (SNP) discovery in a highly polyploid plant species using 454 sequencing. Plant Biotechnol J 7:347–354

    CAS  Article  PubMed  Google Scholar 

  18. Burleigh JG, Bansal MS, Wehe A et al (2009) Locating large-scale gene duplication events through reconciled trees: implications for identifying ancient polyploidy events in plants. J Comput Biol 16:1071–1083

    CAS  Article  PubMed  Google Scholar 

  19. Carputo D, Frusciante L, Peloquin SJ (2003) The role of 2n gametes and endosperm balance number in the origin and evolution of polyploids in the tuber-bearing solanums. Genetics 163:287–294

    CAS  PubMed  Google Scholar 

  20. Chantret N, Salse J, Sabot F et al (2005) Molecular basis of evolutionary events that shaped the Hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:1033–1045

    CAS  Article  PubMed  Google Scholar 

  21. Chaudhary B, Flagel L, Stupar RM et al (2009) Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182:503–517

    CAS  Article  PubMed  Google Scholar 

  22. Chelaifa H, Monnier A, Ainouche M (2010) Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina x townsendii and Spartina anglica (Poaceae). New Phytol 186:161–174

    CAS  Article  PubMed  Google Scholar 

  23. Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15:57–71

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  25. Clarindo WR, de Carvalho CR, Araujo FS et al (2008) Recovering polyploid papaya in vitro regenerants as screened by flow cytometry. Plant Cell Tiss Org 92:207–214

    Article  Google Scholar 

  26. Cousin A, Heel K, Cowling WA et al (2009) An efficient high-throughput flow cytometric method for estimating DNA ploidy level in plants. Cytom Part A 75A:1015–1019

    CAS  Article  Google Scholar 

  27. Dart S, Kron P, Mable BK (2004) Characterizing polyploidy in Arabidopsis lyrata using chromosome counts and flow cytometry. Can J of Bot 82:185–197

    Article  Google Scholar 

  28. Donnison IS, Francis D (1994) Experimental control of floral reversion in isolated shoot apices of the long-day plant Silene coeli-rosa. Physiol Plant 92:329–335

    CAS  Article  Google Scholar 

  29. Eaton TD, Curley J, Williamson RC et al (2004) Determination of the level of variation in polyploidy among Kentucky bluegrass cultivars by means of flow cytometry. Crop Sci 44:2168–2174

    Article  Google Scholar 

  30. Edger PP, Pires JC (2009) Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res 17:699–717

    CAS  Article  PubMed  Google Scholar 

  31. Ewald D, Ulrich K, Naujoks G et al (2009) Induction of tetraploid poplar and black locust plants using colchicine: chloroplast number as an early marker for selecting polyploids in vitro. Plant Cell Tiss Org 99:353–357

    Article  Google Scholar 

  32. Flagel LE, Wendel JF (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186:184–193

    CAS  Article  PubMed  Google Scholar 

  33. Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453

    CAS  Article  PubMed  Google Scholar 

  34. Gao SC, Gu YQ, Wu JJ et al (2007) Rapid evolution and complex structural organization in genomic regions harboring multiple prolamin genes in the polyploid wheat genome. Plant Mol Biol 65:189–203

    CAS  Article  PubMed  Google Scholar 

  35. Goyal A, Bhowmik PK, Basu SK (2009) Minichromosomes: the second generation genetic engineering tool. Plant Omics 2:1–8

    CAS  Google Scholar 

  36. Grant V (1981) Plant speciation. Columbia University Press, New York

    Google Scholar 

  37. Grover CE, Kim H, Wing RA et al (2007) Microcolinearity and genome evolution in the AdhA region of diploid and polyploid cotton (Gossypium). Plant J 50:995–1006

    CAS  Article  PubMed  Google Scholar 

  38. Grundt HH, Obermayer R, Borgen L (2005) Ploidal levels in the arctic-alpine polyploid Draba lactea (Brassicaceae) and its low-ploid relatives. Bot J Linn Soc 147:333–347

    Article  Google Scholar 

  39. Halverson K, Heard SB, Nason JD et al (2008) Origins, distribution, and local co-occurrence of polyploid cytotypes in Solidago altissima (Asteraceae). Am J Bot 95:50–58

    Article  Google Scholar 

  40. Harbaugh DT (2008) Polyploid and hybrid origins of Pacific island sandalwoods (Santalum, Santalaceae) inferred from low-copy nuclear and flow cytometry data. Int J Plant Sci 169:677–685

    CAS  Article  Google Scholar 

  41. Hegarty M, Hiscock S (2007) Polyploidy: doubling up for evolutionary success. Curr Biol 17:R927–R929

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  43. Henry IM, Dilkes BP, Tyagi AP et al (2009) Dosage and parent-of-origin effects shaping aneuploid swarms in Arabidopsis thaliana. Heredity 103:458–468

    CAS  Article  PubMed  Google Scholar 

  44. Ho I, Wan Y, Widholm JM et al (1990) The use of stomatal chloroplast number for rapid-determination of ploidy level in maize. Plant Breed 105:203–210

