The Early Stages of Polyploidy: Rapid and Repeated Evolution in Tragopogon

  • Douglas E. Soltis
  • Richard J. A. Buggs
  • W. Brad Barbazuk
  • Srikar Chamala
  • Michael Chester
  • Joseph P. Gallagher
  • Patrick S. Schnable
  • Pamela S. Soltis
Chapter

Abstract

Elucidating the causes and consequences of polyploidy (whole-genome duplication; WGD) is arguably central to understanding the evolution of most eukaryotic lineages. However, much of what we know about these processes is derived from the study of crops and synthetic polyploids. Tragopogon provides the unique opportunity to investigate the genetic and genomic changes that occur across an evolutionary series from F1 hybrids, synthetic allopolyploids, independently formed natural populations of T. mirus and T. miscellus that are 60–80 years post-formation, to older Eurasian polyploids that are dated by molecular clocks at several million years old, and finally to a putative ancient polyploidization thought to have occurred prior to or early in the history of the Asteraceae (40–43 mya). Tragopogon joins other well-studied natural polyploid systems (e.g., Glycine, Nicotiana, Gossypium, Spartina, Senecio), but presents a range of research possibilities that is not available in any other system. We have shown in T. mirus and T. miscellus that upon allopolyploidization, massive gene loss occurs in patterns that are repeated across populations of independent origin and with a bias against genes derived from T. dubius, the diploid parent shared by both new allotetraploids. We have also shown significant changes in gene expression (transcriptomic shock) in the early generations of allopolyploidy in these species. Massive and repeated patterns of chromosomal variation (intergenomic translocations and aneuploidy) have been revealed by fluorescence in situ hybridization. Aneuploidy results in substitutions between homeologous chromosomes, through reciprocal monosomy-trisomy (1:3 copies) or nullisomy-tetrasomy (0:4 copies). We propose that substantial chromosomal instability results in karyotype restructuring, a likely common process following WGD and a driver of allopolyploid speciation, which has largely unexplored implications for gene losses, gains, and expression patterns. But gene loss and expression changes as well as karyotypic changes are ongoing in T. mirus and T. miscellus, in that no population is fixed for any of these events; thus, we have literally caught evolution in the act.

References

  1. Abbott RJ, Ireland HE, Rogers HJ (2007) Population decline despite high genetic diversity in the new allopolyploid species Senecio cambrensis (Asteraceae). Mol Ecol 16:1023–1033PubMedGoogle Scholar
  2. Abbott RJ, Lowe AJ (2004) Origins, establishment, and evolution of new polyploids species: Senecio cambrensis and S. eboracensis in the British Isles. Biol J Linn Soc 82:467–474Google Scholar
  3. Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Nat Acad Sci USA 100:4649–4654PubMedGoogle Scholar
  4. Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168:2217–2226PubMedGoogle Scholar
  5. Adams KL, Wendel JF (2004) Exploring the genomic mysteries of polyploidy in cotton. Biol J Linn Soc 82:573–581Google Scholar
  6. Ainouche ML, Baumel A, Salmon A (2004) Spartina anglia C. E. Hubbard: a natural model system for analyzing early evolutionary changes that affect allopolyploid genomes. Biol J Linn Soc 82:475–484Google Scholar
  7. Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien M-A, Ricou K, Fukunaga M, Misset M-T (2009) Hybridization, polyploidy and invasion: Lessons from Spartina (Poaceae). Biol Invasion. doi:10.1007s10530-0089383-2 Google Scholar
