Review Article | Published:

Gene retention, fractionation and subgenome differences in polyploid plants

Nature Plantsvolume 4pages258268 (2018) | Download Citation


All natural plant species are evolved from ancient polyploids. Polyloidization plays an important role in plant genome evolution, species divergence and crop domestication. We review how the pattern of polyploidy within the plant phylogenetic tree has engendered hypotheses involving mass extinctions, lag-times following polyploidy, and epochs of asexuality. Polyploidization has happened repeatedly in plant evolution and, we conclude, is important for crop domestication. Once duplicated, the effect of purifying selection on any one duplicated gene is relaxed, permitting duplicate gene and regulatory element loss (fractionation). We review the general topic of fractionation, and how some gene categories are retained more than others. Several explanations, including neofunctionalization, subfunctionalization and gene product dosage balance, have been shown to influence gene content over time. For allopolyploids, genetic differences between parental lines immediately manifest as subgenome dominance in the wide-hybrid, and persist and propagate for tens of millions of years. While epigenetic modifications are certainly involved in genome dominance, it has been difficult to determine which came first, the chromatin marks being measured or gene expression. Data support the conclusion that genome dominance and heterosis are antagonistic and mechanically entangled; both happen immediately in the synthetic wide-cross hybrid. Also operating in this hybrid are mechanisms of ‘paralogue interference’. We present a foundation model to explain gene expression and vigour in a wide hybrid/new allotetraploid. This Review concludes that some mechanisms operate immediately at the wide-hybrid, and other mechanisms begin their operations later. Direct interaction of new paralogous genes, as measured using high-resolution chromatin conformation capture, should inform future research and single cell transcriptome sequencing should help achieve specificity while studying gene sub- and neo-functionalization.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


  1. 1.

    Salmanminkov, A., Sabath, N. & Mayrose, I. Whole-genome duplication as a key factor in crop domestication. Nat. Plants 2, 16115 (2016).

  2. 2.

    Murat, F., Armero, A., Pont, C., Klopp, C. & Salse, J. Reconstructing the genome of the most recent common ancestor of flowering plants. Nat. Genet. 49, 490–496 (2017).

  3. 3.

    Soltis, D. E., Visger, C. J. & Soltis, P. S. The polyploidy revolution then and now: Stebbins revisited. Am. J. Bot. 101, 1057–1078 (2014).

  4. 4.

    Salse, J. In silico archeogenomics unveils modern plant genome organisation, regulation and evolution. Curr. Opin. Plant Biol. 15, 122–130 (2012).

  5. 5.

    Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017).

  6. 6.

    Vanneste, K., Baele, G., Maere, S. & Van de Peer, Y. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous–Paleogene boundary. Genome Res. 24, 1334–1347 (2014).

  7. 7.

    Langham, R. J. et al. Genomic duplication, fractionation and the origin of regulatory novelty. Genetics 166, 935–945 (2004).

  8. 8.

    Freeling, M., Scanlon, M. J. & Fowler, J. E. Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences. Curr. Opin. Genet. Dev. 35, 110–118 (2015).

  9. 9.

    Lewis, E. B. Pseudoallelism and gene evolution. Cold Spring Harb. Sym. 16, 159–174 (1951).

  10. 10.

    Ohno, S. Evolution by Gene Duplication (Springer, Berlin, 1970).

  11. 11.

    Conant, G. C. & Wolfe, K. H. Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9, 938–950 (2008).

  12. 12.

    te Beest, M. et al. The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19–45 (2012).

  13. 13.

    Chao, D. Y. et al. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341, 658–659 (2013).

  14. 14.

    Wendel, J. F. The wondrous cycles of polyploidy in plants. Am. J. Bot. 102, 1753–1756 (2015).

  15. 15.

    Soltis, P. S., Marchant, D. B., Van de Peer, Y. & Soltis, D. E. Polyploidy and genome evolution in plants. Curr. Opin. Genet. Dev. 35, 119–125 (2015).

  16. 16.