    Article  Google Scholar 

  45. Hovav R, Udall JA, Chaudhary B et al (2008) Partitioned expression of duplicated genes during development and evolution of a single cell in a polyploid plant. Proc Natl Acad Sci USA 105:6191–6195

    CAS  Article  PubMed  Google Scholar 

  46. Hufton AL, Panopoulou G (2009) Polyploidy and genome restructuring: a variety of outcomes. Curr Opin Genet Dev 19:600–606

    CAS  Article  PubMed  Google Scholar 

  47. Innes RW, Ameline-Torregrosa C, Ashfield T et al (2008) Differential accumulation of retroelements and diversification of NB-LRR disease resistance genes in duplicated regions following polyploidy in the ancestor of soybean. Plant Physiol 148:1740–1759

    CAS  Article  PubMed  Google Scholar 

  48. Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major Angiosperm phyla. Nature 449:U463–U465

    Article  Google Scholar 

  49. Jannoo N, Grivet L, Chantret N et al (2007) Orthologous comparison in a gene-rich region among grasses reveals stability in the sugarcane polyploid genome. Plant J 50:574–585

    CAS  Article  PubMed  Google Scholar 

  50. Khaitova L, Werlemark G, Nybom H et al (2010) Frequent silencing of rDNA loci on the univalent-forming genomes contrasts with their stable expression on the bivalent-forming genomes in polyploid dogroses (Rosa sect. Caninae). Heredity 104:113–120

    CAS  Article  PubMed  Google Scholar 

  51. Koukalova B, Moraes AP, Renny-Byfield S et al (2010) Fall and rise of satellite repeats in allopolyploids of Nicotiana over c. 5 million years. New Phytol 186:148–160

    CAS  Article  PubMed  Google Scholar 

  52. Lackey E, Ng DWK, Chen ZJ (2010) RNAi-mediated down-regulation of DCL1 and AGO1 induces developmental changes in resynthesized Arabidopsis allotetraploids. New Phytol 186:207–215

    CAS  Article  PubMed  Google Scholar 

  53. Lavania UC, Srivastava S, Lavania S (2010) Ploidy-mediated reduced segregation facilitates fixation of heterozygosity in the aromatic grass, Cymbopogon martinii (Roxb.). J Hered 101:119–123

    Article  PubMed  Google Scholar 

  54. Le Cunff L, Garsmeur O, Raboin LM et al (2008) Diploid/polyploid syntenic shuttle mapping and haplotype-specific chromosome walking toward a rust resistance gene (Bru1) in highly polyploid sugarcane (2n 12x 115). Genetics 180:649–660

    Article  PubMed  Google Scholar 

  55. Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linn Soc 82:651–663

    Article  Google Scholar 

  56. Leitch AR, Leitch IJ (2008) Perspective—genomic plasticity and the diversity of polyploid plants. Science 320:481–483

    CAS  Article  PubMed  Google Scholar 

  57. Leitch IJ, Hanson L, Lim KY et al (2008) The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann Bot Lond 101:805–814

    CAS  Article  Google Scholar 

  58. Li WL, Huang L, Gill BS (2008) Recurrent deletions of puroindoline genes at the grain Hardness locus in four independent lineages of polyploid wheat. Plant Physiol 146:200–212

    CAS  Article  PubMed  Google Scholar 

  59. Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Genet 23:60–66

    CAS  Article  PubMed  Google Scholar 

  60. Liu ZL, Adams KL (2007) Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Curr Biol 17:1669–1674

    CAS  Article  PubMed  Google Scholar 

  61. Liu B, Hu B, Dong YZ et al (2000) Speciation-induced heritable cytosine methylation changes in polyploid wheat. Prog Nat Sci 10:601–606

    CAS  Google Scholar 

  62. Makarevitch I, Harris C (2010) Aneuploidy causes tissue-specific qualitative changes in global gene expression patterns in maize. Plant Physiol 152:927–938

    CAS  Article  PubMed  Google Scholar 

  63. Marmagne A, Brabant P, Thiellement H et al (2010) Analysis of gene expression in resynthesized Brassica napus allotetraploids: transcriptional changes do not explain differential protein regulation. New Phytol 186:216–227

    CAS  Article  PubMed  Google Scholar 

  64. McCullough E, Wright KM, Alvarez A et al (2010) Photoperiod-dependent floral reversion in the natural allopolyploid Arabidopsis suecica. New Phytol 186:239–250

    CAS  Article  PubMed  Google Scholar 

  65. Mestiri I, Chague V, Tanguy AM et al (2010) Newly synthesized wheat allohexaploids display progenitor-dependent meiotic stability and aneuploidy but structural genomic additivity. New Phytol 186:86–101

    CAS  Article  PubMed  Google Scholar 

  66. Mudge SR, Osabe K, Casu RE et al (2009) Efficient silencing of reporter transgenes coupled to known functional promoters in sugarcane, a highly polyploid crop species. Planta 229:549–558

    CAS  Article  PubMed  Google Scholar 

  67. Parisod C, Alix K, Just J et al (2010a) Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol 186:37–45

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  69. Pignatta D, Dilkes BP, Yoo SY et al (2010) Differential sensitivity of the Arabidopsis thaliana transcriptome and enhancers to the effects of genome doubling. New Phytol 186:194–206