  8. Ashton PA, Abbott RJ (1992) Multiple origins and genetic diversity in the newly arisen allopolyploid species Senecio cambrensis Rosser (Compositae). Heredity 68:25–32Google Scholar
  9. Barker MS, Kane NC, Matvienko M, Kozik A, Michelmore RW, Knapp SJ, Rieseberg LH (2008) Multiple Paleopolyploidizations during the evolution of the compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol Biol Evol 25:2445–2455PubMedGoogle Scholar
  10. Birchler JA, Riddle NC, Auger DL, Veitia R (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21:219–226PubMedGoogle Scholar
  11. Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis divergence. Plant Cell 16:1679–1691PubMedGoogle Scholar
  12. Blanca G, Díaz de la Guardia C (1996) Sinopsis del género Tragopogon L. (Asteraceae) en la Peninsula Ibérica. Anales del Jardín Botánico de Madrid 54:358–363Google Scholar
  13. Buggs RJA, Doust AN, Tate JA, Koh J, Soltis K, Feltus FA, Paterson AH, Soltis PS, Soltis DE (2009) Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity 103:73–81PubMedGoogle Scholar
  14. Buggs RJA, Chamala S, Wu W, Gao L, May GD, Schnable PS, Soltis DE, Soltis PS, Barbazuk WB (2010a) Characterization of duplicate gene evolution in the recent natural allopolyploid Tragopogon miscellus by next-generation sequencing and Sequenom iPLEX genotyping. Mol Ecol 19(1):1–15Google Scholar
  15. Buggs RJA, Elliott NM, Zhang L, Koh J, Viccini LF, Soltis DE, Soltis PS (2010b) Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. New Phytol 186:175–183PubMedGoogle Scholar
  16. Buggs RJA, Soltis PS, Soltis DE (2011a) Biosystematic relationships and the formation of polyploids. Taxon 60:324–332Google Scholar
  17. Buggs RJA, Zhang L, Miles N, Tate JA, Gao L, Schnable PS, Barbazuk WB, Soltis PS, Soltis DE (2011b) Genomic and transcriptomic shock generate evolutionary novelty in a newly formed, natural allopolyploid plant. Curr Biol 21:1–6Google Scholar
  18. Buggs RJA, Gao L, Wu W, Chamala S, Tate JA, Schnable PS, Soltis DE, Soltis PS, Barbazuk WB (2012) Rapid and repeated gene loss in a young polyploidy species. Curr Biol 22:248–252PubMedGoogle Scholar
  19. Chaudhary B, Flagel L, Stupar RM, Udall JA, Verma N, Springer NM, Wendel JF (2009) Reciprocal silencing, transcriptional bias and functional divergence of homoeologs in polyploid cotton (Gossypium). Genetics 182:503–517PubMedGoogle Scholar
  20. Chelaifa H, Mahe F, Ainouche M (2010a) Transcriptome divergence between the hexaploid salt-marsh sister species Spartina maritima and Spartina alterniflora (Poaceae). Mol Ecol 19:2050–2063PubMedGoogle Scholar
  21. Chelaifa H, Monnier A, Ainouche M (2010b) Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina x townsendii and Spartina anglica (Poaceae). New Phytol 186:161–174PubMedGoogle Scholar
  22. Chen ZJ, Wang J, Tian L, Lee HS, Wang JJ, Chen M, Lee JJ, Josefsson C, Madlung A, Watson B, Pires JC, Lippman Z, Vaughn M, Colot V, Birchler JA, Doerge RW, Martienssen RA, Comai L, Osborn TC (2004) The development of an Arabidopsis model system for genome-wide analysis of polyploidy effects. Biol J Linn Soc 82:689–700Google Scholar
  23. Chester M, Gallagher JP, Symonds VV, da Veruska Cruz Silva A, Mavrodiev EV, Leitch AR, Soltis PS, Soltis DE (2012) Extensive and repeated patterns of chromosomal variation in natural populations of a recently formed polyploid plant species. Proc Nat Acad Sci USA 109:1176–1181PubMedGoogle Scholar
  24. Clausen J, Keck DD, Hiesey WM. 1945. Experimental studies on the nature of species II. Plant evolution through amphiploidy and autopolyploidy, with examples from the Madiinae. Publication 564, Carnegie Institute of Washington, Washington, DCGoogle Scholar