    Shi, X., Zhang, C., Ko, D. K. & Chen, Z. J. Genome-wide dosage-dependent and -independent regulation contributes to gene expression and evolutionary novelty in plant polyploids. Mol. Biol. Evol. 32, 2351–2366 (2015).

  17. 17.

    Arsovski, A. A., Pradinuk, J., Guo, X. Q., Wang, S. & Adams, K. L. Evolution of cis-regulatory elements and regulatory networks in duplicated genes of Arabidopsis. Plant Physiol. 169, 2982–2991 (2015).

  18. 18.

    Barker, M. S., Husband, B. C. & Pires, J. C. Spreading Winge and flying high: the evolutionary importance of polyploidy after a century of study. Am. J. Bot. 103, 1139–1145 (2016).

  19. 19.

    Renny-Byfield, S., Rodgers-Melnick, E. & Ross-Ibarra, J. Gene fractionation and function in the ancient subgenomes of maize. Mol. Biol. Evol. 34, 1825–1832 (2017).

  20. 20.

    Schnable, J. C., Springer, N. M. & Freeling, M. Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc. Natl Acad. Sci. USA 108, 4069–4074 (2011).

  21. 21.

    Wang, M. et al. Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication. Nat. Genet. 49, 579–587 (2017).

  22. 22.

    Kondrashov, F. A. & Kondrashov, A. S. Role of selection in fixation of gene duplications. J. Theor. Biol. 239, 141–51 (2006).

  23. 23.

    Innan, H. & Kondrashov, F. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97–108 (2010).

  24. 24.

    Force, A. et al. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531–1545 (1999).

  25. 25.

    Lynch, M. & Force, A. The probability of duplicate gene preservation by subfunctionalization. Genetics 154, 459–473 (2000).

  26. 26.

    Stebbins, G. L. Polyploidy in plants: unsolved problems and prospects. Basic Life Sci. 13, 495–520 (1979).

  27. 27.

    Mayrose, I. et al. Methods for studying polyploid diversification and the dead end hypothesis: a reply to Soltis. et al. (2014). New Phytol. 206, 27–35 (2015).

  28. 28.

    Schranz, M. E., Mohammadin, S. & Edger, P. P. Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model. Curr. Opin. Plant. Biol. 15, 147–53 (2012).

  29. 29.

    Kellogg, E. A. Has the connection between polyploidy and diversification actually been tested? Curr. Opin. Plant Biol. 30, 25–32 (2016).

  30. 30.

    Lohaus, R. & Van de Peer, Y. Of dups and dinos: evolution at the K/Pg boundary. Curr. Opin. Plant Biol. 30, 62–69 (2016).

  31. 31.

    Lloyd, A. & Bomblies, K. Meiosis in autopolyploid and allopolyploid Arabidopsis. Curr. Opin. Plant Biol. 30, 116–122 (2016).

  32. 32.

    Freeling, M. The distribution of ancient polyploidies in the plant phylogenetic tree is a spandrel of occasional sex. Plant Cell 29, 202–206 (2017).

  33. 33.

    Gould, S. J. & Lewontin, R. C. The spandrels of San Marco and the panglossian paradigm: a critique of the adaptionist programme. P. Roy. Soc. Lond. B Bio. 205, 581–598 (1979).

  34. 34.

    Friedman, W. E. The meaning of Darwin’s ‘abominable mystery’. Am. J. Bot. 96, 5–21 (2009).

  35. 35.

    Conant, G. C., Birchler, J. A. & Pires, J. C. Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Curr. Opin. Plant Biol. 19, 91–98 (2014).

  36. 36.

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

  37. 37.

    De Smet, R. et al. Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc. Natl Acad. Sci. USA 110, 2898–903 (2013).

  38. 38.

    Duarte, J. M. et al. Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol. Biol. 10, 61 (2010).

  39. 39.

    Sémon, M. & Wolfe, K. H. Consequences of genome duplication. Curr. Opin. Gen. Dev. 17, 505–512 (2007).

  40. 40.