    CAS  Article  PubMed  Google Scholar 

  70. Rong J, Bowers JE, Schulze SR et al (2005) Comparative genomics of Gossypium and Arabidopsis: unraveling the consequences of both ancient and recent polyploidy. Genome Res 15:1198–1210

    CAS  Article  PubMed  Google Scholar 

  71. Rong J, Feltus EA, Waghmare VN et al (2007) Meta-analysis of polyploid cotton QTL shows unequal contributions of subgenomes to a complex network of genes and gene clusters implicated in lint fiber development. Genetics 176:2577–2588

    CAS  Article  PubMed  Google Scholar 

  72. Salmon A, Ainouche ML (2010) Polyploidy and DNA methylation: new tools available. Mol Ecol 19:213–215

    Article  PubMed  Google Scholar 

  73. Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  75. Santos JL, Alfaro D, Sanchez-Moran E et al (2003) Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics 165:1533–1540

    CAS  PubMed  Google Scholar 

  76. Schranz ME, Osborn TC (2000) Novel flowering time variation in the resynthesized polyploid Brassica napus. J Hered 91:242–246

    CAS  Article  PubMed  Google Scholar 

  77. Shiga I, Uno Y, Kanechi M et al (2009) Identification of polyploidy of in vitro anther-derived shoots of Asparagus officinalis L. by flow cytometric analysis and measurement of stomatal length. J Jpn Soc Hort Sci 78:103–108

    Article  Google Scholar 

  78. Shin JH, Van K, Kim DH et al (2008) The lipoxygenase gene family: a genomic fossil of shared polyploidy between Glycine max and Medicago truncatula. BMC Plant Biol 8:133

    Article  PubMed  Google Scholar 

  79. Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588

    CAS  Article  PubMed  Google Scholar 

  80. Soltis DE, Soltis PS, Pires JC et al (2004) Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biol J Linn Soc 82:485–501

    Article  Google Scholar 

  81. Soltis DE, Albert VA, Leebens-Mack J et al (2009) Polyploidy and angiosperm diversification. Am J Bot 96:336–348

    Article  Google Scholar 

  82. Song K, Lu P, Tang K et al (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Natl Acad Sci USA 92:7719–7723

    CAS  Article  PubMed  Google Scholar 

  83. Stuessy T, Weiss-Schneeweiss H, Keil D (2004) Diploid and polyploid cytotype distribution in Melampodium cinereum and M. leucanthum (Asteraceae, Heliantheae). Am J Bot 91:889–898

    Article  Google Scholar 

  84. Stupar RM, Bhaskar PB, Yandell BS et al (2007) Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176:2055–2067

    CAS  Article  PubMed  Google Scholar 

  85. Thomas BC, Pedersen B, Freeling M (2006) Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res 16:934–946

    CAS  Article  PubMed  Google Scholar 

  86. Town CD, Cheung F, Maiti R et al (2006) Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18:1348–1359

    CAS  Article  PubMed  Google Scholar 

  87. Trick M, Long Y, Meng JL et al (2009) Single nucleotide polymorphism (SNP) discovery in the polyploid Brassica napus using Solexa transcriptome sequencing. Plant Biotechnol J 7:334–346

    CAS  Article  PubMed  Google Scholar 

  88. Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr & Gray). Science 313:1596–1604

    CAS  Article  PubMed  Google Scholar 

  89. Udall JA, Swanson JM, Nettleton D et al (2006) A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173:1823–1827

    CAS  Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  91. Verhoeven KJF, Van Dijk PJ, Biere A (2010) Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages. Mol Ecol 19:315–324

    CAS  Article  PubMed  Google Scholar 

  92. Wang BS, Ding ZY, Liu W et al (2009) Polyploid evolution in Oryza officinalis complex of the genus Oryza. BMC Evol Biol 9:250

    CAS  Article  PubMed  Google Scholar 

  93. Wood TE, Takebayashi N, Barker MS et al (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106:13875–13879

    CAS  Article  PubMed  Google Scholar 

  94. Yang XH, Tuskan GA, Cheng ZM (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142:820–830

    CAS  Article  PubMed  Google Scholar 

  95. Yang XH, Kalluri UC, DiFazio SP et al (2009) Poplar genomics: State of the science. Crit Rev Plant Sci 28:285–308

    CAS  Article  Google Scholar 

  96. Zhu JK (2008) Reconstituting plant miRNA biogenesis. Proc Natl Acad Sci USA 105:9851–9852

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgment

The writing of this review was supported by the U.S. DOE Office of Biological and Environmental Research, Genomic Science Program, and the U.S. DOE BioEnergy Science Center. The BioEnergy Science Center is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the U.S. Department of Energy under Contract Number DE-AC05-00OR22725.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Xiaohan Yang.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Yang, X., Ye, CY., Cheng, ZM. et al. Genomic aspects of research involving polyploid plants. Plant Cell Tiss Organ Cult 104, 387–397 (2011). https://doi.org/10.1007/s11240-010-9826-1

Download citation

Keywords

  • Evolution
  • Genetics
  • Epigenetics