  25. Crisp PC (1972) Cytotaxonomic studies in the section Annui of Senecio. Ph. D Thesis, University of LondonGoogle Scholar
  26. Darlington CD (1937) Recent advances in cytology, 2nd edn. The Blakiston Company, PhiladelphiaGoogle Scholar
  27. Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, Leebens-Mack J, Ma H, Altman N, dePamphilis CW (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23:469–478PubMedGoogle Scholar
  28. Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I, De Montigny J, Marck C, Neuvéglise C, Talla E et al (2004) Genome evolution in yeasts. Nature 430:35–44PubMedGoogle Scholar
  29. Flagel L, Udall J, Nettleton D, Wendel J (2008) Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6:11Google Scholar
  30. Flagel LE, Wendel JF (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression during allotetraploid cotton speciation. New Phytol 186:184–193PubMedGoogle Scholar
  31. Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453PubMedGoogle Scholar
  32. Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814PubMedGoogle Scholar
  33. Gaeta RT, Pires JC (2010) Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol 186:18–28PubMedGoogle Scholar
  34. Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19:3403–3417PubMedGoogle Scholar
  35. Ganko EW, Meyers BC, Vision TJ (2007) Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 24:2298–2309PubMedGoogle Scholar
  36. Gould SJ (1994) The evolution of life on Earth. Sci Am 271:85–86Google Scholar
  37. Gregory TR, Mable BK (2005) Polyploidy in animals. In: Gregory TR (ed) The evolution of the Genome. Elsevier/Academic, San Diego, pp 428–501Google Scholar
  38. Hegarty MJ, Jones JM, Wilson ID, Barker GL, Coghill JA, Sanchez-Baracaldo P, Liu G, Buggs RJA, Abbott RJ, Edwards KJ, Hiscock SJ (2005) Development of anonymous cDNA microarrays to study changes to the Senecio floral transcriptome during hybrid speciation. Mol Ecol 14:2493–2510PubMedGoogle Scholar
  39. Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ (2006) Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16:1652–1659PubMedGoogle Scholar
  40. Hegarty MJ, Barker GL, Brennan AC, Edwards KJ, Abbott RJ, Hiscock SJ (2008) Changes to gene expression associated with hybrid speciation in plants: further insights from transcriptomic studies in Senecio. Philos Trans R Soc London B series 363:3055–3069Google Scholar
  41. Hegarty MJ, Batstone T, Barker GL, Edwards KJ, Abbott RJ, Hiscock SJ (2011) Nonadditive changes to cytosine methylation as a consequence of hybridization and genome duplication in Senecio (Asteraceae). Mol Ecol 20:105–113PubMedGoogle Scholar
  42. Hovav R, Udall J, Chaudhary B, Flagel L, Rapp R, Wendel J (2008a) Partitioned expression of duplicated genes during development and evolution of a single cell in a polyploid plant. Proc Nat Acad Sci USA 105:6191Google Scholar
  43. Hovav R, Udall JA, Chaudhary B, Hovav E, Flagel L, Hu G, Wendel JF (2008b) The evolution of spinnable cotton fiber entailed prolonged development and a novel metabolism. PLoS Genet 4:e2Google Scholar
  44. Jiao Y, Wickett N, Ayyampalayam S, Chanderbali A, Landherr L, Ralph PE, Soltis PS, Soltis DE, Clifton SE, Ma H, Leebens-Mack J, dePamphilis CW (2011) Phylogenomic analysis reveals ancient genome duplications in seed plant and angiosperm history. Nature 473:97–100PubMedGoogle Scholar
  45. Jurinke C, Denissenko MF, Oeth P, Ehrich M, van den Boom D, Cantor CR (2005) A single nucleotide polymorphism based approach for the identification and characterization of gene expression modulation using MassARRAY. Mutat Res 573:83–95PubMedGoogle Scholar
  46. Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing, and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659PubMedGoogle Scholar