    Panchy, N., Lehti-Shiu, M. & Shiu, S. H. Evolution of gene duplication in plants. Plant Physiol. 171, 2294–2316 (2016).

  41. 41.

    Soltis, D. E., Visger, C. J., Marchant, D. B. & Soltis, P. S. Polyploidy: pitfalls and paths to a paradigm. Am. J. Bot. 103, 1146–1166 (2016).

  42. 42.

    Li, Z. et al. Gene duplicability of core genes is highly consistent across all angiosperms. Plant Cell 28, 326–344 (2016).

  43. 43.

    Rastogi, S. & Liberles, D. A. Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evol. Biol. 5, 28 (2005).

  44. 44.

    Birchler, J. A. & Veitia, R. A. The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19, 395–402 (2007).

  45. 45.

    Birchler, J. A. Parallel universes for models of X chromosome dosage compensation in Drosophila: a review. Cytogenet. Genome Res. 148, 52–67 (2016).

  46. 46.

    Blakeslee, A. F., Belling, J. & Farnham, M. E. Chromosomal duplication and Mendelian phenomena in Datura mutants. Science 52, 388–390 (1920).

  47. 47.

    Bridges, C. B. Haploidy in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 11, 706–710 (1925).

  48. 48.

    Jiang, W.-k, Liu, Y.-l, Xia, E.-h & Gao, L.-z Prevalent role of gene features in determining evolutionary fates of whole-genome duplication duplicated genes in flowering plants. Plant Physiol. 161, 1844–1861 (2013).

  49. 49.

    Chen, E. C., Morin, A., Chauchat, J. H. & Sankoff, D. Statistical analysis of fractionation resistance by functional category and expression level. BMC Genom. 18, 366 (2017).

  50. 50.

    Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151 (2000).

  51. 51.

    Teufel, A. I., Liu, L. & Liberles, D. A. Models for gene duplication when dosage balance works as a transition state to subsequent neo-or sub-functionalization. BMC Evol. Biol. 16, 1–8 (2016).

  52. 52.

    Lehti-Shiu, M., Panchy, N., Wang, P., Uygun, S. & Shiu, S. H. Diversity, expansion, and evolutionary novelty of plant DNA-binding transcription factor families. Biochim. Biophys. Acta 1860, 3–20 (2016).

  53. 53.

    Rody, H. V. S., Baute, G. J., Rieseberg, L. H. & Oliveira, L. O. Both mechanism and age of duplications contribute to biased gene retention patterns in plants. BMC Genom. 18, 46 (2017).

  54. 54.

    Freeling, M. & Thomas, B. C. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 16, 805–814 (2006).

  55. 55.

    Gout, J. F. & Lynch, M. Maintenance and loss of duplicated genes by dosage subfunctionalization. Mol. Biol. Evol. 32, 2141–2148 (2015).

  56. 56.

    Dickinson, H., Costa, L. & Gutierrez-Marcos, J. Epigenetic neofunctionalisation and regulatory gene evolution in grasses. Trends Plant Sci. 17, 389 (2012).

  57. 57.

    Zhang, X., Wang, L., Yuan, Y., Tian, D. & Yang, S. Rapid copy number expansion and recent recruitment of domains in S-receptor kinase-like genes contribute to the origin of self-incompatibility. FEBS J. 278, 4323–4337 (2011).

  58. 58.

    Cheng, F. et al. Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa. PLoS ONE 7, e36442 (2012).

  59. 59.

    Hughes, A. L. The evolution of functionally novel proteins after gene duplication. Proc. Biol. Sci. 256, 119–124 (1994).

  60. 60.

    Hittinger, C. T. & Carroll, S. B. Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449, 677–681 (2007).

  61. 61.

    Baker, C. R., Hanson-Smith, V. & Johnson, A. D. Following gene duplication, paralog interference constrains transcriptional circuit evolution. Science 342, 104–108 (2013).

  62. 62.

    Bergthorsson, U., Andersson, D. I. & Roth, J. R. Ohno’s dilemma: evolution of new genes under continuous selection. Proc. Natl Acad. Sci. USA 104, 17004–17009 (2007).

  63. 63.

    Francino, M. P. An adaptive radiation model for the origin of new gene functions. Nat. Genet. 37, 573–577 (2005).

  64. 64.

    Penn, D. J., Damjanovich, K. & Potts, W. K. MHC heterozygosity confers a selective advantage against multiple-strain infections. Proc. Natl Acad. Sci. USA 99, 11260–11264 (2002).

  65. 65.

    Van den Bergh, E., Hofberger, J. A. & Schranz, M. E. Flower power and the mustard bomb: comparative analysis of gene and genome duplications in glucosinolate biosynthetic pathway evolution in Cleomaceae and Brassicaceae. Am. J. Bot. 103, 1212–1222 (2016).

  66. 66.

    Hughes, T. E., Langdale, J. A. & Kelly, S. The impact of widespread regulatory neofunctionalization on homeolog gene evolution following whole-genome duplication in maize. Genome Res. 24, 1348–1355 (2014).

  67. 67.

    Muller, H. J. Further studies on the nature and causes of gene mutations. In Proc. 6th Int. Cong. Genet. (Ed. Jones, D. F.) 213–225 (Brooklyn Botanic Garden, Menasha, WI, 1932).

  68. 68.

    Lynch, M. & Katju, V. The altered evolutionary trajectories of gene duplicates. Trends Genet. 20, 544–549 (2004).

  69. 69.

    Lercher, M. J., Blumenthal, T. & Hurst, L. D. Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes. Genome Res. 13, 238–243 (2003).

  70. 70.

    Eichenlaub, M. P. & Ettwiller, L. De novo genesis of enhancers in vertebrates. PLoS Biol. 9, e1001188 (2011).

  71. 71.

    Emera, D., Yin, J., Reilly, S. K., Gockley, J. & Noonan, J. P. Origin and evolution of developmental enhancers in the mammalian neocortex. Proc. Natl Acad. Sci. USA 113, 2617–2626 (2016).

  72. 72.

    Haldane, J. B. S. The part played by recurrent mutation in evolution. Am. Nat. 67, 5–19 (1933).

  73. 73.

    Li, L. et al. Co-expression network analysis of duplicate genes in maize (Zea mays L.) reveals no subgenome bias. BMC Genom. 17, 875 (2016).

  74. 74.

    Renny-Byfield, S., Gong, L., Gallagher, J. P. & Wendel, J. F. Persistence of subgenomes in paleopolyploid cotton after 60 my of evolution. Mol. Biol. Evol. 32, 1063–1071 (2015).

  75. 75.

    Edger, P. P. et al. Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140-year-old naturally established neo-allopolyploid monkeyflower. Plant Cell 29, 2150–2167 (2017).

  76. 76.

    Zhang, J. et al. Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression. Proc. Natl Acad. Sci. 112, 7022–7029 (2015).

  77. 77.

    Sattler, M., Carvalho, C. & Clarindo, W. The polyploidy and its key role in plant breeding. Planta 243, 281–296 (2016).

  78. 78.

    Yant, L. & Bomblies, K. Genome management and mismanagement: cell-level opportunities and challenges of whole-genome duplication. Genes Dev. 29, 2405–2419 (2015).

  79. 79.

    Spofford, J. B. Heterosis and the evolution of duplications. Am. Nat. 103, 407–432 (1969).

  80. 80.

    Proulx, S. R. & Phillips, P. C. Allelic divergence precedes and promotes gene duplication. Evolution 60, 881–892 (2006).

  81. 81.

    Birchler, J. A., Yao, H., Chudalayandi, S., Vaiman, D. & Veitia, R. A. Heterosis. Plant Cell 22, 2105–2112 (2010).

  82. 82.

    Herbst, R. H. et al. Heterosis as a consequence of regulatory incompatibility. BMC Biol. 15, 38 (2017).

  83. 83.

    Steige, K. A. & Slotte, T. Genomic legacies of the progenitors and the evolutionary consequences of allopolyploidy. Curr. Opin. Plant Biol. 30, 88–93 (2016).