  47. Kellis M, Birren BW, Lander ES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428:617–624PubMedGoogle Scholar
  48. Koh J, Tate JA, Soltis PS, Soltis DE (2010) Genomic and expression differences in natural populations of the recently formed allotetraploid Tragopogon mirus (Asteraceae). BMC Genomics 11:97PubMedGoogle Scholar
  49. Kovarik A, Pires JC, Leitch AR, Lim KY, Sherwood A, Matyasek R, Rocca J, Soltis DE, Soltis PS (2005) Rapid concerted evolution in two allopolyploids of recent and recurrent origin. Genetics 169:931–944PubMedGoogle Scholar
  50. Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122:1–25Google Scholar
  51. Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, New YorkGoogle Scholar
  52. Lim KY, Soltis DE, Soltis PS, Tate JA, Matyasek R, Srubarova H, Kovarik A, Pires JC, Xiong ZY, Leitch AR (2008) Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae). PLoS One 3:e3353PubMedGoogle Scholar
  53. Löve A, Löve D (1949) The geobotanical significance of polyploidy. I. Polyploidy and latitude. Portugaliae Acta Biologica Serie A, Suppl vol. pp 273–352Google Scholar
  54. Lynch M, Connery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155PubMedGoogle Scholar
  55. Ma XF, Fang P, Gustafson JP (2004) Polyploidization-induced genome variation in Triticale. Genome 47:839–848PubMedGoogle Scholar
  56. Ma XF, Fang P, Gustafson JP (2006) Timing and rate of genome variation in Triticale following allopolyploidization. Genome 49:950–958PubMedGoogle Scholar
  57. Mable B (2003) Breaking down taxonomic barriers in polyploidy research. Trends Plant Sci 8:582–590PubMedGoogle Scholar
  58. Mable BK, Alexandrou MA, Taylor MI (2011) Genome duplications in amphibians and fish: an extended synthesis. J Zool 284:151–182Google Scholar
  59. Madlung A, Comai L (2004) The effect of stress on genome regulation and structure. Ann Bot 94:481 495PubMedGoogle Scholar
  60. Malinska H, Tate JA, Matyasek R, Leitch AR, Soltis DE, Soltis PS, Kovarik A (2010) Similar patterns of rDNA evolution in synthetic and recently formed natural populations of Tragopogon (Asteraceae) allotetraploids. BMC Evol Biol 10:291PubMedGoogle Scholar
  61. Malinska H, Tate JA, Mavrodiev E, Matyasek R, Lim KY, Leitch AR, Soltis DE, Soltis PS, Kovarik A (2011) Ribosomal RNA genes evolution in Tragopogon: A story of New and Old World allotetraploids and synthetic lines. Taxon 60:348–354Google Scholar
  62. Matyasek R, Tate J, Lim YK, Srubaraova H, Koh J, Leitch A, Soltis DE, Soltis PS (2007) Concerted evolution of rDNA in recently formed Tragopogon allotetraploids is typically associated with an inverse correlation between gene copy number and expression. Genetics 176:2509–2519PubMedGoogle Scholar
  63. Mavrodiev E, Soltis PS, Soltis DE (2008a) Parentage of six Old World polyploids in Tragopogon L. (Asteraceae: Scorzonerinae) based on ITS. ETS and plastid sequence data. Taxon 57:1217–1232Google Scholar
  64. Mavrodiev E, Nawchoo I, Soltis DE, Soltis PS (2008b) Molecular data reveal that the tetraploid Tragopogon kashmirianus Singh, a narrow endemic of Kashmir, is distinct from the North American T. mirus M. Ownbey. Bot J Linn Soc 158:391–398Google Scholar
  65. Mavrodiev EV, Albach DC, Speranza P (2008c) A new polyploid species of the genus Tragopogon (Asteraceae, Cichorieae) from Russia. Novon 18:229–232Google Scholar
  66. McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801PubMedGoogle Scholar
  67. Morris SC (1998) The crucible of creation: the Burgess shale and the rise of animals. Oxford University Press, OxfordGoogle Scholar
  68. Müntzing A (1936) The evolutionary significance of autopolyploidy. Hereditas 21:263–378Google Scholar
  69. Novak SJ, Soltis DE, Soltis PS (1991) Ownbey Tragopogons—40 Years later. Am J Bot 78:1586–1600Google Scholar
  70. Ohno S (1970) Evolution by gene duplication. Springer, BerlinGoogle Scholar
  71. Ownbey M (1950) Natural hybridization and amphiploidy in the genus Tragopogon. Am J Bot 37:487–499Google Scholar
  72. Ownbey M, McCollum G (1954) The chromosomes of Tragopogon. Rhodora 56:7–21Google Scholar
  73. Ownbey M, McCollum GD (1953) Cytoplasmic inheritance and reciprocal amphiploidy in Tragopogon. Am J Bot 40:788–796Google Scholar
  74. Panopoulou G, Poustka AJ (2005) Timing and mechanism of ancient vertebrate genome duplications—the adventure of a hypothesis. Trends Genet 10:559–567Google Scholar
  75. Papp B, Pal C, Hurst LD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424:194–197PubMedGoogle Scholar
  76. Parisod C, Salmon A, Zerjal T, Tenaillon M, Grandbastien M-A, Ainouche M (2009) Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytol 184:1003–1015PubMedGoogle Scholar
  77. Paterson AH, Chapman BA, Kissinger J, Bowers JE, Feltus FA, Estill JC, Marler BS (2006) Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. Trends Genet 22:597–602PubMedGoogle Scholar
  78. Petit RJ, Aguinagalde, JL de Beaulieu, C Bittkau, S Brewer, R Cheddadi, R Ennos, S Fineschi, D Grivet, M Lascoux, A Mohanty, G Müller-Starck, B Musch, A Palmé, S Rendell, GG. Vendramin (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565Google Scholar
  79. Ramsey J (2011) Polyploidy and ecological adaptation in wild yarrow. Proc Nat Acad Sci USA 108:6697–6698Google Scholar
  80. Rapp RA, Udall JA, Wendel JF (2009) Genomic expression dominance in allopolyploids. BMC Biol. 7:18PubMedGoogle Scholar
  81. Renny-Byfield S, Ainouche M, Leitch IJ, Lim KY, Le Comber SC, Leitch AR (2010) Flow cytometry and GISH reveal mixed ploidy populations and Spartina nonaploids with genomes of S. alterniflora and S. maritima origin. Ann Bot 105:527–533PubMedGoogle Scholar
  82. Rodin SN, Riggs AD (2003) Epigenetic silencing may aid evolution by gene duplication. J Mol Evol 56:718–729PubMedGoogle Scholar
  83. Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175PubMedGoogle Scholar
  84. Semon M, Wolfe KH (2008) Preferential subfunctionalization of slow-evolving genes after allopolyploidization in Xenopus laevis. Proc Nat Acad Sci USA 105:8333–8338PubMedGoogle Scholar
  85. Soltis DE, Soltis PS (1995) The dynamic nature of polyploid genomes. Proc Nat Acad Sci USA 92:8089–8091PubMedGoogle Scholar
  86. Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E (2004) Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biol J Linn Soc 82:485–501Google Scholar
  87. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson A, Zheng C, Sankoff D, Wall PK, Soltis PS (2009a) Polyploidy and angiosperm diversification. Am J Bot 96:336–348PubMedGoogle Scholar
  88. Soltis DE, Buggs RJA, Barbazuk WB, Schnable PS, Soltis PS (2009b) On the origins of species: does evolution repeat itself in polyploid populations of independent origin? Cold spring harbor symposia on quantitative biology, Vol. LXXIVGoogle Scholar
  89. Soltis DE, Mavrodiev EV, Meyers, SC, Severns PM, Zhang L, Gitzendanner MA, Ayers T, Chester M, Soltis PS (2012) Additional origins of Ownbey’s Tragopogon mirus. Bot Linn Soc 169:297–311 Google Scholar
  90. Soltis DE, Soltis PS (1989) Allopolyploid speciation in Tragopogon: Insights from chloroplast DNA. Am J Bot. 76:1119–1124Google Scholar
  91. Soltis DE, Soltis PS (1993) Molecular data and the dynamic nature of polyploidy. Crit Rev Plant Sci 12:243–273Google Scholar
  92. Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol 14:348–352PubMedGoogle Scholar