  84. 84.

    Schnable, J. C. & Freeling, M. Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize. PLoS ONE 6, e17855 (2011).

  85. 85.

    Murat, F. et al. Shared subgenome dominance following polyploidization explains grass genome evolutionary plasticity from a seven protochromosome ancestor with 16K protogenes. Genome Biol. Evol. 6, 12–33 (2013).

  86. 86.

    Garsmeur, O. et al. Two evolutionarily distinct classes of paleopolyploidy. Mol. Biol. Evol. 31, 448–454 (2014).

  87. 87.

    Gill, N. et al. Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol. 151, 1167–1174 (2009).

  88. 88.

    Sun, H. et al. Karyotype stability and unbiased fractionation in the paleo-allotetraploid cucurbita genomes. Mol. Plant 10, 1293–1306 (2017).

  89. 89.

    Cheng, F. et al. Epigenetic regulation of subgenome dominance following whole genome triplication in Brassica rapa. New Phytol. 211, 288–299 (2016).

  90. 90.

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

  91. 91.

    Mei, W. et al. A comprehensive analysis of alternative splicing in paleopolyploid maize. Front. Plant Sci. 10, 694 (2017).

  92. 92.

    Springer, N. M., Lisch, D. & Li, Q. Creating order from chaos: epigenome dynamics in plants with complex genomes. Plant Cell 28, 314–325 (2016).

  93. 93.

    Hollister, J. D. & Gaut, B. S. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 19, 1419–1428 (2009).

  94. 94.

    Woodhouse, M. R. et al. Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids. Proc. Natl Acad. Sci. USA 111, 5283–5288 (2014).

  95. 95.

    Pophaly, S. D. & Tellier, A. Population level purifying selection and gene expression shape subgenome evolution in maize. Mol. Biol. Evol. 32, 3226–3235 (2015).

  96. 96.

    Wendel, J. F., Lisch, D., Hu, G. & Mason, A. S. The long and short of doubling down: polyploidy, epigenetics, and the temporal dynamics of genome fractionation. Curr. Opin. Genet. Dev. 49, 1–7 (2018).

  97. 97.

    Talbert, P. B. & Henikoff, S. Spreading of silent chromatin: inaction at a distance. Nat. Rev. Genet. 7, 793–803 (2006).

  98. 98.

    Eichten, S. R. et al. Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet. 8, e1003127 (2012).

  99. 99.

    Buggs, R. J. et al. Tissue-specific silencing of homoeologs in natural populations of the recent allopolyploid Tragopogon mirus. New Phytol. 186, 175–183 (2010).

  100. 100.

    Li, A. et al. mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26, 1878–1900 (2014).

  101. 101.

    Vallejo-Marin, M. et al. Strongly asymmetric hybridization barriers shape the origin of a new polyploid species and its hybrid ancestor. Am. J. Bot. 103, 1272–1288 (2016).

  102. 102.

    Yoo, M. J., Szadkowski, E. & Wendel, J. F. Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110, 171–180 (2013).

  103. 103.

    Freeling, M. et al. Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants. Curr. Opin. Plant Biol. 15, 131–139 (2012).

  104. 104.

    Darwin, C. The effects of cross and self-fertilization in the vegetable kingdom (John Murray, London, 1876).

  105. 105.

    Davenport, C. B. Degeneration, albinism and inbreeding. Science 28, 454–455 (1908).

  106. 106.

    Groszmann, M. et al. Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc. Natl Acad. Sci. USA 108, 2617–2622 (2011).

  107. 107.

    Kawanabe, T. et al. Role of DNA methylation in hybrid vigor in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 113, 6704–6711 (2016).

  108. 108.

    Zhang, Q. et al. Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation. Proc. Natl Acad. Sci. USA 113, 4248–4256 (2016).

  109. 109.

    Rowley, M. J., Rothi, M. H., Bohmdorfer, G., Kucinski, J. & Wierzbicki, A. T. Long-range control of gene expression via RNA-directed DNA methylation. PLoS Genet. 13, e1006749 (2017).