  93. Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proc Nat Acad Sci (USA) 97:7051–7057Google Scholar
  94. Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588PubMedGoogle Scholar
  95. Soltis PS, Plunkett GM, Novak SJ, Soltis DE (1995) Genetic variation in Tragopogon species: additional origins of the allotetraploids T. mirus and T. miscellus (Compositae). Am J Bot 82:1329–1341Google Scholar
  96. Song KM, Lu P, Tang KL, Osborn TC (1995) Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc Nat Acad Sci USA 92:7719–7723PubMedGoogle Scholar
  97. Stebbins GL (1950) Variation and evolution in plants. Columbia, New YorkGoogle Scholar
  98. Stebbins GL (1971) Chromosomal evolution in higher plants. Addison-Wesley, LondonGoogle Scholar
  99. Stern DL, Orgogozo V (2009) Is genetic evolution predictable? Science 323:746–751PubMedGoogle Scholar
  100. Symonds VV, Soltis PS, Soltis DE (2010) Dynamics of polyploid formation in Tragopogon (Asteraceae): recurrent formation, gene flow, and population structure. Evolution 64:1984–2003PubMedGoogle Scholar
  101. Szadkowski E, Eber F, Huteau V, Lod M, Huneau C, Belcram H, Coriton O, Manzanares-Dauleux M, Delourme R, King G (2010) The first meiosis of resynthesized Brassica napus, a genome blender. New Phytol 186:102–112PubMedGoogle Scholar
  102. Tate JA, Ni Z, Scheen AC, Koh J, Gilbert CA, Lefkowitz D, Chen ZJ, Soltis PS, Soltis DE (2006) Evolution and expression of homoeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173:1599–1611PubMedGoogle Scholar
  103. Tate JA, Symonds VV, Doust AN, Buggs RJA, Mavrodiev EV, Soltis PS, Soltis DE (2009a) Synthetic polyploids of Tragopogon miscellus and T. mirus (Asteraceae): 50 + years after Ownbey’s discovery. Am J Bot 96:979–988PubMedGoogle Scholar
  104. Tate JA, Joshi P, Soltis K, Soltis PS, Soltis DE (2009b) On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae). BMC Plant Biol 9:80PubMedGoogle Scholar
  105. Udall JA, Swanson JM, Nettleton D, Percifield RJ, Wendel JF (2006) A novel approach for characterizing expression levels of genes duplicated by polyploidy. Genetics 173(3):1823–1827PubMedGoogle Scholar
  106. Xiong Z, Gaeta RT, Pires JC (2011) Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc Nat Acad Sci USA 108:7908–7913PubMedGoogle Scholar
  107. Wang JL, Tian L, Madlung A, Lee HS, Chen M, Lee JJ, Watson B, Kagochi T, Comai L, Chen ZJ (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167:1961–1973PubMedGoogle Scholar
  108. Wang JL, Tian L, Lee HS, Wei NE, Jiang HM, Watson B, Madlung A, Osborn TC, Doerge RW, Comai L, Chen ZJ (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517PubMedGoogle Scholar
  109. Wolfe KH, Shields DC (1997) Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713PubMedGoogle Scholar
  110. Zimmer EA, Martin SL, Beverley SM, Kan YW, Wilson AC (1980) Rapid duplication and loss of genes coding for the ∂ chains of hemoglobin. Proc Nat Acad Sci USA 77:2158–2162PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Douglas E. Soltis
    • 1
  • Richard J. A. Buggs
    • 1
    • 3
  • W. Brad Barbazuk
    • 1
  • Srikar Chamala
    • 1
  • Michael Chester
    • 1
  • Joseph P. Gallagher
    • 1
    • 2
  • Patrick S. Schnable
    • 4
  • Pamela S. Soltis
    • 5
  1. 1.Department of BiologyUniversity of FloridaGainesvilleUSA
  2. 2.Department of Ecology, Evolution, and Organismal BiologyIowa State UniversityAmesUSA
  3. 3.School of Biological and Chemical Sciences, Queen Mary University of LondonLondonUK
  4. 4.Center for Plant Genomics, Iowa State UniversityAmesUSA
  5. 5.Florida Museum of Natural History, University of FloridaGainesvilleUSA

Personalised recommendations