  110. 110.

    Rosa, S. et al. Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization. Genes Dev. 27, 1845–1850 (2013).

  111. 111.

    Liu, C. et al. Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res. 26, 1057–1068 (2016).

  112. 112.

    Grob, S. & Grossniklaus, U. Chromosome conformation capture-based studies reveal novel features of plant nuclear architecture. Curr. Opin. Plant Biol. 36, 149–157 (2017).

  113. 113.

    Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289–293 (2009).

  114. 114.

    Feng, S. et al. Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol. Cell 55, 694–707 (2014).

  115. 115.

    Han, J. et al. A and D genomes spatial separation at somatic metaphase in tetraploid cotton: evidence for genomic disposition in a polyploid plant. Plant J. 84, 1167–177 (2015).

  116. 116.

    Wills, Q. F. et al. Single-cell gene expression analysis reveals genetic associations masked in whole-tissue experiments. Nat. Biotechnol. 31, 748–752 (2013).

  117. 117.

    Jaitin, D. A. et al. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 343, 776–779 (2014).

  118. 118.

    Macosko, E. Z. et al. Highly Parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161, 1202–1214 (2015).

  119. 119.

    Pollen, A. A. et al. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat. Biotechnol. 32, 1053–1058 (2014).

  120. 120.

    Zheng, G. X. et al. Massively parallel digital transcriptional profiling of single cells. Nat. Commun. 8, 14049 (2017).

  121. 121.

    Coate, J. E., Song, M. J., Bombarely, A. & Doyle, J. J. Expression‐level support for gene dosage sensitivity in three glycine subgenus glycine polyploids and their diploid progenitors. New Phytol. 212, 1083–1093 (2016).

  122. 122.

    Birchler, J. A. & Veitia, R. A. Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc. Natl Acad. Sci. USA 109, 14746–14753 (2012).

  123. 123.

    Fawcett, J. A., Maere, S. & Van de Peer, Y. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl Acad. Sci. USA 106, 5737–5742 (2009).

  124. 124.

    Ruprecht, C. et al. Revisiting ancestral polyploidy in plants. Sci. Adv. 3, e1603195 (2017).

  125. 125.

    Joint Genome Institute. Phytozome. US Department of Energy;

  126. 126.

    CoGepedia (Comparative Genomics, 2015);

  127. 127.

    Li, Y., Varala, K., Moose, S. P. & Hudson, M. E. The inheritance pattern of 24 nt siRNA clusters in Arabidopsis hybrids is influenced by proximity to transposable elements. PLoS ONE 7, e47043 (2012).

Download references


The Chinese authors are supported by the National Program on Key Research Project (2016YFD0100307), the National Natural Science Foundation of China (NSFC grants 31630068 and 31722048), the Prospect of Shandong Seed Project (Shandong Government, 2015, reference no. 212), the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences, and the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, P.R. China. MF’s support is from the National Science Foundation, USA, Plant Genome Research Program grant IOS-1546825 to R. Mosher and team.

Author information


  1. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops of the Ministry of Agriculture, Sino-Dutch Joint Laboratory of Horticultural Genomics, Beijing, China

    • Feng Cheng
    • , Jian Wu
    • , Xu Cai
    • , Jianli Liang
    •  & Xiaowu Wang
  2. Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA

    • Michael Freeling
  3. Shandong Provincial Key Laboratory of Protected Vegetable Molecular Breeding, Shandong Shouguang Vegetable Seed Industry Group Co. Ltd., Shandong Province, China

    • Xiaowu Wang


  1. Search for Feng Cheng in:

  2. Search for Jian Wu in:

  3. Search for Xu Cai in:

  4. Search for Jianli Liang in:

  5. Search for Michael Freeling in:

  6. Search for Xiaowu Wang in:

Competing interests

The authors declare no competing interests

Corresponding authors

Correspondence to Michael Freeling or Xiaowu Wang.

About this article

Publication history




Issue Date


Further reading